the transcription machineries of plant mitochondria and chloroplasts

R

TC

KI

a

KCMPRR

C

spt

0d

Journal of Plant Physiology 168 (2011) 1345– 1360

Contents lists available at ScienceDirect

Journal of Plant Physiology

jou rn al h o mepage: www.elsev ier .de / jp lph

eview

he transcription machineries of plant mitochondria and chloroplasts:omposition, function, and regulation

arsten Liere, Andreas Weihe, Thomas Börner ∗

nstitut für Biologie/Genetik, Humboldt-Universität zu Berlin, Chausseestr. 117, 10115 Berlin, Germany

r t i c l e i n f o

eywords:hloroplast transcriptionitochondrial transcription

romoteregulation of transcriptionNA polymerase

s u m m a r y

Although genomes of mitochondria and plastids are very small compared to those of their bacterial ances-tors, the transcription machineries of these organelles are of surprising complexity. With respect to thenumber of different RNA polymerases per organelle, the extremes are represented on one hand by chloro-plasts of eudicots which use one bacterial-type RNA polymerase and two phage-type RNA polymerasesto transcribe their genes, and on the other hand by Physcomitrella possessing three mitochondrial RNA
polymerases of the phage type. Transcription of genes/operons is often driven by multiple promoters inboth organelles. This review describes the principle components of the transcription machineries (RNApolymerases, transcription factors, promoters) and the division of labor between the different RNA poly-merases. While regulation of transcription in mitochondria seems to be only of limited importance, theplastid genes of higher plants respond to exogenous and endogenous cues rather individually by alteringtheir transcriptional activities.
© 2011 Elsevier GmbH. All rights reserved.

ontents

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1346The transcription machinery of plant mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1346

Mitochondrial RNA polymerases are phage-type enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1346The function of RpoTm and RpoTmp in mitochondrial transcription . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1346Phage-type RNA polymerases require auxiliary factors for transcription initiation in vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1347Mitochondrial promoters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1348Multilevel regulation of mitochondrial gene expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1348

The transcriptional machinery of chloroplasts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1349Plastid RNA polymerases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1349

PEP: the plastid-encoded plastid RNA polymerase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1349NEP: the nuclear-encoded plastid RNA polymerase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1349

Plastid promoters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1350Conserved sequences and structures of PEP promoters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1350Conserved sequences and structures of NEP promoters and internal promoters of tRNA genes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1350

Division of labor between PEP and NEP . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1351Regulation of plastid transcription and transcription factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1352

Nuclear-encoded plastid sigma factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1352NEP transcription factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1352
Exogenous and endogenous factors affecting plastid transcrip
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Abbreviations: ABA, abscisic acid; BLRP, blue light responsive promoter; CMS, cytoplatrand promoter; LSP, light-strand promoter; mtTF, mitochondrial transcription factor;

olymerase; PQ, plastoquinone pool; PTK, plastid transcription kinase; R, purine (adeninype; RSH, RelA/SpoT homolog; TAC, transcriptionally active chromosome; UCR, unconse∗ Corresponding author. Tel.: +49 30 2093 8140; fax: +49 30 2093 8141.

E-mail address: [email protected] (T. Börner).

176-1617/$ – see front matter © 2011 Elsevier GmbH. All rights reserved.oi:10.1016/j.jplph.2011.01.005

tion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1353. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1355

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1355

smic male sterility; CR, conserved region; HMG, high mobility group; HSP, heavy-NEP, nuclear-encoded plastid RNA polymerase; PEP, plastid-encoded plastid RNAe or guanine); RNAP, RNA polymerase; RpoT, RNA polymerase of the T3/7-phage

rved region; Y, pyrimidine (thymine or cytosine).

dx.doi.org/10.1016/j.jplph.2011.01.005

http://www.sciencedirect.com/science/journal/01761617

http://www.elsevier.de/jplph

mailto:[email protected]

dx.doi.org/10.1016/j.jplph.2011.01.005

1 t Physiology 168 (2011) 1345– 1360

I

sosieftGasaM2Lopttp2meptpcp

T

M

pS2ica2maPd(c2RPHBttsaptptKma

Fig. 1. Evolution of phage-type RNA polymerases: a hypothetical scenario. Geneduplications and/or loss of genes occurred several times during evolution, givingrise to small RpoT gene families. Gene duplication(s) of the single RpoT gene ofgreen algae, encoding a mitochondrial RNAP, led to multiple organellar RNAPs inPhyscomitrella and, probably, other mosses which are localized mitochondrially ortargeted to both organelles. 1 and 2 designate alternative routes of evolution to thelycophytes, which, in the case of Selaginella, contain a single mitochondrial RNAP.Route 2 implicates losses of RpoT gene copies. Gene duplication events (routes 3 or4) resulted in two mitochondrial and one plastid-localized RNAP in Nuphar. Otherbasal angiosperms (N.n. ssp.) may contain only one mitochondrial and one plastidphage-type RNAP. Monocot and eudicot organellar RNAPs of higher plants arose byevolution from the basal angiosperm RpoT polymerases via alternative routes 5 or

346 K. Liere et al. / Journal of Plan

ntroduction

Mitochondria and plastids possess their own genomes and tran-cription machineries. Although both organelles preserve featuresf eubacterial genomes, they have acquired, during their evolution,pecialized components for gene expression, which are encodedn the nucleus. During the co-evolution of plastids (cyanobacterialndosymbiont) and the eukaryotic host cell massive losses of genesrom the chondrome (mitochondrial genome) and plastome (plas-id genome) have occurred (Martin et al., 2002; Dyall et al., 2004;ray, 2004, 2010; Knoop, 2004; Richly and Leister, 2004; Brandvainnd Wade, 2009). However, the cells did not lose all of those genes,ince thousands of them have been transferred to the nucleus, still

relatively frequent and ongoing process (Brennicke et al., 1993;artin and Herrmann, 1998; Palmer et al., 2000; Herrmann et al.,

003; Martin, 2003; Adams and Daley, 2004; Timmis et al., 2004;eister, 2005; Stegemann and Bock, 2006). A considerable numberf proteins encoded by those genes were rerouted back into thelastids/mitochondria by acquiring plastid and/or mitochondrialargeting sequences. In a similar way, many nuclear-encoded pro-eins of non-organellar origin also became part of the organellarroteome (eukaryotization; Sato, 2001; Hengeveld and Fedonkin,004). This eukaryotization is also reflected by the transcriptionalachineries of mitochondria and plastids in higher plants. Consid-

ring the small sizes of the chondromes and plastomes of higherlants compared to the genomes of their bacterial ancestors, theranscriptional machineries of mitochondria and even more oflastids are surprisingly complex. Here we describe the differentomponents of the transcriptional machinery in mitochondria andlastids and their roles in transcription and its regulation.

he transcription machinery of plant mitochondria

itochondrial RNA polymerases are phage-type enzymes

Mitochondrial transcription is performed by nuclear-encodedhage-type RNA polymerase(s) (RNAP(s); reviewed in Tracy andtern, 1995; Hess and Börner, 1999; Weihe, 2004; Liere and Börner,011). The protist Reclinomonas americana is the only known organ-

sm which has retained the ancestral bacterial RNAP genes in itshondrome (Lang et al., 1997). While most eukaryotes includinglso algae and the lycophyte Selaginella moellendorffii (Yin et al.,009) possess only one nuclear gene for a (in most or all casesitochondrial) phage-type RNA polymerase, phage-type RNAPs

re encoded by a small family of nuclear encoded RpoT genes inhyscomitrella and angiosperms (Figs. 1 and 2). Several indepen-ent duplications of the gene encoding the mitochondrial RNAPRpoTm) provided the basis for the evolution of a second mito-hondrial RNAP (in the basal angiosperm Nuphar advena; Yin et al.,010), of plastid RNAPs (RpoTp; probably all angiosperms) and ofNAPs, dual-targeted to both mitochondria and plastids (RpoTmp;hyscomitrella, eudicots; Hedtke et al., 1997, 2000; see reviews byess and Börner, 1999; Weihe, 2004; Shiina et al., 2005; Liere andörner, 2007b; Figs. 1 and 2). The amphidiploid genome of Nicotianaabacum harbors six RpoT genes with two sets of three genes fromhe two diploid parental species (Hedtke et al., 2002). Preliminaryequence data from the poplar genome project suggest that Populuslso contains more than one set of RpoT genes (http://genome.jgi-sf.org/Poptr1 1/Poptr1 1.home.html). Aside from dicots, two ofhe three RpoT polymerases identified in the moss Physcomitrellaatens have been demonstrated to contain bifunctional transit pep-
ides, i.e. should represent RpoTmp enzymes (Richter et al., 2002; cf.abeya and Sato, 2005). The third RpoT gene of the moss encodes aitochondrial RNAP (U. Richter, personal communication). RpoTp
nd RpoTmp represent the nuclear-encoded plastid RNA poly-

6, comprising duplication and/or losses of RpoT genes. Subcellular localization ofthe polymerases is color-coded: orange, mitochondrial; green, plastid; mixed color,dual-targeted.

merase, NEP (see NEP: the nuclear-encoded plastid RNA polymerase).The phylogenetically earliest plastid RpoTp (NEP) of higher plantswas identified, in addition to two phage-type mitochondrial RNAPs,in the waterlily Nuphar advena, a basal angiosperm (Yin et al., 2010).

The function of RpoTm and RpoTmp in mitochondrial transcription

Not much is known yet about potential division of labor betweenRpoTm and RpoTmp in mitochondrial transcription. The RpoTm andRpoTmp genes in Arabidopsis display overlapping expression pat-terns (Emanuel et al., 2006). Recent analyses of Arabidopsis RpoTmmutants showed that both RpoTm and RpoTmp are important forgametogenesis, but furthermore have distinct roles in plant devel-
opment (Tan et al., 2010). Analysis of an RpoTmp null mutantrevealed that the lack of RpoTmp resulted in induction of severalplastid genes in dark-grown seedlings upon illumination (Baba etal., 2004). Therefore it was suggested that RpoTmp was the key
http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.html

K. Liere et al. / Journal of Plant Physiology 168 (2011) 1345– 1360 1347

Fig. 2. Localization of organellar phage-type RNA polymerases in different organisms. Genes in the nucleus (N) of eukaryotic organisms code for T3/T7 phage-type RNApolymerases, which are imported into mitochondria (M) and plastids (P) as indicated by arrows. Green algae such as Chlamydomonas and the lycophyte Selaginella possess onlyone nuclear RpoT gene probably encoding the mitochondrial RNA polymerase (RpoTm). Nuclear genomes of cereals contain two RpoT genes, one encoding the mitochondrialRNA polymerase (RpoTm), the other a plastid RNA polymerase (RpoTp) representing NEP. Arabidopsis and other eudicots additionally acquired RpoTmp, which contributest sses tm o mito

edpl2dmoprmmnc

Pt

ursfaaatc2pftmcgase

o transcription in mitochondria and plastids. The moss Physcomitrella patens posseitochondria and plastids (RpoTmp1, RpoTmp2) and an enzyme solely dedicated t

nzyme transcribing plastid (and possibly mitochondrial) genesuring early seedling development, while RpoTm (and RpoTp inlastids) would take over transcription in their respective organelle

ater in development. According to a recent study (Kühn et al.,009), RpoTm has to be considered as the basic RNAP in mitochon-ria of eudicots required for the transcription of most, if not all,itochondrial genes. In the RpoTmp mutants, decreased amounts

f nad2, nad6 and cox1 transcripts and a lower abundance of the res-iratory chain complexes I and IV were found suggesting a specificole of RpoTmp for the formation of these complexes. Decreaseditochondrial transcription did not correlate with changes in pro-oter utilization of these genes. The recruitment of RpoTmp, and

ot of RpoTm seems to be dependent upon additional gene-specificis elements (Kühn et al., 2009).

hage-type RNA polymerases require auxiliary factors forranscription initiation in vivo

The yeast mitochondrial RNAP has recently been shown totilize, like the T7 polymerase, a C-terminal loop for promoterecognition (Nayak et al., 2009). The yeast enzyme may act as aingle-subunit RNAP and initiate transcription without accessoryactors, provided the promoter is supercoiled or modified to form

bubble around the initiation site to facilitate melting (Matsunagand Jaehning, 2004). Likewise, the Arabidopsis polymerases RpoTmnd RpoTp recognize a number of promoters, initiate transcrip-ion and perform elongation of the transcript without additionalo-factors in vitro on supercoiled, but not linear DNA (Kühn et al.,007). However, in contrast to the RNAPs of bacteriophages, thelant, animal or fungal RpoT polymerases require auxiliary factorsor accurate and efficient transcription initiation in vivo. Such fac-ors conferring promoter recognition, herein after referred to as

tTFA and mtTFB, have been identified in yeast and animal mito-hondria. In baker’s yeast, mtTFA binds DNA via two high mobility
roup (HMG) boxes. It plays a major role in structural organizationnd maintenance of the mtDNA. It stimulates, but is not neces-ary for transcription initiation (Diffley and Stillman, 1991; Fishert al., 1992; Xu and Clayton, 1992; Parisi et al., 1993). Mitochon-
hree RpoT genes encoding polymerases, two of which are dually targeted into bothchondria (RpoTm).

drial mtTFBs are related to a family of rRNA methyltransferaseswhich dimethylate two adenosines near the 3′ end of the rRNAin the small ribosomal subunit (Schubot et al., 2001; Park et al.,2009; Richter et al., 2010). Two yeast mtTFB homologs, mtTFB1 andmtTFB2 were identified in humans as well as in mice. Experimentaldata suggest that mtTFB1 functions in organello as a methyltrans-ferase, while mtTFB2 has evolved to act as a transcription factor(reviewed in Asin-Cayuela and Gustafsson, 2007; Scarpulla, 2008).Faithful transcription can be initiated from the human LSP andHSP1 promoters in vitro by the mitochondrial RNA polymerase andhuman mtTFB2 alone suggesting the core human mitochondrialtranscription apparatus is formed by these two components like inyeast (Shutt et al., 2010). Nonetheless, it is still a matter of debateif the human mtTFA represents a crucial factor of the human mito-chondrial transcription apparatus (Litonin et al., 2010; Shutt et al.,2010).

Homologs of mtTFB (and mtTFA) are potential candi-dates for mitochondrial specificity factors in plants. Severalmethyltransferase-like open reading frames were found in thecompletely sequenced genome of Arabidopsis. Mitochondrial tar-geting as well as methylation of the conserved adenosines in themitochondrial rRNA by the recombinant protein could be demon-strated experimentally for one of them (at5g66360). However,neither in vitro transcription assays nor analysis of a respectivemutant line did support a functional role of this protein in mito-chondrial transcription (Richter et al., 2010). In silico screening formitochondrial-localized HMG-box proteins in Arabidopsis did notreveal any mtTFA-homologs (Elo et al., 2003; Kühn et al., unpub-lished data). Thus, plant mitochondria seem not to use mtTFA andmtTFB homologs as transcription factors.

Potential specific co-factors of the mitochondrial RNAP wereidentified in mitochondrial lysates used for in vitro transcriptionassays. A 69-kDa protein from wheat stimulated transcription froma wheat cox2 promoter in vitro (Ikeda and Gray, 1999). This protein
shows not only similarities to regions 2 and 3 of bacterial sigma fac-tors and the yeast mtTFB, but is also a member of the family of PPRproteins which function in RNA metabolism (Schmitz-Linneweberand Small, 2008). Three homologous, mitochondrial-localized PPR

1 t Phys

pwaRuppd2b

flo1

Ad2mmsfR

M

st1nsaaBe1(psiWoescbpeBacps+Ab+ntwdCAl


roteins from Arabidopsis were analyzed in in vitro assays. Theyere shown to bind to mitochondrial promoter fragments only in

n unspecific manner and did not interact with RpoTm or withpoTmp to confer correct initiation of transcription (Kühn et al.,npublished data; Kühn et al., 2007). From pea mitochondria, tworoteins of 43 and 32 kDa were isolated that bound to the atp9romoter. The 43-kDa protein was highly similar to isovaleryl CoAehydrogenases involved in leucine catabolism (Däschner et al.,001). The identity and function of the 32-kDa protein remain toe investigated.

The product of Mct, a maize nuclear gene, is another candidateactor that might be involved in transcription initiation and regu-ation. It binds to the mitochondrial cox2 promoter, which is activenly in the presence of the dominant Mct allele (Newton et al.,995).

Interestingly, some nuclear-encoded plastid sigma factors, i.e.thSig5 (Fujiwara et al., 2000; Yao et al., 2003), AthSig1 (Tan-ara and Liere, unpublished data), and ZmaSig2B (Beardslee et al.,002) were found to additionally localize to mitochondria. Further-ore, ZmaSig2B was biochemically co-purified with RpoTm, theitochondrial phage-type RNA polymerase (Beardslee et al., 2002),

uggesting a possible role of these mitochondrially localized sigmaactors in regulating mitochondrial transcription by phage-typeNAPs.

itochondrial promoters

In vitro capping techniques, in vitro transcription assays andequence analysis led to the identification of transcription ini-iation sites and promoter motifs in Zea mays (Mulligan et al.,988, 1991; Rapp et al., 1993; Caoile and Stern, 1997), Zea peren-is (Newton et al., 1995), Glycine max (Brown et al., 1991), Pisumativum (Binder et al., 1995; Giese et al., 1996; Dombrowski etl., 1999; Hoffmann and Binder, 2002), Triticum aestivum (Covellond Gray, 1991), Nicotiana (Lelandais et al., 1996; Edqvist andergman, 2002), Solanum tuberosum (Binder et al., 1994; Lizamat al., 1994; Giese et al., 1996; Remacle and Maréchal-Drouard,996), Sorghum (Yan and Pring, 1997) and Oenothera berterianaBinder and Brennicke, 1993). One type of plant mitochondrialromoters is characterized by a consensus sequence motif (CRTA)imilar to the YRTA motif of plastid NEP promoters (see reviewsn Fey and Maréchal-Drouard, 1999; Binder and Brennicke, 2003;

eihe, 2004). In dicotyledoneous plants, the CRTA motif is partf a nonanucleotide sequence including the initiation site (Bindert al., 1996). The conserved nonanucleotide (CRTAaGaGA, tran-cription initiation site underlined) of eudicot promoters showsonsiderable sequence identity between different genes as well asetween different species. As shown by mutational analyses theromoter regions required for successful transcription initiationxtend beyond the obviously conserved regions (Hoffmann andinder, 2002). Comparing 11 promoters from pea, soybean, potatond Oenothera Dombrowski et al. (1999) deduced an extendedonsensus sequence (AAAATATCATAAGAGAAG, 100% conservedositions in bold, transcription initiation site underlined) that con-ists of three parts: the conserved nonanucleotide motif from −7 to2, containing the transcription initiation site; the less conservedT-box, consisting of predominantly adenosine and thymidineases located through positions −14 to −8; and the positions3 and +4, where mainly purines are found. Additionally, certainucleotide identities are required for efficient in vitro transcrip-ion initiation in the AT-rich region. Alternative promoter motifsere described in a more recent study on mapping of mitochon-
rial promoters in Arabidopsis (Kühn et al., 2005). In addition to theRTA-type consensus motif, loose or unusual core motifs such asTTA and RGTA were identified. Several putative promoters were
acking consensus sequences (Kühn et al., 2005). Mutation of the

iology 168 (2011) 1345– 1360

CATA motif of the atp8 promoter P-228/226 to CtgA led to a dra-matic drop of levels of correctly initiated transcripts in vitro, anevidence for the functional importance of the core motif (Kühn etal., 2007). Many other promoters identified lack common struc-tures or sequence motifs. However, it cannot be excluded that thereexist hidden similarities between several transcription initiationsites of this divergent class of mitochondrial promoters (Binder andBrennicke, 2003).

Monocot promoters are much less conserved (Fey andMaréchal-Drouard, 1999; Weihe, 2004). The core promoter con-sists of a CRTA tetranucleotid motif, often located just upstreamof the first transcribed nucleotide. Functional studies of the maizeatp1 and cox3 promoters confirmed the substantial role of this coremotif (Rapp et al., 1993; Caoile and Stern, 1997). Apart from theCRTA motif, degenerated YRTA, AATA, and CTTA sequences wereidentified in Sorghum (Yan and Pring, 1997). Most consensus-typepromoters in monocots share a small upstream element whichresides about 10 nucleotides further upstream and contains anAT-rich region of six nucleotides (Rapp et al., 1993; Tracy andStern, 1995). Full activity of the maize mitochondrial atp1 promoterrequired a 26-bp sequence, and an unaltered spacing between theupstream and the core elements was essential (Caoile and Stern,1997).

The presence of more than one promoter and multiple tran-scription initiation sites is a common feature of both monocot andeudicot chondromes (Mulligan et al., 1988; Tracy and Stern, 1995;Lupold et al., 1999b; Kühn et al., 2005). Thus, three initiation siteswere reported for the Z. mays cox2 and cob genes, and six for the atp9gene. Kühn et al. (2005) suggested that the presence of multiplepromoters could ensure transcription despite possible mitochon-drial genome rearrangements. The activity of maize cox2 promotersis dependent on their genomic context reflecting the consequencesof intra- and intergenomic recombination for plant mitochondrialgene expression (Lupold et al., 1999a).

Multilevel regulation of mitochondrial gene expression

Gene expression is regulated at transcriptional, post-transcriptional, translational, and post translational levels. Atthe DNA level, unregulated differences in promoter strength maylead to differential gene expression (Muise and Hauswirth, 1992).By comparing mitochondrial transcriptional rates in Arabidopsisand a cytoplasmic male sterile and a fertile line of Brassica napusspecies-specific transcription rates for several genes (cox1, nad4L,nad9, ccmB, rps7, and rrn5) were demonstrated, most likely aconsequence of different promoter strength (Leino et al., 2005).A study comprising all mitochondrial-encoded genes in Ara-bidopsis revealed distinct transcription rates of genes encodingcomponents of the same multisubunit complex (Giegé et al.,2000). Tissue- or cell-specific differences in mitochondrial geneexpression have been correlated with transcriptional levels in afew reports (Topping and Leaver, 1990; Li et al., 1996). Multiplemitochondrial promoters have been identified in a comprehen-sive study in Arabidopsis (Kühn et al., 2005), but mapping datadid not support a role of distinct promoters in developmentalor tissue-specific regulation of mitochondrial gene expression.Differences in transcriptional activities of genes are, at least par-tially, counterbalanced in the steady-state RNA pool, most likelyby posttranscriptional processes and different RNA stabilities(Mulligan et al., 1988; Tracy and Stern, 1995; Lupold et al., 1999a;Giegé et al., 2000; Leino et al., 2005; Holec et al., 2008). Theinfluence of the nuclear background on both transcription rates
and posttranscriptional mechanisms in alloplasmic cytoplasmicmale sterility (CMS) lines of Brassica suggests that both processesare not only depending on mitochondrial cis-elements, but also onnuclear trans-factors (Edqvist and Bergman, 2002).

t Physi

ggsttcc

Frscbheocl

db2bsrictttg1coqiatbdPtaWs

T

P

P

rReSsEettedl

K. Liere et al. / Journal of Plan

A minor importance of regulatory mechanisms in mitochondrialene expression is suggested by the observation that mitochondrialene expression remained more or less unaffected at the tran-criptional, posttranscriptional, and translational levels in responseo sugar starvation (Giegé et al., 2005). The observed reduc-ion of ATPase complexes could be attributed to nuclear-encodedomponents of the ATPase being down-regulated. The correct stoi-hiometric proportions seemed to be achieved posttranslationally.

The existence of two RNA polymerases (RpoTm and RpoTmp;igs. 1 and 2) in angiosperm mitochondria might be employed foregulatory purposes. The lack of RpoTmp resulted in reduced tran-cription and transcript accumulation of the genes nad2, nad6, andox1 coding for subunits of the complexes I and IV. It is likely thatoth RpoTm and RpoTmp transcribe these genes, with RpoTmpaving a role in fine-tuning their expression. Moreover, the reducedxpression of these genes correlated with a reduction in the amountf complexes I and IV supporting the view that, also in plant mito-hondria, regulation of transcription may be of importance for theevel of the gene products (Kühn et al., 2009).

The copy numbers of mitochondrial genes in Arabidopsis mayiffer considerably not only between individual genes, but alsoetween organs and different developmental stages (Preuten et al.,010). It is tempting to speculate that the control of copy num-ers of mitochondrial genes in different tissues and developmentaltages could be a mechanism to regulate transcript levels andates of respiration. Indeed, the formation of anthers and pollens associated with increased transcript levels and numbers of mito-hondria and possibly with enhanced mtDNA in certain flowerissues (Warmke and Lee, 1978; Geddy et al., 2005 and referencesherein). Both transcript levels and gene copy numbers were foundo be enhanced in photosynthetically inactive white compared toreen leaves in the albostrians mutant of barley (Hedtke et al.,999). Increased mitochondrial gene copies were also positivelyorrelated with transcript and protein levels in an RpoTmp mutantf Arabidopsis (Kühn et al., 2009). Comparing mitochondrial geneuantities (determined by DNA hybridization) and transcription

n maize and Brassica hirta, Muise and Hauswirth (1995) found direct relationship between gene copy number and transcrip-ional rate. This seems not generally to be the case. No correlationetween gene copy numbers and transcript levels were founduring leaf development in Arabidopsis (Preuten et al., 2010) andhaseolus vulgaris (Woloszynska and Trojanowski, 2009). However,he data of the different studies may not be comparable since Muisend Hauswirth (1995) determined transcription rates, whereasoloszynska and Trojanowski (2009) and Preuten et al. (2010)

tudied transcript levels.

he transcriptional machinery of chloroplasts

lastid RNA polymerases

EP: the plastid-encoded plastid RNA polymeraseThe plastomes of algae and higher plants possess rpoA, rpoB,

poC1, and rpoC2 genes for core subunits of a cyanobacterial-typeNA polymerase, which is commonly abbreviated as PEP (plastid-ncoded plastid RNA polymerase; Lysenko and Kuznetsov, 2005;hiina et al., 2005; Liere and Börner, 2007a,b). PEP ß- and ß′-ubunits can functionally substitute homologous subunits of the. coli RNA polymerase (Severinov et al., 1996). Furthermore, PEPxhibits sensitivity to inhibitors of bacterial transcription such asagetitoxin (e.g. Mathews and Durbin, 1990; Sakai et al., 1998) and
he group of rifampicin-related drugs (e.g. Surzycki, 1969; Loiseauxt al., 1975; Pfannschmidt and Link, 1997) demonstrating the highegree of conservation of these eubacterial-type RNAPs during evo-
ution. Moreover, the PEP holoenzyme too is formed by the addition

ology 168 (2011) 1345– 1360 1349

of sigma factors for promoter recognition to the plastid-encodedcore subunits. However, the sigma factors are encoded by nucleargenes (see Nuclear-encoded plastid sigma factors).

PEP can be isolated from plastids as a soluble enzymeand, together with DNA, as an insoluble form as the so-called‘transcriptionally active chromosome’ (TAC; e.g. Briat et al., 1979;Greenberg et al., 1984; Little and Hallick, 1988; Suck et al., 1996). Itis commonly accepted for higher plants that the basic eubacterial-type holoenzyme is combined with various accessory proteinfactors (Schweer et al., 2010a). While the soluble PEP isolated fromphotosynthetically inactive etioplasts essentially consists of thecore subunits (Pfannschmidt and Link, 1997), additional proteinswere found in PEP preparations from photosynthetically activechloroplasts. More than 50 proteins have been identified to be asso-ciated with or be part of the PEP complex (Pfannschmidt and Link,1994, 1997; Link, 1996; Baginsky et al., 1999; Krause and Krupinska,2000; Pfannschmidt et al., 2000; Ogrzewalla et al., 2002; Loschelderet al., 2004; Suzuki et al., 2004; Pfalz et al., 2006; Schröter et al.,2010). Since the addition of several accessory components to theeubacterial core enzyme as well as the nuclear origin of these fac-tors assigns further eukaryotic characteristics to the PEP, it is agood example of the eukaryotization of the plastid to integrate theorganelle into the cellular network. In algae, PEP might be responsi-ble for transcription of all plastid genes in algae. However, in mostland plants PEP is further complemented by an additional RNAPactivity, which is nuclear-encoded (NEP; Fig. 2).

NEP: the nuclear-encoded plastid RNA polymeraseEarly studies in effects of inhibitors of translation on cyto-

plasmic and plastid ribosomes suggested the existence of one ormore nuclear-encoded plastid RNA polymerase(s) (NEP; Ellis andHartley, 1971). The detection of active transcription in plastidswith impaired biogenesis, development, and/or protein synthesisimplied a nuclear location of gene(s) encoding the RNAP activity(Bünger and Feierabend, 1980; Siemenroth et al., 1981; Falk et al.,1993; Han et al., 1993; Hess et al., 1993). In addition, plastid geneswere still transcribed in transplastomic tobacco plants with deletedPEP (Allison et al., 1996; Hajdukiewicz et al., 1997; Krause et al.,2000; Legen et al., 2002). The albino phenotype of these plantsindicates that the transcriptional activity of the NEP alone is not suf-ficient for the biogenesis of photosynthetically active chloroplasts.Similarly, RNA synthesis was still detectable in nonphotosyntheticplastids of the parasitic plant Epifagus virginiana, which lacks thegenes for the PEP core subunits (Morden et al., 1992; Ems et al.,1995). Similar observations have been made after sequencing plas-tomes of other parasitic plants with functionally reduced plastids(Lusson et al., 1998; Krause et al., 2003; Berg et al., 2004; Krause,2008).

The RNAPs responsible for the NEP activity in plastids are knownto be RNA polymerases of the bacteriophage T3/7-type (Fig. 2).RpoT genes coding for phage-type RNA polymerases in plants werediscovered in a variety of plants (see Mitochondrial RNA poly-merases are phage-type enzymes; for reviews see Shiina et al., 2005;Liere and Börner, 2007a). Already before, Lerbs-Mache (1993) hadobserved an RNAP activity in spinach chloroplasts with a size of110 kDa, which coincides with the size expected for RpoT prod-ucts, initiating transcription from a promoter generally recognizedby the RNA polymerase of T7 phages (gene 10 promoter; Dunnand Studier, 1983). In eudicots such as Nicotiana sylvestris and Ara-bidopsis thaliana the RpoT gene family consists of three genes, fromwhich two gene products are targeted into plastids, RpoTp and thedually localized RpoTmp (Fig. 2, bottom right panel). However, with
nuclear chromosomes only encoding RpoTm and RpoTp (to date,only cereals have been investigated) monocotyledonous plantshave only RpoTp as a plastid NEP enzyme (Fig. 2, top right panel;see also Mitochondrial RNA polymerases are phage-type enzymes, and

1 t Phys

rtagpyRau(e

rdKlftaFgtwlBmg2

P

C

pc(aBtt(Bad−tapaedstp

Ci

d1crt1eS


eferences therein). Whether algae need NEP in addition to PEP toranscribe their plastid genes is not known yet (see review by Smithnd Purton, 2002). However, in case of Chlamydomonas, the nuclearenome contains only one RpoT gene (see above; Fig. 2, top leftanel) and a NEP activity is apparently lacking as shown by anal-ses of plastid transcription after inhibition of the plastid encodedNAP (Surzycki, 1969; Guertin and Bellemare, 1979; Eberhard etl., 2002). Also other algae, such as Osteococcus tauri (Hess et al.,npublished data; Derelle et al., 2006) and Thalassiosira pseudonanaArmbrust et al., 2004) possess only one RpoT gene which likelyncodes the mitochondrial RNAP.

Several lines of evidence demonstrated that RpoTp and RpoTmpepresent the NEP activity. RpoTp and RpoTmp proteins have beenetected by specific antibodies in chloroplasts (Chang et al., 1999;usumi et al., 2004; Azevedo et al., 2008; Sobanski et al., unpub-

ished data). A direct link between RpoTp and plastid transcriptionrom NEP promoters was provided by studies on transgenic Nico-iana and Arabidopsis plants overexpressing RpoTp, which exhibitedn increased usage of certain NEP promoters (Liere et al., 2004).urthermore, Arabidopsis knockout mutants of the RpoTp or RpoTmpenes led to impaired chloroplast biogenesis and altered accumula-ion of plastid transcripts (Hricová et al., 2006). Similar observationsere made in Arabidopsis plants with reduced RpoTp transcript

evels due to the expression of antisense RNA (Emanuel andörner, unpublished data). Furthermore, RpoTp/RpoTmp doubleutants showed an even more severe phenotype than the sin-

le mutants and were extremely growth retarded (Hricová et al.,006).

lastid promoters

onserved sequences and structures of PEP promotersConform to the cyanobacterial origin of chloroplasts many

lastid promoters contain the −35 (TTGaca) and −10 (TAtaaT)onsensus sequences of typical eubacterial �70-type promotersReznikov et al., 1985; Weihe, 2004; for recent reviews see Lysenkond Kuznetsov, 2005; Shiina et al., 2005; Liere and Börner, 2007a,b).ecause such plastid �70-type promoters are served by PEP,hey are also termed PEP promoters. The E. coli RNAP is ableo faithfully recognize PEP promoters further demonstrating thecyano)bacterial roots of chloroplasts (e.g. Gatenby et al., 1981;radley and Gatenby, 1985; Boyer and Mullet, 1988; Eisermann etl., 1990). Interestingly, most plastid promoters in Chlamydomonaso not possess a valid −35 element. Both a downstream-extended10 box (Klein et al., 1992) and further remote sequences such as

he coding regions seem to compensate the lack of the −35 box andre needed to gain full promoter strength (e.g. rbcL and psbA, but notsbD, atpA, and atpB; Blowers et al., 1990; Klein et al., 1994; Shiina etl., 1998; Ishikura et al., 1999; Kasai et al., 2003). Although cis-actinglements within the coding regions may be unique for Chlamy-omonas (Shiina et al., 1998; Kasai et al., 2003), further regulatoryequences in addition to the promoter core were also identified inhe proximity of PEP promoters in higher plants (see Regulation oflastid transcription and transcription factors).

onserved sequences and structures of NEP promoters andnternal promoters of tRNA genes

Generally, NEP transcripts are, with a few exceptions, rarelyetectable in green chloroplasts (Maliga, 1998; Hess and Börner,999; Liere and Maliga, 2001). Therefore, for identification andharacterization of NEP initiation sites and promoters plants witheduced or eliminated transcriptional activity by PEP were advan-
ageous (Allison et al., 1996; Vera et al., 1996; Hajdukiewicz et al.,997; Kapoor et al., 1997; Hübschmann and Börner, 1998; Miyagit al., 1998; Serino and Maliga, 1998; Silhavy and Maliga, 1998a,b;wiatecka-Hagenbruch et al., 2007).
iology 168 (2011) 1345– 1360

In accordance with the similarity of the phage-type RNAPsin mitochondria and plastids, NEP promoters analyzed thus farclearly resemble plant mitochondrial promoters in their struc-tural organization (see Mitochondrial promoters). Indeed, NEP veryactively initiated transcription from a mitochondrial promoter intransplastomic tobacco chloroplasts (Bohne et al., 2007). NEP pro-moters can be grouped into three types based on their sequenceproperties (Weihe and Börner, 1999; Liere and Maliga, 2001).Type-I promoters are characterized by a conserved YRTa-motifembedded in a small DNA fragment (−15 to +5) upstream of thetranscription initiation site (+1), which is critical for promoterrecognition (PatpB-289; Kapoor and Sugiura, 1999; PaccD-129;Liere and Maliga, 1999b; PrpoB-345; Liere and Maliga, 1999a; Xieand Allison, 2002) and may have up- and downstream regulatoryregions (Inada et al., 1997; Hirata et al., 2004). However, additionalsequence elements outside of the promoter core did not influ-ence transcription of the rpoB promoter in vitro (Liere and Maliga,1999a). A second, conserved sequence motif (ATAN0–1GAA) ∼18to 20 bp upstream of the YRTa-motif, designated box II or GAA-box (Silhavy and Maliga, 1998a; Kapoor and Sugiura, 1999; Xie andAllison, 2002) is characteristic of a subset of Type-Ib NEP promoters(Weihe and Börner, 1999; Liere and Börner, 2007a).

Type-II promoters lack the YRTa-motif and differ completelyin sequence and organization from Type-I promoters and so farcomprise the so-called ‘non-consensus’ NEP promoters. This is aheterogenous group and may need to be divided into subgroupswhen more non-consensus promoters will be characterized. Thusfar, the best characterized, the tobacco PclpP-53, was dissectedusing a transplastomic in vivo approach demonstrating that crit-ical promoter sequences are located mainly downstream of thetranscription initiation site (−5 to +25; Sriraman et al., 1998).Although the clpP-53 promoter is conserved among monocots,eudicots, conifers, and liverworts, it is not used as a promoter inrice and Chlamydomonas. However, the rice sequence is accuratelyrecognized in transplastomic tobacco plants, i.e. the tobacco NEPrecognizes this conserved Type-II promoter. Therefore, the lackof transcription in rice from the PclpP Type-II promoter might bea consequence of the lack of a distinct NEP enzyme not presentin monocots (e.g. RpoTmp, see Mitochondrial RNA polymerases arephage-type enzymes and NEP: the nuclear-encoded plastid RNA poly-merase; Sriraman et al., 1998; Liere et al., 2004; Courtois et al., 2007;Swiatecka-Hagenbruch et al., 2008). A further non-YRTa-type NEPpromoter is the rrn operon Pc promoter found in spinach, mus-tard, and Arabidopsis (Pc promoter; Baeza et al., 1991; Iratni et al.,1994, 1997; Pfannschmidt and Link, 1997; Sriraman et al., 1998;Swiatecka-Hagenbruch et al., 2007). The rrn16 promoter regionis highly conserved and contains typical �70-elements, which areactive as the principal rrn operon PEP promoter in other species(Liere and Börner, 2007b). However, in spinach plastids transcrip-tion solely initiates at a site between the conserved −10/−35PEP promoter elements. In Arabidopsis usage of the Pc promoteris developmentally timed. Initially transcribed by RpoTmp, tran-scription from the enclosing PEP promoter takes over later indevelopment (Courtois et al., 2007; Swiatecka-Hagenbruch et al.,2008). Sequences relevant for transcription initiation from Pc haveyet to be identified.

Although the majority of plastid tRNA genes are transcribed bythe PEP from upstream �70-type promoters, several reports sug-gested transcription from internal promoters: the spinach trnS,trnR, and trnT (Gruissem et al., 1986; Cheng et al., 1997), the mus-tard trnS, trnH, and trnR (Neuhaus and Link, 1990; Nickelsen andLink, 1990; Liere and Link, 1994), and the Chlamydomonas trnE gene
(Jahn, 1992). Wu et al. (1997) demonstrated in in vitro transcriptionassays that the sole coding region (+1/+93) of the spinach trnS genepromotes basal levels (8%) of transcription. These tRNAs may betranscribed by specialized NEP or PEP enzymes associated with dis-

t Physiology 168 (2011) 1345– 1360 1351

ts

D

fRpabSdp(a2cPaHPfeyieKSt((t

(m

Fr2tettrttpsla

Fig. 4. Exogenous and endogenous factors such as light, hormones, photosynthesis,plastid type and chloroplast development differentially modulate transcription ofplastid genes. Cues with repressing action on plastid transcription are depicted withlines terminated with a bar while arrows represent promoting signals (see text for


inct transcription factors recognizing the unique tRNA promotertructures.

ivision of labor between PEP and NEP

In spite of the diversity of promoter usage in plastids of dif-erent species, the available data points to a common pattern inNAP-dependent promoter usage: most genes have PEP and NEPromoters, a few house-keeping genes have only NEP promotersnd transcription of a few photosynthesis genes is directed onlyy PEP genes (reviewed in Maliga, 1998; Liere and Maliga, 2001;wiatecka-Hagenbruch et al., 2007; Zhelyazkova et al., unpublishedata). NEP and PEP seem to be active in all investigated types oflastids: chloroplasts, etioplasts, amyloplasts, and chromoplastse.g. Marano and Carrillo, 1992; Tiller and Link, 1993; Isono etl., 1997a; Baginsky et al., 2004; Wurbs et al., 2007; Barsan et al.,010). Interestingly, the rpoB operon encoding three of the four PEPore subunits in all higher plants is solely transcribed by NEP (seelastid RNA polymerases; Hajdukiewicz et al., 1997; Hübschmannnd Börner, 1998; Silhavy and Maliga, 1998a; Swiatecka-agenbruch et al., 2007). Consequently, not only the activity ofEP is regulated by the nucleus via various means (e.g. sigmaactors) but also the abundance of PEP depends on a nuclear-ncoded RNAP (Figs. 3 and 4). NEP promoters are more active inoungest, non-green tissues early in leaf development, while PEPncreases activity during maturation of chloroplasts (Bisanz-Seyert al., 1989; Baumgartner et al., 1993; Hajdukiewicz et al., 1997;apoor et al., 1997; Emanuel et al., 2004; Courtois et al., 2007;wiatecka-Hagenbruch et al., 2007, 2008; Zoschke et al., 2007). E.g.he Arabidopsis rrn operon was shown to be transcribed by NEPRpoTmp) during seed germination and early plant developmentCourtois et al., 2007; Swiatecka-Hagenbruch et al., 2008), with PEP
aking over the expression during later developmental stages.
The identification of integral thylakoid membrane proteinsNIPs; NEP interacting proteins) interacting with RpoTmp led to a

odel to explain the developmental switch from NEP to PEP tran-

ig. 3. Model on the role of nuclear-encoded phage-type RNA polymerases inegulating plastid gene expression (updated and modified after Liere and Börner,007b). The nuclear RpoTp gene encodes in part the NEP transcription activity. NEPranscribes and therefore may regulate the expression of the plastid rpoB operonncoding subunits of the plastid-encoded RNA-polymerase (PEP). PEP, however,ranscribes genes encoding components of the photosynthetic complexes (PSI, PSII)hat modulate nuclear transcription by generating various ‘plastid signals’ (e.g. ROS,eactive oxygen species). PEP also transcribes trnE encoding a tRNA (trnAGlu). TheRNA is required for the synthesis of �-aminolevulinic acid (ALA), the precursor ofhe tetrapyrrole (TP) biosynthesis (chlorophyll and heme), which too is thought torovide ‘plastid signals’. Thus, the regulatory network of the nuclear and plastid tran-cription machineries may be a key element for adjusting the expression of genesocated within different compartments of the plant cell in response to exogenousnd endogenous factors.

references; effects of respiration on chloroplast transcription: T. Potapova, Y. Zubo,Y. Konstantinov, T. Börner, unpublished data).

scription (Azevedo et al., 2008). The light-induced expression ofNIPs might mediate binding of RpoTmp to the thylakoid mem-branes as demonstrated for spinach chloroplasts and lead finallyto down-regulation of plastid rrn-operon transcription (Azevedoet al., 2008). In immuno-assays with Arabidopsis plants constitu-tively expressing epitope-tagged AthRpoTp and AthRpoTmp partialmembrane association has also been detected (Sobanski et al.,unpublished data). However, given the fact that, similar to bacteria,the plastid transcriptional apparatus and the plastid DNA (orga-nized in nucleoids) are supposed to be membrane associated (Sato,2001; Sato et al., 2003; Karcher et al., 2009; Schweer et al., 2010a),it seems unlikely that binding to the thylakoid membrane is anindication for the inactivation of RpoTmp.

A regulatory role, which links chlorophyll synthesis and thedevelopmental switch from NEP to PEP, has been proposed forthe plastid-encoded tRNAGlu in Arabidopsis (Hanaoka et al., 2005).tRNAGlu is not only required for translation, but also for synthesisof �-aminolevulinic acid, a precursor of chlorophyll (Fig. 3; Schönet al., 1986). However, reinvestigation of the postulated inhibitoryactivity of tRNAGlu demonstrated a rather unspecific binding of allthree Arabidopsis phage-type RNA polymerases (RpoTp, RpoTmp,and RpoTm) to not only tRNAGlu but also to other tRNAs tested.Additionally, NEP activity is not down-regulated during chloroplastdevelopment and leaf maturation (Cahoon et al., 2004; Zoschke etal., 2007), thereby suggesting that tRNAGlu does not play a role inspecifically regulating NEP activity (Bohne et al., 2009).

The simplistic model on a sequential division of labor betweenNEP and PEP has been further extended by several observa-tions. Firstly, macroarray analyses of the transcriptome of tobacco�rpo mutants lacking PEP showed that spurious transcripts ini-tiated by NEP cover the entire plastome (Krause et al., 2000;Legen et al., 2002). Besides selective promoter utilization, alteredpost-transcriptional processes may also determine the transcriptpattern of plastid genes in these mutants. Secondly, both NEPand PEP are active throughout leaf development in Arabidopsis(Zoschke et al., 2007). Cahoon et al. (2004) showed in maizethat while NEP becomes less abundant as chloroplasts matureits transcriptional activity increases. Despite that, the stability ofthe RNA generated by NEP declined during chloroplast develop-ment. The transcription rates of PEP, however, increased duringchloroplasts development, while the RNA stability of its tran-
scripts remained constant or even increased. Thus, a model wasproposed for maize plastid biogenesis in which NEP-controlledtranscript accumulation changes little during plastid development

1 t Phys

wa

aSNPthRicAmwsoPtc

R

N

cnSrwSilt�nlw2c2rt2(u2

ipFtA2Nbea

bitoipp


hile PEP-controlled transcript accumulation increases (Cahoon etl., 2004).

An additional role of NEP has been proposed by Schweer etl. (2006). Analyses of transcript accumulation of atpB in an Ath-ig6 knockout mutant suggested that a further upstream-locatedEP promoter compensates for failing transcription from the mainEP promoter thereby attributing NEP as an SOS-enzyme in plastidranscription. Thus, NEP transcription by phage-type enzymes mayave been established in chloroplasts for an entire different reason.poT enzymes exhibit an intrinsic transcription initiation activity,

.e. act as single-polypeptide RNAPs able to recognize several mito-hondrial and chloroplast promoters in vitro (Kühn et al., 2007).fter the nuclear-encoded RpoTs acquired organellar targeting, thisight have been sufficient to support transcription from promotersith simple structures (see Mitochondrial promoters and Conserved

equences and structures of NEP promoters and internal promotersf tRNA genes), thereby counteracting effects of point mutations inEP promoters. Therefore, the complexity of the plastid transcrip-ion may perhaps have evolved to compensate for degeneratinghloroplast promoters (Maier et al., 2008).

egulation of plastid transcription and transcription factors

uclear-encoded plastid sigma factorsThe eubacterial-type RNAP complex in plastids of higher plants

ontains sigma factors, which are responsible for promoter recog-ition and contribute to DNA melting around the initiation site.tructure, evolution and function of plastid sigma factors haveecently been reviewed and are here therefore only briefly dealtith (see Lysenko, 2007; Shiina et al., 2009; Lerbs-Mache, 2010;

chweer, 2010; Schweer et al., 2010a; Weihe et al., 2011). The fam-ly of plant sigma factors represents a monophyletic group with ateast 5 subgroups: Sig1, Sig2, Sig3, Sig5, and Sig6. They are relatedo bacterial primary (group 1) and non-essential primary (group 2)70-factors (Lysenko, 2006, 2007). However, none fit into the alter-ative group 3 nor seem to be related to �54-factors, though a very

imited similarity of Sig5 to the bacterial alternative sigma factorsas detected (Tsunoyama et al., 2002; Shiina et al., 2005; Lysenko,

006). Similar to bacterial �70-factors, plant sigma factors haveonserved domains involved in binding the core RNAP (domains.1 and 3), hydrophobic core formation (2.2), DNA melting (2.3),ecognition of the -10 promoter motif (2.4), and recognition ofhe -35 promoter motif (4.1 and 4.2; Shiina et al., 2009; Schweer,010; Schweer et al., 2010a). In addition to this conserved regionCR), plastid sigma factors possess at the N-terminus an additionalnconserved region (UCR) of functional importance (Schweer et al.,009).

Most plastid sigma factor genes of higher plants are expressedn light-dependent manner in green tissue but are silent in non-hotosynthetic roots (Isono et al., 1997b; Tanaka et al., 1997;ujiwara et al., 2000; Oikawa et al., 2000). The expression of plas-id sigma factors seems to be differentially regulated during earlyrabidopsis development (Kanamaru et al., 1999; Lahiri and Allison,000; Homann and Link, 2003; Privat et al., 2003; Kasai et al., 2004;agashima et al., 2004b; Fey et al., 2005; Ishizaki et al., 2005) and toe regulated by circadian rhythms (Nakahira et al., 1998; Kanamarut al., 1999; Morikawa et al., 1999; Oikawa et al., 2000; Ichikawa etl., 2004).

The most conclusive clues for their functions have been obtainedy extensive characterization of Arabidopsis sigma factor T-DNA

nsertion mutants, overexpression or anti-sense lines. Most plas-id genes appear to be controlled by several sigma factors with
verlapping functions. However, within a certain time frame dur-ng Arabidopsis plant development the expression of about sevenlastid genes seems to be coordinated by a distinct sigma factor: i.e.saA by AthSig1; psaJ by AthSig2, psbN by AthSig3, ndhF by AthSig4,
iology 168 (2011) 1345– 1360

psbD (BLRP) by AthSig5, and atpB by AthSig6 (recently reviewed inLysenko, 2007; Shiina et al., 2009; Lerbs-Mache, 2010; Schweer,2010; Schweer et al., 2010a).

AthSig2 and AthSig6 seem to be important factors early inseedling development with restricted roles in recognition of cer-tain promoters later on. AthSig1, AthSig3, and AthSig4 may haveoverlapping roles in the transcription of photosynthesis genes inmature leaves maybe in response to the developmental and envi-ronmental signals. AthSig5 might have gained an important role indifferent signaling pathways in response to environmental stressesbased on its weaker binding affinity to the PEP core enzyme in com-parison to that of the other sigma factors as suggested by sequenceanalyses, which results in a PEP holoenzyme less prone to abortivetranscription (Lysenko, 2007). Hence, plants, similar to bacteria, usea set of sigma factors to differentially regulate plastid gene expres-sion. The diversity of plastid sigma factors in higher plants may bea result of the demands of both environment and stress toleranceduring evolution.

Phosphorylation of sigma factors and the PEP enzyme hasbeen shown to be responsible for changes in chloroplast tran-scription (Tiller and Link, 1993; Baginsky et al., 1997; Christopheret al., 1997). Available data (Baginsky et al., 1997, 1999; Baena-Gonzalez et al., 2001) points to a PEP-associated Ser/Thr proteinkinase, termed plastid transcription kinase (PTK), to be involvedin plastid sigma factor phosphorylation. The catalytic compo-nent of PTK is closely related to the �-subunit of casein kinase2 (CK2) and was subsequently named cpCK2 (Ogrzewalla et al.,2002), which is present in a number of plant species, includingArabidopsis (Loschelder et al., 2004; Salinas et al., 2006). Basedon the observation that cpCK2 itself is antagonistically regulatedby phosphorylation and redox state, cpCK2 was proposed to bepart of a signaling pathway controlling PEP activity (for reviewssee Pfannschmidt and Liere, 2005; Liere and Börner, 2007a,b).Light dependent reduction of GSH would inactivate cpCK2, whiledephosphorylation of PEP under high light conditions wouldenhance PEP-dependent transcription. The regulatory phospho-acceptor sites reside within the UCRs of plastid sigma factors.cpCK2 might be assisted by other kinase(s) by pre-phosphorylation(‘pathfinder’ kinase; Schweer et al., 2010b). Furthermore, the phos-phorylation of AthSig1 is involved in the stoichiometric adjustmentof PS I and II in response to different light conditions (see above;Shimizu et al., 2010). In this case, a pathway different from thatinvolving cpCK2 seems to be used. Depending on its oxidation statePQ generates a ‘priming signal’ (Buchanan and Balmer, 2005), whichmight be promoted as an early step in the signal transduction path-way by a chloroplast sensor kinase (CSK; Puthiyaveetil et al., 2008,2010).

In bacteria, sigma factor activity is controlled by so called anti-sigma factors (Ishihama, 2000). Although proteins associated withAthSig1 associated were identified in Arabidopsis (SIB1 and T3K9.5;Morikawa et al., 2002), they are not related to any proteins ofknown function. Based on their expression pattern, which is devel-opmental and tissue-specific, and regulated by light, they might beinvolved in regulation of AthSig1 activity.

NEP transcription factorsThus far identification of factors involved in specific pro-

moter recognition and transcription initiation by NEP has failed(see Phage-type RNA polymerases require auxiliary factors for tran-scription initiation in vivo). BLAST searches of the Arabidopsisgenome revealed a mtTFB-like dimethyladenosine transferase geneformerly characterized as PFC1 (Tokuhisa et al., 1998), which pos-
sesses an N-terminal transit peptide mediating protein importinto plastids of isolated tobacco protoplasts (Kuhla et al., unpub-lished data). However, neither the phenotype of PFC1-knockoutmutants nor in vitro transcription studies with recombinant PFC1

t Physi

alfu

r(WrNIbNteahtt

tRtmpti

E

tCatmeadarba

hm(sigtleSCswt(tcsipara


nd AthRpoTp did support the idea that this mtTFB-like dimethy-adenosine transferase may act as a primary transcription factoror the phage-type RNA polymerases (Swiatecka-Hagenbruch et al.,npublished data).

A factor involved in NEP transcription is the spinach CDF2,eported to stimulate transcription of the rrn operon Pc promoterBligny et al., 2000). CDF2 is proposed to exist in two distinct forms.

hile CDF2-A might repress transcription initiation by PEP at thern16 P1 promoter (termed P2 in spinach), CDF2-B possibly bindsEP and initiates specific transcription from the rrn16 Pc promoter.

n addition, a role of RPL4 (plastid ribosomal protein L4, encodedy the nuclear Rpl4 gene) has been discussed to be involved inEP transcription, since it co-purifies with the T7-like transcrip-

ion complex in spinach (Trifa et al., 1998). The bacterial L4 hasxtra-ribosomal functions in transcriptional regulation (Zengel etl., 1980). The spinach and Arabidopsis Rpl4 genes have acquiredighly acidic C-terminal extensions, which are common amongranscription factors. A function for this protein in plastid transcrip-ion, however, has yet to be demonstrated.

Interestingly, some nuclear-encoded sigma factors were foundo be dual-targeted to plastids and mitochondria (see Phage-typeNA polymerases require auxiliary factors for transcription initia-ion in vivo). One might speculate that sigma factors therefore

ay generally have a role as co-factors in the transcription byhage-type RNAPs. Yet, experimental data to link the activity ofhe bacterial-type plastid sigma factors to the phage-type enzymesn mitochondria or plastids are still lacking.

xogenous and endogenous factors affecting plastid transcriptionAlthough post-transcriptional events contribute significantly to

he regulation of plastid gene expression (Barkan and Goldschmidt-lermont, 2000; Monde et al., 2000; Stern et al., 2010), exogenousnd endogenous factors such as light, temperature, hormones, plas-id type and chloroplast development were shown to differentially

odulate also the transcriptional activity of plastid genes (Rappt al., 1992; Mullet, 1993; Mayfield et al., 1995; Link, 1996; Lierend Börner, 2007a). Apparently, the transcriptional response toevelopmental and environmental changes is mediated via inter-ction of the core RNAPs with specific sigma factors and/or otheregulatory factors. In silico analyses revealed up to 78 nuclear Ara-idopsis genes for putative plastid transcription factors (Wagnernd Pfannschmidt, 2006; Schwacke et al., 2007).

Light plays a major role in activating plastid transcription inigher plants. Environmental control of plastid gene expression isost intense in differentiation from proplastids to either etioplasts

dark) or chloroplasts (light). To rapidly build up the photosynthe-is apparatus, the light-induced plant (and plastid) developments accompanied by an increase of transcription of most plastidenes. Moreover, light-dependent transcription of certain plas-id genes occurs in leaves during greening as well as in matureeaves (Greenberg et al., 1989; Schrubar et al., 1990; Baumgartnert al., 1993; DuBell and Mullet, 1995; Hoffer and Christopher, 1997;hiina et al., 1998; Satoh et al., 1999; Baena-Gonzalez et al., 2001;hun et al., 2001; Nakamura et al., 2003). In plants light is sensed bypecific photoreceptors responsible for the perception of particularavelengths (Chory, 2010), which also are involved in transcrip-

ional activation of photosynthesis-related genes in chloroplastsChun et al., 2001; Thum et al., 2001). Global activation of plas-id transcription after dark adaptation is likely to be mediated byryptochromes, while red light only partially increases plastid tran-cription. Interestingly, phytochromes were shown to also functionn blue light reception to induce transcription of certain chloro-
last genes (Chun et al., 2001; Thum et al., 2001). Cryptochromesre discussed to be sensors of blue/green light ratios under natu-al radiation (Sellaro et al., 2010). Therefore, green light might play
balancing/antagonistic role to blue light during early photomor-

ology 168 (2011) 1345– 1360 1353

phogenic development by down-regulating plastid transcription ofgenes normally induced by light (Dhingra et al., 2006).

Well-characterized examples of light-induced plastid genes are:e.g. psbA, psbD-psbC, petG, rbcL, and atpB (Klein et al., 1988; Haleyand Bogorad, 1990; Klein and Mullet, 1990; Sexton et al., 1990;Isono et al., 1997a). Generally, transcription of the psbA gene, whichencodes the D1 photosystem II reaction center polypeptide, isdevelopmentally timed and activated by light in vivo (Klein andMullet, 1990; Schrubar et al., 1990; Baumgartner et al., 1993). Thecis-elements involved in the light-regulated transcription from thispromoter differ in various plant species (reviewed in Shiina et al.,2005; Liere and Börner, 2007a,b). The rbcL gene, which encodes thelarge subunit of the ribulose-1,5-bisphosphate carboxylase oxy-genase, is transcribed from a well conserved PEP promoter withan additional upstream element (Shinozaki and Sugiura, 1982;Gruissem and Zurawski, 1985; Hanley-Bowdoin et al., 1985; Mulletet al., 1985; Reinbothe et al., 1993; Isono et al., 1997a), which hasbeen suggested to function as a binding site for the chloroplastDNA-binding factor 1 (CDF1) in maize (Lam et al., 1988). How-ever, CDF1 seems not to play a role in light-regulated expression ofthe rbcL gene in tobacco (Shiina et al., 1998). Nevertheless, anotherlight-induced DNA-binding protein (RLBP, rbcL promoter-bindingprotein) binds specifically to the rbcL promoter core (−3 to −32)suggesting a role in light-dependent rbcL transcription in tobacco(Kim et al., 2002).

The psbD–psbC operon, encoding reaction center protein D2and the chlorophyll-binding antenna protein cp43 of photosys-tem II, is actively transcribed even in mature chloroplasts (Kleinand Mullet, 1990; Baumgartner et al., 1993; DuBell and Mullet,1995). Responsible for this activation is one of the psbD pro-moters, the blue light-responsive promoter (BLRP; Sexton et al.,1990), which is found upstream of the psbD gene of various plantspecies (Christopher et al., 1992; Wada et al., 1994; Allison andMaliga, 1995; Kim and Mullet, 1995; To et al., 1996; Hoffer andChristopher, 1997; Kim et al., 1999b; Thum et al., 2001). Salientfeatures of this particular promoter are two additional conservedelements (PGT-box, AAG-box) upstream of core promoter ele-ments. Although suggested to be responsible for light-activatedtranscript accumulation (Allison and Maliga, 1995), both PGT- andAAG-box and their interacting factors (PGTF; AGF, containing PTF1,plastid transcription factor 1) are not required for light-dependentactivation (Kim and Mullet, 1995; To et al., 1996; Satoh et al., 1997;Nakahira et al., 1998; Kim et al., 1999a,b; Baba et al., 2001; Thumet al., 2001). AthSig5 was shown to act as a mediator of blue lightsignaling to activate psbD BLRP transcription (see Nuclear-encodedplastid sigma factors; Tsunoyama et al., 2002, 2004; Nagashima etal., 2004a; Onda et al., 2008). The signal transduction pathway isassumed to involve reception of blue light by cryptochromes andphytochrome A (PhyA; Thum et al., 2001; Mochizuki et al., 2004),transfer by a protein phosphatase PP7 (Moller et al., 2003), and sub-sequent induction of AthSig5 expression (Mochizuki et al., 2004).Furthermore, co-regulation of both leaf development and the psbDBLRP has been shown by down-regulation of psbD BLRP in youngArabidopsis seedlings by DET1 (Christopher and Hoffer, 1998).

Further factors involved in regulation of transcription by PEPare the chloroplast proteins CSP41a and CSP41b from Arabidop-sis. While CSP41a binds and cleaves RNA (Yang and Stern, 1997;Bollenbach et al., 2003), CSP41b co-purifies with CSP41a, ribo-somes, and the plastid-encoded RNA polymerase (Pfannschmidtet al., 2000; Suzuki et al., 2004; Raab et al., 2006). Bollenbach etal. (2009) suggested a general function of these proteins in bothtranscription and translation in chloroplasts, with a specific role
in atpB operon expression. Since both AthSig6 and CSP41 seem toinfluence the promoter choice for the atpB operon (see Division oflabor between PEP and NEP; Schweer et al., 2006; Bollenbach et al.,2009), their possible interactions need further investigation.

1 t Phys

thtft(MFt(Saiotrei(a1bfC

sgoafeantasintiaitrmlpfAtSPtd

pdtetgaeeD


Not only light but also circadian and diurnal rhythms seemo control the expression of several plastid genes in algae andigher plants, which is expected to be mediated by nuclear fac-ors (Piechulla and Gruissem, 1987; Nakahira et al., 1998). Sigmaactors are good candidates to represent such factors, regulation ofheir expression by circadian or diurnal rhythms has been describedTozawa et al., 1998; Kanamaru et al., 1999; Lahiri et al., 1999;

orikawa et al., 1999; Oikawa et al., 2000; Ichikawa et al., 2004).actors, which are proposed to integrate light and circadian con-rol in the regulation of chloroplast development, are PIF1 and PIF3phytochrome interacting factor), a control that might involve Ath-ig5 (Monte et al., 2004; Tepperman et al., 2006; Stephenson etl., 2009). This seems to be reflected in P. patens where PpaSig5 isnvolved in the regulation of a diurnal rhythm and light inductionf psbD expression (Ichikawa et al., 2008). In Chlamydomonas theranscription of plastid genes too is under control of a circadianhythm mediated by a nuclear factor (Salvador et al., 1993; Hwangt al., 1996; Kawazoe et al., 2000; Lee and Herrin, 2002). Interest-ngly, expression of the sole, nuclear-encoded sigma factor CreRpoDCarter et al., 2004; Bohne et al., 2006) and the plastome topologyre also influenced by circadian rhythms (Thompson and Mosig,990; Salvador et al., 1998; Carter et al., 2004). Therefore, assistedy topological fluctuations of the plastome, CreRpoD might have aurther role in maintaining circadian controlled gene expression inhlamydomonas plastids (Misquitta and Herrin, 2005).

Feedback from the plastids depending on their developmentaltatus, metabolism, and/or gene expression is controlling nuclearene expression by generating so called ‘plastid signals’. Amongthers, reactive oxygen species, redox state, certain tetrapyrroles,nd products of chloroplast gene expression are discussed as plastidactors or plastid signals (Fig. 3; Rodermel, 2001; Gray, 2003; Grayt al., 2003; Brown et al., 2005; Kleine et al., 2009; Galvez-Valdiviesond Mullineaux, 2010; Inaba, 2010; Pfannschmidt, 2010). Theuclear RpoTp gene in barley, encoding the NEP activity, is one ofhe targets of plastid signal(s) (Emanuel et al., 2004; Colombo etl., 2008). Retrograde signaling coordinates therefore the expres-ion of PEP and NEP as a prerequisite of concerted gene expressionn both plastids and the nucleus (Fig. 3). Although retrograde sig-aling is directed from the organelle toward the nucleus, the samerigger may affect both nuclear and plastid transcription. A wellnvestigated example is the redox-dependent regulation of nuclearnd plastid genes (see below). Also plant hormones play a rolen coordinating the gene expression in plastids/chloroplasts andhe nucleus, a function that has not been recognized until mostecently (Fig. 4; Zubo et al., 2008b; Yamburenko, personal com-unication; Zubo et al., 2011). Since the biosynthesis of hormones

ike cytokinins, abscisic acid (ABA), and methyl jasmonate takeslace (at least partially) in plastids, they may be regarded as “plastidactors” triggering “retrograde signaling” to the nucleus. AlthoughBA, an important hormone in stress signaling, has been discussed

o be involved in retrograde signaling (Mochizuki et al., 2001;hen et al., 2006; Bräutigam et al., 2007; Koussevitzky et al., 2007;fannschmidt, 2010), plant hormones have not been shown yeto act as retrograde signals communicating the metabolic and/orevelopmental state of plastids/chloroplasts.

Effects of the redox state of the plastoquinone pool (PQ) onlastid gene transcription (and on retrograde signaling) wereemonstrated by generating an imbalance in excitation energy dis-ribution between the photosystems PSI and PSII (Pfannschmidtt al., 1999a,b; Fey et al., 2005; Bräutigam et al., 2009). This pho-osynthetic redox control is mediated toward the level of plastidene expression via plastid STN7 and CSK kinases (Puthiyaveetil
nd Allen, 2008; Pesaresi et al., 2009; Steiner et al., 2009). Shimizut al. (2010) recently suggested that CSK might be involved in anarly step in the signal transduction pathway involving AthSig1.ependent on the redox state of the PQ pool phosphorylation of
iology 168 (2011) 1345– 1360

AthSig1 differentially regulated transcription of psaA in Arabidop-sis thereby maintaining a balanced expression of photosystem Iand II components under various light conditions. Other plastidtranscription factors that transmit redox signals have yet to becharacterized. A putative DNA-binding protein of PS II, TSP9, is par-tially released from PSII upon PQ reduction in spinach and mayrepresent such a signal transducer towards transcription (Carlberget al., 2003; Zer and Ohad, 2003). Furthermore, both the redoxchanges in the PQ and thioredoxin pools might act as cooper-ative signals that coordinate not only plastid and nuclear geneexpression but also the metabolism (Bräutigam et al., 2009). Aplastid-localized thioredoxin (TRX z) has recently been shown tointeract with two fructokinase-like proteins (FLNs), apparentlyboth necessary for PEP-dependent gene expression in chloroplasts.Therefore, together with the two FLNs, TRX z was discussed to forma thus far unknown protein interaction module essential for chloro-plast development (Arsova et al., 2010).

Not only transcription by PEP is redox regulated (Pfannschmidtet al., 1999a,b; Fey et al., 2005; Bräutigam et al., 2009), but alsothe expression of several components/subunits of the PEP complexsuch as rpoB (plastid-encoded �-subunit), AthSig5 (nuclear-encoded sigma factor), and SibI (nuclear-encoded Sig1-bindingprotein; Morikawa et al., 2002; Fey et al., 2005). Interestingly, NEPis responsible for rpoB operon transcription, thereby suggesting aregulation of this enzyme by redox signaling. Although PEP wasreported to be regulated via redox control mediated by glutathione(Baginsky et al., 1999), the analyses by Fey et al. (2005) did notindicate differences in the glutathione redox-state. It seems likelythat the control of plastid transcription is mediated via severaldistinct redox signaling pathways, which depend on environmen-tal conditions such as responses to low or high light (Link, 2003;Pfannschmidt and Liere, 2005).

Bacteria developed a so-called ‘stringent control’, which enablesthem to adapt to nutrient-limiting stress conditions (Cashel etal., 1996). The effector molecule is guanosine 5′-diphosphate 3′-diphosphate (ppGpp), which modifies the promoter specificity ofthe bacterial RNAP (Toulokhonov et al., 2001; Jishage et al., 2002).Homologues of the bacterial key enzymes in the stress-inducedppGpp synthesis, RelA and SpoT, were found in Chlamydomonasreinhardtii (Kasai et al., 2002), Arabidopsis (van der Biezen et al.,2000) and tobacco (Givens et al., 2004) and termed RSH (RelA/SpoThomologs). Both the expression of plastid-targeted RSH enzymesand the levels of plastid ppGpp are elevated by light and various abi-otic and biotic stress conditions. Furthermore, the transcriptionalactivity of PEP in vitro is inhibited by ppGpp through directly bind-ing to the �’-subunit (Givens et al., 2004; Takahashi et al., 2004;Sato et al., 2009). Thus, it is conceivable that under stress con-ditions PEP might be under control of a bacterial-like stringentresponse mediated by ppGpp, which is also discussed for cyanobac-teria (Imamura and Asayama, 2009). Interestingly, stress signalsspecifically induce plastid transcription of the psbD BLRP conferredby sigma factor AthSig5 (see above and Nuclear-encoded plastidsigma factors; Nagashima et al., 2004a; Tsunoyama et al., 2004). Oth-erwise, stress seems in first line to down-regulate transcription ofchloroplast genes like it does with nuclear photosynthesis-relatedgenes (Fig. 4). Zubo et al. (2008a) found a significantly reducedexpression of several genes in barley chloroplasts in response toheat stress. Moreover, when applied to detached leaves, ABA (Yam-burenko et al., unpublished data) and methyl jasmonate (Zubo et al.,2011), hormones known to be involved in the response of plants toabiotic and biotic stresses, drastically inhibited the transcription ofplastid genes (Fig. 4). Cytokinins exhibited the contrary effect. The
cytokinin 6-benzyl adenine stimulated the transcription of manychloroplast genes, which is in agreement with the stimulating roleof cytokinins in chloroplast development and their well-knowndelaying effect on senescence (Zubo et al., 2008b and references

t Physi

tt

A

ma

R

A

A

A

A

A

A

A

B

B

B

B

B

B

B

B

B

B

B

B

B

B

B

B


herein). How plant hormones act on plastid transcription remainso be investigated.

cknowledgements

The work of the authors is supported by Deutsche Forschungsge-einschaft (SFB 429). We thank Kristina Kühn for providing initial

rtwork.

eferences

dams KL, Daley DO. Plant mitochondrial genome evolution and gene transfer tothe nucleus. Plant mtochondria: from genome to function. In: Day DA, MillarAH, Whelan J, editors. Advances in photosynthesis and respiration. Dordrecht:Springer; 2004. p. 107–20.

llison LA, Maliga P. Light-responsive and transcription-enhancing elements regu-late the plastid psbD core promoter. EMBO J 1995;14:3721–30.

llison LA, Simon LD, Maliga P. Deletion of rpoB reveals a second distinct transcrip-tion system in plastids of higher plants. EMBO J 1996;15:2802–9.

rmbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, AllenAE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, DemarestMS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, JenkinsBD, Jurka J, Kapitonov VV, Kroger N, Lau WWY, Lane TW, Larimer FW, LippmeierJC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ,Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, ValentinK, Vardi A, Wilkerson FP, Rokhsar DS. The genome of the diatom Thalassiosirapseudonana: ecology, evolution, and metabolism. Science 2004;306:79–86.

rsova B, Hoja U, Wimmelbacher M, Greiner E, Ustün S, Melzer M, Petersen K, Lein W,Börnke F. Plastidial thioredoxin z interacts with two fructokinase-like proteinsin a thiol-dependent manner: evidence for an essential role in chloroplast devel-opment in Arabidopsis and Nicotiana benthamiana. Plant Cell 2010;22:1498–515.

sin-Cayuela J, Gustafsson CM. Mitochondrial transcription and its regulation inmammalian cells. Trends Biochem Sci 2007;32:111–7.

zevedo J, Courtois F, Hakimi M-A, Demarsy E, Lagrange T, Alcaraz J-P, Jaiswal P,Maréchal-Drouard L, Lerbs-Mache L. Intraplastidial trafficking of a phage-typeRNA polymerase is mediated by a thylakoid RING-H2 protein. Proc Natl Acad SciUSA 2008;105:9123–8.

aba K, Nakano T, Yamagishi K, Yoshida S. Involvement of a nuclear-encoded basichelix-loop-helix protein in transcription of the light-responsive promoter ofpsbD. Plant Physiol 2001;125:595–603.

aba K, Schmidt J, Espinosa-Ruiz A, Villarejo A, Shiina T, Gardestrom P, Sane AP,Bhalerao RP. Organellar gene transcription and early seedling development areaffected in the RpoT;2 mutant of Arabidopsis. Plant J 2004;38:38–48.

aena-Gonzalez E, Baginsky S, Mulo P, Summer H, Aro E-M, Link G. Chloroplasttranscription at different light intensities. Glutathione-mediated phosphoryla-tion of the major RNA polymerase involved in redox-regulated organellar geneexpression. Plant Physiol 2001;127:1044–52.

aeza L, Bertrand A, Mache R, Lerbs-Mache S. Characterization of a protein bindingsequence in the promoter region of the 16S rRNA gene of the spinach chloroplastgenome. Nucleic Acids Res 1991;19:3577–81.

aginsky S, Tiller K, Link G. Transcription factor phosphorylation by a protein kinaseassociated with chloroplast RNA polymerase from mustard (Sinapis alba). PlantMol Biol 1997;34:181–9.

aginsky S, Tiller K, Pfannschmidt T, Link G. PTK, the chloroplast RNA polymerase-associated protein kinase from mustard (Sinapis alba), mediates redox controlof plastid in vitro transcription. Plant Mol Biol 1999;39:1013–23.

aginsky S, Siddique A, Gruissem W. Proteome analysis of tobacco bright yellow-2(BY-2) cell culture plastids as a model for undifferentiated heterotrophic plas-tids. J Proteome Res 2004;3:1128–37.

arkan A, Goldschmidt-Clermont M. Participation of nuclear genes in chloroplastgene expression. Biochimie 2000;82:559–72.

arsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, Kuntz M, Zouine M, LatchéA, Bouzayen M, Pech J-C. Characteristics of the tomato chromoplast revealed byproteomic analysis. J Exp Bot 2010;61:2413–31.

aumgartner BJ, Rapp JC, Mullet JE. Plastid genes encoding the transcrip-tion/translation apparatus are differentially transcribed early in barley(Hordeum vulgare) chloroplast development: evidence for selective stabilizationof psbA mRNA. Plant Physiol 1993;101:781–91.

eardslee TA, Roy-Chowdhury S, Jaiswal P, Buhot L, Lerbs-Mache S, Stern DB, AllisonLA. A nucleus-encoded maize protein with sigma factor activity accumulates inmitochondria and chloroplasts. Plant J 2002;31:199–209.

erg S, Krause K, Krupinska K. The rbcL genes of two Cuscuta species, C. gronovii andC. subinclusa, are transcribed by the nuclear-encoded plastid RNA polymerase(NEP). Planta 2004;219:541–6.

inder S, Brennicke A. Transcription initiation sites in mitochondria of Oenotheraberteriana. J Biol Chem 1993;268:7849–55.

inder S, Thalheim C, Brennicke A. Transcription of potato mitochondrial 26S rRNAis initiated at its mature 5′ end. Curr Genet 1994;26:519–23.

inder S, Hatzack F, Brennicke A. A novel pea mitochondrial in vitro transcriptionsystem recognizes homologous and heterologous mRNA and tRNA promoters. JBiol Chem 1995;270:22182–9.

inder S, Marchfelder A, Brennicke A. Regulation of gene expression in plant mito-chondria. Plant Mol Biol 1996;32:303–14.

ology 168 (2011) 1345– 1360 1355

Binder S, Brennicke A. Gene expression in plant mitochondria: transcriptional andpost-transcriptional control. Philos Trans R Soc Lond B Biol Sci 2003;358:181–8[Discussion 8–9].

Bisanz-Seyer C, Li Y-F, Seyer P, Mache R. The components of the plastid ribosomeare not accumulated synchronously during the early development of spinachplants. Plant Mol Biol 1989;12:201–11.

Bligny M, Courtois F, Thaminy S, Chang CC, Lagrange T, Baruah-Wolff J, Stern D,Lerbs-Mache S. Regulation of plastid rDNA transcription by interaction of CDF2with two different RNA polymerases. EMBO J 2000;19:1851–60.

Blowers AD, Ellmore GS, Klein U, Bogorad L. Transcriptional analysis of endogenousand foreign genes in chloroplast transformants of Chlamydomonas. Plant Cell1990;2:1059–70.

Bohne A-V, Irihimovitch V, Weihe A, Stern D. Chlamydomonas reinhardtii encodesa single sigma70-like factor which likely functions in chloroplast transcription.Curr Genet 2006;49:333–40.

Bohne A-V, Ruf S, Börner T, Bock R. Faithful transcription initiation from a mitochon-drial promoter in transgenic plastids. Nucleic Acids Res 2007;35:7256–66.

Bohne AV, Weihe A, Börner T. Interaction of Arabidopsis phage-type RNA poly-merases with transfer RNAs. Endocytobiosis Cell Res 2009;19:63–9.

Bollenbach TJ, Tatman DA, Stern DB. CSP41a, a multifunctional RNA-bindingprotein, initiates mRNA turnover in tobacco chloroplasts. Plant J 2003;36:842–52.

Bollenbach TJ, Sharwood RE, Gutierrez R, Lerbs-Mache S, Stern DB. The RNA-bindingproteins CSP41a and CSP41b may regulate transcription and translation ofchloroplast-encoded RNAs in Arabidopsis. Plant Mol Biol 2009;69:541–52.

Boyer SK, Mullet JE. Sequence and transcript map of barley chloroplast psbA gene.Nucleic Acids Res 1988;16:8184.

Bradley D, Gatenby AA. Mutational analysis of the maize chloroplast ATPase-beta subunit gene promoter: the isolation of promoter mutants in E. coli andtheir characterization in a chloroplast in vitro transcription system. EMBO J1985;4:3641–8.

Brandvain Y, Wade M. The functional transfer of genes from the mitochondria tothe nucleus: the effects of selection, mutation, population size and rate of self-fertilization. Genetics 2009;182:1129–39.

Bräutigam K, Dietzel L, Pfannschmidt T. Plastid-nucleus communication: antero-grade and retrograde signalling in the development and function of plastids. In:Bock R, editor. Topics in current genetics, cell and molecular biology of plastids.Springer; 2007. p. 409–55.

Bräutigam K, Dietzel L, Kleine T, Ströher E, Wormuth D, Dietz K, Radke D, WirtzM, Hell R, Dörmann P, Nunes-Nesi A, Schauer N, Fernie A, Oliver S, Geigen-berger P, Leister D, Pfannschmidt T. Dynamic plastid redox signals integrate geneexpression and metabolism to induce distinct metabolic states in photosyntheticacclimation in Arabidopsis. Plant Cell 2009;21:2715–32.

Brennicke A, Grohmann L, Hiesel R, Knoop V, Schuster W. The mitochondrial genomeon its way to the nucleus: different stages of gene transfer in higher plants. FEBSLett 1993;325:140–5.

Briat JF, Laulhere JP, Mache R. Transcription activity of a DNA–protein complexisolated from spinach plastids. Eur J Biochem 1979;98:285–92.

Brown GG, Auchincloss AH, Covello PS, Gray MW, Menassa R, Singh M. Character-ization of transcription initiation sites in the soybean mitochondrial genomeallows identification of a transcription-associated sequence motif. Mol GenGenet 1991;228:345–55.

Brown NJ, Sullivan JA, Gray JC. Light and plastid signals regulate the expression ofthe pea plastocyanin gene through a common region at the 5′ end of the codingregion. Plant J 2005;43:541–52.

Buchanan BB, Balmer Y. Redox regulation: a broadening horizon. Annu Rev PlantBiol 2005;56:187–220.

Bünger W, Feierabend J. Capacity for RNA synthesis in 70S ribosome-deficient plas-tids of heat-bleached rye leaves. Planta 1980;149:163–9.

Cahoon AB, Harris FM, Stern DB. Analysis of developing maize plastids revealstwo mRNA stability classes correlating with RNA polymerase type. EMBO Rep2004;5:801–6.

Caoile AGFS, Stern DB. A conserved core element is functionally important for maizemitochondrial promoter activity in vitro. Nucleic Acids Res 1997;25:4055–60.

Carlberg I, Hansson M, Kieselbach T, Schroder WP, Andersson B, Vener AV. A novelplant protein undergoing light-induced phosphorylation and release from thephotosynthetic thylakoid membranes. Proc Natl Acad Sci USA 2003;100:757–62.

Carter ML, Smith AC, Kobayashi H, Purton S, Herrin DL. Structure, circadianregulation and bioinformatic analysis of the unique sigma factor gene in Chlamy-domonas reinhardtii. Photosynth Res 2004;82:339–49.

Cashel M, Gentry DM, Hernandez VJ, Vinella D. The stringent response. In: NeidhardtFC, editor. Escherichia coli and Salmonella typhimurium: cellular and molecularbiology. Washington, DC: ASM Press; 1996. p. 1458–96.

Chang C-C, Sheen J, Bligny M, Niwa Y, Lerbs-Mache S, Stern DB. Functionalanalysis of two maize cDNAs encoding T7-like RNA polymerases. Plant Cell1999;11:911–26.

Cheng YS, Lin CH, Chen LJ. Transcription and processing of the gene for spinachchloroplast threonine tRNA in a homologous in vitro system. Biochem BiophysRes Commun 1997;233:380–5.

Chory J. Light signal transduction: an infinite spectrum of possibilities. Plant J
2010;61:982–91.
Christopher DA, Kim M, Mullet JE. A novel light-regulated promoter is conserved incereal and dicot chloroplasts. Plant Cell 1992;4:785–98.

Christopher DA, Li XL, Kim M, Mullet JE. Involvement of protein kinase and extraplas-tidic Serine/Threonine protein phosphatases in signaling pathways regulating

1 t Phys

C

C

C

C

C

D

D

D

D

D

D

D

D

E

E

E

E

E

E

E

E

F

F

F

F

F

G

G


plastid transcription and the psbD blue light-responsive promoter in barley.Plant Physiol 1997;113:1273–82.

hristopher DA, Hoffer PH. DET1 represses a chloroplast blue light-responsive pro-moter in a developmental and tissue-specific manner in Arabidopsis thaliana.Plant J 1998;14:1–11.

hun L, Kawakami A, Christopher DA. Phytochrome A mediates blue light andUV-A-dependent chloroplast gene transcription in green leaves. Plant Physiol2001;125:1957–66.

ourtois F, Merendino L, Demarsy E, Mache R, Lerbs-Mache S. Phage-type RNApolymerase RPOTmp transcribes the rrn operon from the PC promoter at earlydevelopmental stages in Arabidopsis. Plant Physiol 2007;145:712–21.

ovello PS, Gray MW. Sequence analysis of wheat mitochondrial transcripts cappedin vitro: definitive identification of transcription initiation sites. Curr Genet1991;20:245–52.

olombo N, Emanuel C, Lainez V, Maldonado S, Prina AR, Börner T. The barleyplastome mutant CL2 affects expression of nuclear and chloroplast house-keeping genes in a cell-age dependent manner. Mol Gen Genomics 2008;27:403–14.

äschner K, Couée I, Binder S. The mitochondrial isovaleryl-coenzyme A dehydro-genase of Arabidopsis oxidizes intermediates of leucine and valine catabolism.Plant Physiol 2001;126:601–12.

erelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F,Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O,Piegu B, Ball SG, Ral J-P, Bouget F-Y, Piganeau G, De Baets B, Picard A, Delseny M,Demaille J, Van de Peer Y, Moreau H. Genome analysis of the smallest free-livingeukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad SciUSA 2006;103:11647–52.

hingra A, Bies DH, Lehner KR, Folta KM. Green light adjusts the plastidtranscriptome during early photomorphogenic development. Plant Physiol2006;142:1256–66.

iffley JF, Stillman B. A close relative of the nuclear, chromosomal high-mobility group protein HMG1 in yeast mitochondria. Proc Natl Acad Sci USA1991;88:7864–8.

ombrowski S, Hoffmann M, Guha C, Binder S. Continuous primary sequencerequirements in the 18-nucleotide promoter of dicot plant mitochondria. J BiolChem 1999;274:10094–9.

uBell AN, Mullet JE. Differential transcription of pea chloroplast genes during light-induced leaf development. Plant Physiol 1995;109:105–12.

unn JJ, Studier FW. Complete nucleotide sequence of bacteriophage T7 DNA andthe locations of T7 genetic elements. J Mol Biol 1983;166:477–535.

yall SD, Brown MT, Johnson PJ. Ancient invasions: from endosymbionts toorganelles. Science 2004;304:253–7.

berhard S, Drapier D, Wollman F-A. Searching limiting steps in the expres-sion of chloroplast-encoded proteins: relations between gene copy number,transcription, transcript abundance and translation rate in the chloroplast ofChlamydomonas reinhardtii. Plant J 2002;31:149–60.

dqvist J, Bergman P. Nuclear identity specifies transcriptional initiation in plantmitochondria. Plant Mol Biol 2002;49:59–68.

isermann A, Tiller K, Link G. In vitro transcription and DNA binding characteris-tics of chloroplast and etioplast extracts from mustard (Sinapis alba) indicatedifferential usage of the psbA promoter. EMBO J 1990;9:3981–7.

llis RJ, Hartley MR. Sites of synthesis of chloroplast proteins. Nature1971;233:193–6.

lo A, Lyznik A, Gonzalez DO, Kachman SD, Mackenzie SA. Nuclear genes that encodemitochondrial proteins for DNA and RNA metabolism are clustered in the Ara-bidopsis genome. Plant Cell 2003;15:1619–31.

manuel C, Weihe A, Graner A, Hess WR, Börner T. Chloroplast developmentaffects expression of phage-type RNA polymerases in barley leaves. Plant J2004;38:460–72.

manuel C, von Groll U, Müller M, Börner T, Weihe A. Development- andtissue-specific expression of the RpoT gene family of Arabidopsis encoding mito-chondrial and plastid RNA polymerases. Planta 2006;223:998–1009.

ms SC, Morden CW, Dixon CK, Wolfe KH, dePamphilis CW, Palmer JD. Transcription,splicing and editing of plastid RNAs in the nonphotosynthetic plant Epifagusvirginiana. Plant Mol Biol 1995;29:721–33.

alk J, Schmidt A, Krupinska K. Characterization of plastid DNA transcription inribosome deficient plastids of heat-bleached barley leaves. J Plant Physiol1993;141:176–81.

ey J, Maréchal-Drouard L. Compilation and analysis of plant mitochondrial pro-moter sequences: an illustration of a divergent evolution between monocot anddicot mitochondria. Biochem Biophys Res Commun 1999;256:409–14.

ey V, Wagner R, Bräutigam K, Wirtz M, Hell R, Dietzmann A, Leister D, OelmüllerR, Pfannschmidt T. Retrograde plastid redox signals in the expression ofnuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem2005;280:5318–28.

isher RP, Lisowsky T, Parisi MA, Clayton DA. DNA wrapping and bending by a mito-chondrial high mobility group-like transcriptional activator protein. J Biol Chem1992;267:3358–67.

ujiwara M, Nagashima A, Kanamaru K, Tanaka K, Takahashi H. Three new nucleargenes, sigD, sigE and sigF, encoding putative plastid RNA polymerase � factorsin Arabidopsis thaliana. FEBS Lett 2000;481:47–52.

alvez-Valdivieso G, Mullineaux PM. The role of reactive oxygen species in signallingfrom chloroplasts to the nucleus. Physiol Plant 2010;138:430–9.

atenby AA, Castleton JA, Saul MW. Expression in E. coli of maize and wheatchloroplast genes for large subunit of ribulose bisphosphate carboxylase. Nature1981;291:117–21.

iology 168 (2011) 1345– 1360

Geddy R, Mahé L, Brown GG. Cell-specific regulation of a Brassica napus CMS-associated gene by a nuclear restorer with related effects on a floral homeoticgene promoter. Plant J 2005;41:333–45.

Giegé P, Hoffmann M, Binder S, Brennicke A. RNA degradation buffers asymmetriesof transcription in Arabidopsis mitochondria. EMBO Rep 2000;1:164–70.

Giegé P, Sweetlove LJ, Cognat V, Leaver CJ. Coordination of nuclear and mitochondrialgenome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell2005;17:1497–512.

Giese A, Thalheim C, Brennicke A, Binder S. Correlation of nonanucleotide motifswith transcript initiation of 18S rRNA genes in mitochondria of pea, potato andArabidopsis. Mol Gen Genet 1996;252:429–36.

Givens RM, Lin MH, Taylor DJ, Mechold U, Berry JO, Hernandez VJ. Inducible expres-sion, enzymatic activity, and origin of higher plant homologues of bacterialRelA/SpoT stress proteins in Nicotiana tabacum. J Biol Chem 2004;279:7495–504.

Gray JC. Chloroplast-to-nucleus signalling: a role for Mg-protoporphyrin. TrendsGenet 2003;19:526–9.

Gray JC, Sullivan JA, Wang JH, Jerome CA, MacLean D. Coordination of plastid andnuclear gene expression. Philos Trans R Soc Lond B Biol Sci 2003;358:135–44[Discussion 44–45].

Gray MW. The evolutionary origins of plant organelles. In: Daniell H, Chase CD,editors. Molecular biology and biotechnology of plant organelles. Dordrecht:Springer; 2004. p. 15–36.

Gray MW. Rethinking plastid evolution. EMBO Rep 2010;11:562–3.Greenberg BM, Narita JO, DeLuca-Flaherty C, Gruissem W, Rushlow KA, Hallick RB.

Evidence for two RNA polymerase activities in Euglena gracilis chloroplasts. JBiol Chem 1984;259:14880–7.

Greenberg BM, Gaba V, Canaani O, Malkin S, Mattoo AK, Edelman M. Separatephotosensitizers mediate degradation of the 32-kDa photosystem II reactioncenter protein in the visible and UV spectral regions. Proc Natl Acad Sci USA1989;86:6617–20.

Gruissem W, Zurawski G. Analysis of promoter regions for the spinach chloroplastrbcL, atpB and psbA genes. EMBO J 1985;4:3375–83.

Gruissem W, Elsner-Menzel C, Latshaw S, Narita JO, Schaffer MA, Zurawski G. Asubpopulation of spinach chloroplast tRNA genes does not require upstreampromoter elements for transcription. Nucleic Acids Res 1986;14:7541–56.

Guertin M, Bellemare G. Synthesis of chloroplast ribonucleic acid in Chlamydomonasreinhardtii toluene-treated cells. Eur J Biochem 1979;96:125–9.

Hajdukiewicz PTJ, Allison LA, Maliga P. The two RNA polymerases encoded by thenuclear and the plastid compartments transcribe distinct groups of genes intobacco plastids. EMBO J 1997;16:4041–8.

Haley J, Bogorad L. Alternative promoters are used for genes within maize chloro-plast polycistronic transcription units. Plant Cell 1990;2:323–33.

Han CD, Patrie W, Polacco M, Coe EH. Abberations in plastid transcripts anddeficiency of plastid DNA in striped and albino mutants in maize. Planta1993;191:552–63.

Hanaoka M, Kanamaru K, Fujiwara M, Takahashi H, Tanaka K. Glutamyl-tRNA medi-ates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep2005;6:545–50.

Hanley-Bowdoin L, Orozco EMJ, Chua NH. In vitro synthesis and processing of a maizechloroplast transcript encoded by the ribulose 1,5-bisphosphate carboxylaselarge subunit gene. Mol Cell Biol 1985;5:2733–45.

Hedtke B, Börner T, Weihe A. Mitochondrial and chloroplast phage-type RNA poly-merases in Arabidopsis. Science 1997;277:809–11.

Hedtke B, Wagner I, Börner T, Hess WR. Interorganellar crosstalk in higher plants:impaired chloroplast development affects mitochondrial gene and transcriptlevels. Plant J 1999;19:635–43.

Hedtke B, Börner T, Weihe A. One RNA polymerase serving two genomes. EMBO Rep2000;1:435–40.

Hedtke B, Legen J, Weihe A, Herrmann RG, Börner T. Six active phage-type RNApolymerase genes in Nicotiana tabacum. Plant J 2002;30:625–37.

Hengeveld R, Fedonkin MA. Causes and consequences of eukaryotizationthrough mutualistic endosymbiosis and compartmentalization. Acta Biotheor2004;52:105–54.

Herrmann RG, Maier RM, Schmitz-Linneweber C. Eukaryotic genome evolution:rearrangement and coevolution of compartmentalized genetic information. Phi-los Trans R Soc Lond B Biol Sci 2003;358:87–97 [Discussion].

Hess WR, Prombona A, Fieder B, Subramanian AR, Börner T. Chloroplast rps15 and therpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids:evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J1993;12:563–71.

Hess WR, Börner T. Organellar RNA polymerases of higher plants. Int Rev Cytol1999;190:1–59.

Hirata N, Yonekura D, Yanagisawa S, Iba K. Possible involvement of the 5′-flankingregion and the 5′UTR of plastid accD gene in NEP-dependent transcription. PlantCell Physiol 2004;45:176–86.

Hoffer PH, Christopher DA. Structure and blue-light-responsive transcriptionof a chloroplast psbD promoter from Arabidopsis thaliana. Plant Physiol1997;115:213–22.

Hoffmann M, Binder S. Functional importance of nucleotide identities within thepea atp9 mitochondrial promoter sequence. J Mol Biol 2002;320:943–50.

Holec S, Lange H, Canaday J, Gagliardi D. Coping with cryptic and defective transcriptsin plant mitochondria. Biochim Biophys Acta 2008;1779:566–73.

Homann A, Link G. DNA-binding and transcription characteristics of three clonedsigma factors from mustard (Sinapis alba L.) suggest overlapping and distinctroles in plastid gene expression. Eur J Biochem 2003;270:1288–300.

t Physi

H

H

H

I

I

I

I

I

I

I

I

I

I

I

I

I

J

J

K

K

K

K

K

K

K

K

K

K

K

K


ricová A, Quesada V, Micol JL. The SCABRA3 nuclear gene encodes the plastid RpoTpRNA polymerase, which is required for chloroplast biogenesis and mesophyll cellproliferation in Arabidopsis. Plant Physiol 2006;141:942–56.

übschmann T, Börner T. Characterisation of transcript initiation sites in ribosome-deficient barley plastids. Plant Mol Biol 1998;36:493–6.

wang S, Kawazoe R, Herrin DL. Transcription of tufA and other chloroplast-encodedgenes is controlled by a circadian clock in Chlamydomonas. Proc Natl Acad SciUSA 1996;93:996–1000.

chikawa K, Sugita M, Imaizumi T, Wada M, Aoki S. Differential expression on a dailybasis of plastid sigma factor genes from the moss Physcomitrella patens. Regu-latory interactions among PpSig5, the circadian clock, and blue light signalingmediated by cryptochromes. Plant Physiol 2004;136:4285–98.

chikawa K, Shimizu A, Okada R, Satbhai SB, Aoki S. The plastid sigma factor SIG5is involved in the diurnal regulation of the chloroplast gene psbD in the mossPhyscomitrella patens. FEBS Lett 2008;582:405–9.

keda T, Gray M. Characterization of a DNA-binding protein implicated in transcrip-tion in wheat mitochondria. Mol Cell Biol 1999;19:8113–22.

mamura S, Asayama M. Sigma factors for cyanobacterial transcription. Gene RegulSyst Biol 2009;3:65–87.

naba T. Bilateral communication between plastid and the nucleus: plastid proteinimport and plastid-to-nucleus retrograde signaling. Biosci Biotechnol Biochem2010;74:471–6.

nada H, Seki M, Morikawa H, Nishimura M, Iba K. Existence of three regulatoryregions each containing a highly conserved motif in the promoter of plastid-encoded RNA polymerase gene (rpoB). Plant J 1997;11:883–90.

ratni R, Baeza L, Andreeva A, Mache R, Lerbs-Mache S. Regulation of rDNA transcri-pion in chloroplasts: promoter exclusion by constitutive repression. Genes Dev1994;8:2928–38.

ratni R, Diederich L, Harrak H, Bligny M, Lerbs-Mache S. Organ-specific transcriptionof the rrn operon in spinach plastids. J Biol Chem 1997;272:13676–82.

shihama A. Functional modulation of Escherichia coli RNA polymerase. Annu RevMicrobiol 2000;54:499–518.

shikura K, Takaoka Y, Kato K, Sekine M, Yoshida K, Shinmyo A. Expression of a foreigngene in Chlamydomonas reinhardtii chloroplast. J Biosci Bioeng 1999;87:307–14.

shizaki Y, Tsunoyama Y, Hatano K, Ando K, Kato K, Shinmyo A, Kobori M, TakebaG, Nakahira Y, Shiina T. A nuclear-encoded sigma factor, Arabidopsis SIG6, rec-ognizes sigma-70 type chloroplast promoters and regulates early chloroplastdevelopment in cotyledons. Plant J 2005;42:133–44.

sono K, Niwa Y, Satoh K, Kobayashi H. Evidence for transcriptional regulationof plastid photosynthesis genes in Arabidopsis thaliana roots. Plant Physiol1997a;114:623–30.

sono K, Shimizu M, Yoshimoto K, Niwa Y, Satoh K, Yokota A, Kobayashi H. Leaf-specifically expressed genes for polypeptides destined for chloroplasts withdomains of sigma70 factors of bacterial RNA polymerases in Arabidopsis thaliana.Proc Natl Acad Sci USA 1997b;94:14948–53.

ahn D. Expression of the Chlamydomonas reinhardtii chloroplast tRNA(Glu) gene in ahomologous in vitro transcription system is independent of upstream promoterelements. Arch Biochem Biophys 1992;298:505–13.

ishage M, Kvint K, Shingler V, Nyström T. Regulation of sigma factor competitionby the alarmone ppGpp. Genes Dev 2002;16:1260–70.

abeya Y, Sato N. Unique translation initiation at the second AUG codon deter-mines mitochondrial localization of the phage-type RNA polymerases in themoss Physcomitrella patens. Plant Physiol 2005;138:369–82.

anamaru K, Fujiwara M, Seki M, Katagiri T, Nakamura M, Mochizuki N, Nagatani A,Shinozaki K, Tanaka K, Takahashi H. Plastidic RNA polymerase sigma factors inArabidopsis. Plant Cell Physiol 1999;40:832–42.

apoor S, Suzuki JY, Sugiura M. Identification and functional significance of a newclass of non-consensus-type plastid promoters. Plant J 1997;11:327–37.

apoor S, Sugiura M. Identification of two essential sequence elements in the non-consensus Type II PatpB-290 plastid promoter by using plastid transcriptionextracts from cultured tobacco BY-2 cells. Plant Cell 1999;11:1799–810.

archer D, Köster D, Schadach A, Klevesath A, Bock R. The Chlamydomonaschloroplast HLP protein is required for nucleoid organization and genome main-tenance. Mol Plant 2009;2:1223–32.

asai K, Usami S, Yamada T, Endo Y, Ochi K, Tozawa Y. A RelA-SpoT homolog (Cr-RSH) identified in Chlamydomonas reinhardtii generates stringent factor in vivoand localizes to chloroplasts in vitro. Nucleic Acids Res 2002;30:4985–92.

asai K, Kawagishi-Kobayashi M, Teraishi M, Ito Y, Ochi K, Wakasa K, TozawaY. Differential expression of three plastidial sigma factors, OsSIG1, OsSIG2A,and OsSIG2B, during leaf development in rice. Biosci Biotechnol Biochem2004;68:973–7.

asai S, Yoshimura S, Ishikura K, Takaoka Y, Kobayashi K, Kato K, Shinmyo A. Effectof coding regions on chloroplast gene expression in Chlamydomonas reinhardtii.J Biosci Bioeng 2003;95:276–82.

awazoe R, Hwang S, Herrin DL. Requirement for cytoplasmic protein synthesisduring circadian peaks of transcription of chloroplast-encoded genes in Chlamy-domonas. Plant Mol Biol 2000;V44:699–709.

im JW, Park JK, Kim BH, Lee J-S, Sim WS. Molecular analysis of the accumula-tion of the transcripts of the large subunit gene of ribulose-1,5-bisphosphatecarboxylase/oxygenase by light. Mol Cells 2002;14:281–7.

im M, Mullet JE. Identification of a sequence-specific DNA binding factor required
for transcription of the barley chloroplast blue light-responsive psbD-psbC pro-moter. Plant Cell 1995;7:1445–57.
im M, Christopher DA, Mullet JE. ADP-Dependent phosphorylation regulatesassociation of a DNA-binding complex with the barley chloroplast psbD blue-light-responsive promoter. Plant Physiol 1999a;119:663–70.

ology 168 (2011) 1345– 1360 1357

Kim M, Thum KE, Morishige DT, Mullet JE. Detailed architecture of the bar-ley chloroplast psbD–psbC blue light-responsive promoter. J Biol Chem1999b;274:4684–92.

Klein RR, Mason HS, Mullet JE. Light-regulated translation of chloroplast pro-teins. I. Transcripts of psaA–psaB, psbA, and rbcL are associated with polysomesin dark-grown and illuminated barley seedlings. J Cell Biol 1988;106:289–301.

Klein RR, Mullet JE. Light-induced transcription of chloroplast genes. psbAtranscription is differentially enhanced in illuminated barley. J Biol Chem1990;265:1895–902.

Klein U, De Camp JD, Bogorad L. Two types of chloroplast gene promoters in Chlamy-domonas reinhardtii. Proc Natl Acad Sci USA 1992;89:3453–7.

Klein U, Salvador ML, Bogorad L. Activity of the Chlamydomonas chloroplast rbcLgene promoter is enhanced by a remote sequence element. Proc Natl Acad SciUSA 1994;91:10819–23.

Kleine T, Voigt C, Leister D. Plastid signalling to the nucleus: messengers still lost inthe mists? Trends Genet 2009;25:185–92.

Knoop V. The mitochondrial DNA of land plants: peculiarities in phylogenetic per-spective. Curr Genet 2004;46:123–39.

Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J,Mittler R, Chory J. Signals from chloroplasts converge to regulate nuclear geneexpression. Science 2007;316:715–9.

Krause K, Krupinska K. Molecular and functional properties of highly purifiedtranscriptionally active chromosomes from spinach chloroplasts. Physiol Plant2000;109:188–95.

Krause K, Maier RM, Kofer W, Krupinska K, Herrmann RG. Disruption of plastid-encoded RNA polymerase genes in tobacco: expression of only a distinct set ofgenes is not based on selective transcription of the plastid chromosome. MolGen Genet 2000;263:1022–30.

Krause K, Berg S, Krupinska K. Plastid transcription in the holoparasitic plant genusCuscuta: parallel loss of the rrn16 PEP-promoter and of the rpoA and rpoB genescoding for the plastid-encoded RNA polymerase. Planta 2003;216:815–23.

Krause K. From chloroplasts to “cryptic” plastids: evolution of plastid genomes inparasitic plants. Curr Genet 2008;54:111–21.

Kühn K, Weihe A, Börner T. Multiple promoters are a common feature of mitochon-drial genes in Arabidopsis. Nucleic Acids Res 2005;33:337–46.

Kühn K, Bohne A-V, Liere K, Weihe A, Börner T. Arabidopsis phage-type RNApolymerases: accurate in vitro transcription of organellar genes. Plant Cell2007;19:959–71.

Kühn K, Richter U, Meyer E, Delannoy E, de Longevialle AF, O’Toole N, Börner T,Millar A, Small I, Whelan J. Phage-type RNA polymerase RPOTmp performsgene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell2009;21:2762–79.

Kusumi K, Yara A, Mitsui N, Tozawa Y, Iba K. Characterization of a ricenuclear-encoded plastid RNA polymerase gene OsRpoTp. Plant Cell Physiol2004;45:1194–201.

Lahiri SD, Yao J, McCumbers C, Allison LA. Tissue-specific and light-dependentexpression within a family of nuclear-encoded sigma-like factors from Zea mays.Mol Cell Biol Res Commun 1999;1:14–20.

Lahiri SD, Allison LA. Complementary expression of two plastid-localized sigma-likefactors in maize. Plant Physiol 2000;123:883–94.

Lam E, Hanley-Bowdoin L, Chua NH. Characterization of a chloroplast sequence-specific DNA binding factor. J Biol Chem 1988;263:8288–93.

Lang BF, Burger G, O’Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, TurmelM, Gray MW. An ancestral mitochondrial DNA resembling a eubacterial genomein miniature. Nature 1997;387:493–7.

Lee J, Herrin DL. Assessing the relative importance of light and the circadian clockin controlling chloroplast translation in Chlamydomonas reinhardtii. PhotosynthRes 2002;72:295–306.

Legen J, Kemp S, Krause K, Profanter B, Herrmann RG, Maier RM. Comparativeanalysis of plastid transcription profiles of entire plastid chromosomes fromtobacco attributed to wild-type and PEP-deficient transcription machineries.Plant J 2002;31:171–88.

Leino M, Landgren M, Glimelius K. Alloplasmic effects on mitochondrial transcrip-tional activity and RNA turnover result in accumulated transcripts of ArabidopsisORFs in cytoplasmic male-sterile Brassica napus. Plant J 2005;42:469–80.

Leister D. Origin, evolution and genetic effects of nuclear insertions of organelleDNA. Trends Genet 2005;21:655–63.

Lelandais C, Gutierres S, Mathieu C, Vedel F, Remacle C, Maréchal-Drouard L, Bren-nicke A, Binder S, Chétrit P. A promoter element active in run-off transcriptioncontrols the expression of two cistrons of nad and rps genes in Nicotiana sylvestrismitochondria. Nucleic Acids Res 1996;24:4798–804.

Lerbs-Mache S. The 110-kDa polypeptide of spinach plastid DNA-dependent RNApolymerase: single-subunit enzyme or catalytic core of multimeric enzymecomplexes? Proc Natl Acad Sci USA 1993;90:5509–13.

Lerbs-Mache S. Function of plastid sigma factors in higher plants: regulation ofgene expression or just preservation of constitutive transcription? Plant MolBiol 2010., doi:10.1007/s11103-010-9714-4.

Li XQ, Zhang M, Brown GG. Cell-specific expression of mitochondrial transcripts inmaize seedlings. Plant Cell 1996;8:1961–75.

Liere K, Link G. Structure and expression characteristics of the chloroplast DNA
region containing the split gene for tRNA(Gly) (UCC) from mustard (Sinapis albaL.). Curr Genet 1994;26:557–63.
Liere K, Maliga P. In vitro characterization of the tobacco rpoB promoter reveals a coresequence motif conserved between phage-type plastid and plant mitochondrialpromoters. EMBO J 1999a;18:249–57.

1 t Phys

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

LL

M

M

M

M

M

M

M

M

M

M

M

M

M


iere K, Maliga P. Novel in vitro transcription assay indicates that the accD NEP pro-moter is contained in a 19 bp fragment. In: Argyroudi-Akoyunoglou JH, Senger H,editors. The chloroplast: from molecular biology to biotechnology. Amsterdam:Kluwer Academic Publishers; 1999b. p. 79–84.

iere K, Maliga P. Plastid RNA polymerases in higher plants. In: Andersson B, AroE-M, editors. Regulation of photosynthesis. Netherlands, Dordrecht: KluwerAcademic Publishers; 2001. p. 29–49.

iere K, Kaden D, Maliga P, Börner T. Overexpression of phage-type RNA polymeraseRpoTp in tobacco demonstrates its role in chloroplast transcription by recogniz-ing a distinct promoter type. Nucleic Acids Res 2004;32:1159–65.

iere K, Börner T. Transcription of plastid genes. In: Grasser KD, editor. Reg-ulation of transcription in plants. Oxford: Blackwell Publishing; 2007a. p.184–224.

iere K, Börner T. Transcription and transcriptional regulation in plastids. In: BockR, editor. Topics in current genetics: cell and molecular biology of plastids.Berlin/Heidelberg: Springer; 2007b. p. 121–74.

iere K, Börner T. Transcription in plant mitochondria. In: Kempken F, editor. Plantmitochondria. New York: Springer; 2011. p. 85–105.

ink G. Green life: control of chloroplast gene transcription. Bioessays 1996;18:465–71.

ink G. Redox regulation of chloroplast transcription. Antioxid Redox Signal2003;5:79–87.

itonin D, Sologub M, Shi Y, Savkina M, Anikin M, Falkenberg M, Gustafsson C, Temi-akov D. Human mitochondrial transcription revisited: only TFAM and TFB2 Mare required for transcription of the mitochondrial genes in vitro. J Biol Chem2010;285:18129–33.

ittle MC, Hallick RB. Chloroplast rpoA, rpoB, and rpoC genes specify at least threecomponents of a chloroplast DNA-dependent RNA polymerase active in tRNAand mRNA transcription. J Biol Chem 1988;263:14302–7.

izama L, Holuigue L, Jordana X. Transcription initiation sites for the potatomitochondrial gene coding for subunit 9 of ATP synthase (atp9). FEBS Lett1994;349:243–8.

oiseaux S, Mache R, Rozier C. Rifampicin inhibition of the plastid rRNA synthesis ofMarchantia polymorpha. J Cell Sci 1975;17:327–35.

oschelder H, Homann A, Ogrzewalla K, Link G. Proteomics-based sequence analysisof plant gene expression—the chloroplast transcription apparatus. Phytochem-istry 2004;65:1785–93.

upold DS, Caoile AGFS, Stern DB. Genomic context influences the activity of maizemitochondrial cox2 promoters. Proc Natl Acad Sci USA 1999a;96:11670–5.

upold DS, Caoile AG, Stern DB. The maize mitochondrial cox2 gene has five promot-ers in two genomic regions, including a complex promoter consisting of sevenoverlapping units. J Biol Chem 1999b;274:3897–903.

usson NA, Delavault PM, Thalouarn PA. The rbcL gene from the non-photosyntheticparasite Lathraea clandestina is not transcribed by a plastid-encoded RNA poly-merase. Curr Genet 1998;34:212–5.

ysenko E. Plant sigma factors and their role in plastid transcription. Plant Cell Rep2007;26:845–59.

ysenko EA, Kuznetsov VV. Plastid RNA polymerases. Mol Biol 2005;39:661–74.ysenko EA. Analysis of the evolution of the family of the Sig genes encoding plant

sigma factors. Russ J Plant Physiol 2006;53:605–14.aier UG, Bozarth A, Funk HT, Zauner S, Rensing SA, Schmitz-Linneweber C, Börner

T, Tillich M. Complex chloroplast RNA metabolism: just debugging the geneticprogramme? BMC Biol 2008;6:36.

aliga P. Two plastid polymerases of higher plants: an evolving story. Trends PlantSci 1998;3:4–6.

arano MR, Carrillo N. Constitutive transcription and stable RNA accumulationin plastids during the conversion of chloroplasts to chromoplasts in ripeningtomato fruits. Plant Physiol 1992;100:1103–13.

artin W, Herrmann RG. Gene transfer from organelles to the nucleus: how much,what happens, and why? Plant Physiol 1998;118:9–17.

artin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B,Hasegawa M, Penny D. Evolutionary analysis of Arabidopsis, cyanobacterial, andchloroplast genomes reveals plastid phylogeny and thousands of cyanobacterialgenes in the nucleus. Proc Natl Acad Sci USA 2002;99:12246–51.

artin W. Gene transfer from organelles to the nucleus: frequent and in big chunks.Proc Natl Acad Sci USA 2003;100:8612–4.

athews DE, Durbin RD. Tagetitoxin inhibits RNA synthesis directed by RNApolymerases from chloroplasts and Escherichia coli. J Biol Chem 1990;265:493–8.

atsunaga M, Jaehning JA. Intrinsic promoter recognition by a “core” RNA poly-merase. J Biol Chem 2004;279:44239–42.

ayfield SP, Yohn CB, Cohen A, Danon A. Regulation of chloroplast gene expression.Annu Rev Plant Physiol Plant Mol Biol 1995;46:147–66.

isquitta RW, Herrin DL. Circadian regulation of chloroplast gene transcription: areview. Plant Tissue Cult 2005;15:83–101.

iyagi T, Kapoor S, Sugita M, Sugiura M. Transcript analysis of the tobaccoplastid operon rps2/atpI/H/F/A reveals the existence of a non-consensus typeII (NCII) promoter upstream of the atpI coding sequence. Mol Gen Genet1998;257:299–307.

ochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J. Arabidopsis genomes uncou-pled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit
in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 2001;98:2053–8.
ochizuki T, Onda Y, Fujiwara E, Wada M, Toyoshima Y. Two independent lightsignals cooperate in the activation of the plastid psbD blue light-responsivepromoter in Arabidopsis. FEBS Lett 2004;571:26–30.

iology 168 (2011) 1345– 1360

Moller SG, Kim YS, Kunkel T, Chua NH. PP7 is a positive regulator of blue lightsignaling in Arabidopsis. Plant Cell 2003;15:1111–9.

Monde RA, Schuster G, Stern DB. Processing and degradation of chloroplast mRNA.Biochimie 2000;82:573–82.

Monte E, Tepperman JM, Al-Sady B, Kaczorowski KA, Alonso JM, Ecker JR, Li X, ZhangY, Quail PH. The phytochrome-interacting transcription factor, PIF3, acts early,selectively, and positively in light-induced chloroplast development. Proc NatlAcad Sci USA 2004;101:16091–8.

Morden CW, Delwiche CF, Kuhsel M, Palmer JD. Gene phylogenies and the endosym-biotic origin of plastids. Biosystems 1992;28:75–90.

Morikawa K, Ito S, Tsunoyama Y, Nakahira Y, Shiina T, Toyoshima Y. Circadian-regulated expression of a nuclear encoded plastid sigma factor gene (sigA) inwheat seedlings. FEBS Lett 1999;451:275–8.

Morikawa K, Shiina T, Murakami S, Toyoshima Y. Novel nuclear-encoded proteinsinteracting with a plastid sigma factor, Sig1, in Arabidopsis thaliana. FEBS Lett2002;514:300–4.

Muise RC, Hauswirth WW. Transcription in maize mitochondria: effects of tissueand mitochondrial genotype. Curr Genet 1992;22:235–42.

Muise RC, Hauswirth WW. Selective DNA amplification regulates transcript levelsin plant mitochondria. Curr Genet 1995;28:113–21.

Mullet JE, Orozco EM, Chua N-H. Multiple transcripts for higher plant rbcL and atpBgenes and localization of the transcription initiation sites of the rbcL gene. PlantMol Biol 1985;4:39–54.

Mullet JE. Dynamic regulation of chloroplast transcription. Plant Physiol1993;103:309–13.

Mulligan RM, Lau GT, Walbot V. Numerous transcription initiation sites exist for themaize mitochondrial genes for subunit 9 of the ATP synthase and subunit 3 ofcytochrome oxidase. Proc Natl Acad Sci USA 1988;85:7998–8002.

Mulligan RM, Leon P, Walbot V. Transcription and posttranscriptional regulation ofmaize mitochondrial gene expression. Mol Cell Biol 1991;11:533–43.

Nagashima A, Hanaoka M, Shikanai T, Fujiwara M, Kanamaru K, Takahashi H, TanakaK. The multiple-stress responsive plastid sigma factor, SIG5, directs activationof the psbD blue light-responsive promoter (BLRP) in Arabidopsis thaliana. PlantCell Physiol 2004a;45:357–68.

Nagashima A, Hanaoka M, Motohashi R, Seki M, Shinozaki K, Kanamaru K, TakahashiH, Tanaka K. DNA microarray analysis of plastid gene expression in an Arabidopsismutant deficient in a plastid transcription factor sigma, SIG2. Biosci BiotechnolBiochem 2004b;68:694–704.

Nakahira Y, Baba K, Yoneda A, Shiina T, Toyoshima Y. Circadian-regulated transcrip-tion of the psbD light-responsive promoter in wheat chloroplasts. Plant Physiol1998;118:1079–88.

Nakamura T, Furuhashi Y, Hasegawa K, Hashimoto H, Watanabe K, Obokata J, SugitaM, Sugiura M. Array-based analysis on tobacco plastid transcripts: preparationof a genomic microarray containing all genes and all intergenic regions. PlantCell Physiol 2003;44:861–7.

Nayak D, Guo Q, Sousa R. A promoter recognition mechanism common toyeast mitochondrial and phage T7 RNA polymerases. J Biol Chem 2009;284:13641–7.

Neuhaus H, Link G. The chloroplast psbK operon from mustard (Sinapis alba L.):multiple transcripts during seedling development and evidence for divergentoverlapping transcription. Curr Genet 1990;18:377–83.

Newton KJ, Winberg B, Yamato K, Lupold S, Stern DB. Evidence for a novel mito-chondrial promoter preceding the cox2 gene of perennial teosintes. EMBO J1995;14:585–93.

Nickelsen J, Link G. Nucleotide sequence of the mustard chloroplast genes trnH andrps19′ . Nucleic Acids Res 1990;18:1051.

Ogrzewalla K, Piotrowski M, Reinbothe S, Link G. The plastid transcription kinasefrom mustard (Sinapis alba L.). A nuclear-encoded CK2-type chloroplast enzymewith redox-sensitive function. Eur J Biochem 2002;269:3329–37.

Oikawa K, Fujiwara M, Nakazato E, Tanaka K, Takahashi H. Characterization of twoplastid sigma factors, SigA1 and SigA2, that mainly function in matured chloro-plasts in Nicotiana tabacum. Gene 2000;261:221–8.

Onda Y, Yagi Y, Saito Y, Takenaka N, Toyoshima Y. Light induction of ArabidopsisSIG1 and SIG5 transcripts in mature leaves: differential roles of cryptochrome1 and cryptochrome 2 and dual function of SIG5 in the recognition of plastidpromoters. Plant J 2008;55:968–78.

Palmer JD, Adams KL, Cho Y, Parkinson CL, Qiu YL, Song K. Dynamic evolution of plantmitochondrial genomes: mobile genes and introns and highly variable mutationrates. Proc Natl Acad Sci USA 2000;97:6960–6.

Parisi MA, Xu B, Clayton DA. A human mitochondrial transcriptional activator canfunctionally replace a yeast mitochondrial HMG-box protein both in vivo and invitro. Mol Cell Biol 1993;13:1951–61.

Park AK, Kim H, Jin HJ. Comprehensive phylogenetic analysis of evolutionarilyconserved rRNA adenine dimethyltransferase suggests diverse bacterial con-tributions to the nucleus-encoded plastid proteome. Mol Phylogenet Evol2009;50:282–9.

Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V,Scharfenberg M, Schneider A, Pfannschmidt T, Leister D. Arabidopsis STN7 kinaseprovides a link between short- and long-term photosynthetic acclimation. PlantCell 2009;21:2402–23.

Pfalz J, Liere K, Kandlbinder A, Dietz K-J, Oelmüller R. pTAC2, -6 and -12 are compo-
nents of the transcriptionally active plastid chromosome that are required forplastid gene expression. Plant Cell 2006;18:176–97.
Pfannschmidt T, Link G. Separation of two classes of plastid DNA-dependentRNA polymerases that are differentially expressed in mustard (Sinapis alba L.)seedlings. Plant Mol Biol 1994;25:69–81.

t Physi

P

P

P

P

P

P

P

P

P

P

P

P

R

R

R

R

R

R

R

R

R

R

S

S

S

S

S

S

S

S


fannschmidt T, Link G. The A and B forms of plastid DNA-dependent RNA poly-merase from mustard (Sinapis alba L.) transcribe the same genes in a differentdevelopmental context. Mol Gen Genet 1997;257:35–44.

fannschmidt T, Nilsson A, Allen JF. Photosynthetic control of chloroplast geneexpression. Nature 1999a;397:625–8.

fannschmidt T, Nilsson A, Tullberg A, Link G, Allen JF. Direct transcriptional controlof the chloroplast genes psbA and psaAB adjusts photosynthesis to light energydistribution in plants. IUBMB Life 1999b;48:271–6.

fannschmidt T, Ogrzewalla K, Baginsky S, Sickmann A, Meyer HE, Link G. Themultisubunit chloroplast RNA polymerase A from mustard (Sinapis alba L.):Integration of a prokaryotic core into a larger complex with organelle-specificfunctions. Eur J Biochem 2000;267:253–61.

fannschmidt T, Liere K. Redox regulation and modification of proteins controllingchloroplast gene expression. Antioxid Redox Signal 2005;7:607–18.

fannschmidt T. Plastidial retrograde signalling—a true “plastid factor” or justmetabolite signatures? Trends Plant Sci 2010;15:427–35.

iechulla B, Gruissem W. Diurnal mRNA fluctuations of nuclear and plastid genes indeveloping tomato fruits. EMBO J 1987;6:3593–9.

reuten T, Cincu E, Fuchs J, Zoschke R, Liere K, Börner T. Fewer genes than organelles:extremely low and variable gene copy numbers in mitochondria of somatic plantcells. Plant J 2010;64:948–59.

rivat I, Hakimi MA, Buhot L, Favory JJ, Mache-Lerbs S. Characterization of Arabidop-sis plastid sigma-like transcription factors SIG1, SIG2 and SIG3. Plant Mol Biol2003;51:385–99.

uthiyaveetil S, Allen JF. A bacterial-type sensor kinase couples electron trans-port to gene expression in chloroplasts. Photosynthesis Energy from the Sun2008:1181–6.

uthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C,van der Giezen M, Rogers MB, Allen JF. The ancestral symbiont sensor kinaseCSK links photosynthesis with gene expression in chloroplasts. Proc Natl AcadSci USA 2008;105:10061–6.

uthiyaveetil S, Ibrahim IM, Jelicic B, Tomasic A, Fulgosi H, Allen JF. Transcriptionalcontrol of photosynthesis genes: the evolutionarily conserved regulatory mech-anism in plastid genome function. Genome Biol Evolut 2010;2:888–96.

aab S, Toth Z, de Groot C, Stamminger T, Hoth S. ABA-responsive RNA-binding pro-teins are involved in chloroplast and stromule function in Arabidopsis seedlings.Planta 2006;224:900–14.

app JC, Baumgartner BJ, Mullet J. Quantitative analysis of transcription and RNAlevels of 15 barley chloroplast genes. Transcription rates and mRNA lev-els vary over 300-fold; predicted mRNA stabilities vary 30-fold. J Biol Chem1992;267:21404–11.

app WD, Lupold DS, Mack S, Stern DB. Architecture of the maize mitochondrialatp1 promoter as determined by linker-scanning and point mutagenesis. MolCell Biol 1993;13:7232–8.

einbothe S, Reinbothe C, Heintzen C, Seidenbecher C, Parthier B. A methyljasmonate-induced shift in the length of the 5′ untranslated region impairstranslation of the plastid rbcL transcript in barley. EMBO J 1993;12:1505–12.

emacle C, Maréchal-Drouard L. Characterization of the potato mitochondrial tran-scription unit containing ‘native’ trnS (GCU), trnF (GAA) and trnP (UGG). PlantMol Biol 1996;30:553–63.

eznikov W, Siegle DA, Cowing DW, Gross CA. The regulation of transcription initi-ation in bacteria. Annu Rev Genet 1985;19:355–87.

ichly E, Leister D. NUMTs in sequenced eukaryotic genomes. Mol Biol Evol2004;21:1081–4.

ichter U, Kiessling J, Hedtke B, Decker E, Reski R, Börner T, Weihe A. Two RpoTgenes of Physcomitrella patens encode phage-type RNA polymerases with dualtargeting to mitochondria and plastids. Gene 2002;290:95–105.

ichter U, Kühn K, Okada S, Brennicke A, Weihe A, Börner T. A mitochondrial rRNAdimethyladenosine methyltransferase in Arabidopsis. Plant J 2010;61:558–69.

odermel S. Pathways of plastid-to-nucleus signaling. Trends Plant Sci2001;6:471–8.

akai A, Saito C, Inada N, Kuroiwa T. Transcriptional activities of the chloroplast-nuclei and proplastid-nuclei isolated from tobacco exhibit different sensitivitiesto tagetitoxin: implication of the presence of distinct RNA polymerases. PlantCell Physiol 1998;39:928–34.

alinas P, Fuentes D, Vidal E, Jordana X, Echeverria M, Holuigue L. An extensive surveyof CK2 � and � subunits in Arabidopsis: multiple isoforms exhibit differentialsubcellular localization. Plant Cell Physiol 2006;47:1295–308.

alvador ML, Klein U, Bogorad L. Light-regulated and endogenous fluctuations ofchloroplast transcript levels in Chlamydomonas. Regulation by transcription andRNA degradation. Plant J 1993;3:213–9.

alvador ML, Klein U, Bogorad L. Endogenous fluctuations of DNA topology in thechloroplast of Chlamydomonas reinhardtii. Mol Cell Biol 1998;18:7235–42.

ato M, Takahashi K, Ochiai Y, Hosaka T, Ochi K, Nabeta K. Bacterial alarmone,guanosine 5′-diphosphate 3′-diphosphate (ppGpp), predominantly binds the�′ subunit of plastid-encoded plastid RNA polymerase in chloroplasts. Chem-biochem 2009;10:1227–33.

ato N. Was the evolution of plastid genetic machinery discontinuous? Trends PlantSci 2001;6:151–5.

ato N, Terasawa K, Miyajima K, Kabeya Y. Organization, developmental dynamics,
and evolution of plastid nucleoids. Int Rev Cytol 2003;232:217–62.
atoh J, Baba K, Nakahira Y, Shiina T, Toyoshima Y. Characterization of dynamics ofthe psbD light-induced transcription in mature wheat chloroplasts. Plant MolBiol 1997;33:267–78.

ology 168 (2011) 1345– 1360 1359

Satoh J, Baba K, Nakahira Y, Tsunoyama Y, Shiina T, Toyoshima Y. Devolpmentalstage-specific multi-subunit plastid RNA polymerases (PEP) in wheat. Plant J1999;18:407–16.

Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesisand function. Physiol Rev 2008;88:611–38.

Schmitz-Linneweber C, Small I. Pentatricopeptide repeat proteins: a socket set fororganelle gene expression. Trends Plant Sci 2008;13:663–70.

Schön A, Krupp G, Gough S, Berry-Lowe S, Kannangara CG, Söll D. The RNA requiredin the first step of chlorophyll biosynthesis is a chloroplast glutamate tRNA.Nature 1986;322:281–4.

Schröter Y, Steiner S, Matthäi K, Pfannschmidt T. Analysis of oligomeric proteincomplexes in the chloroplast sub-proteome of nucleic acid-binding proteinsfrom mustard reveals potential redox regulators of plastid gene expression.Proteomics 2010;10:2191–204.

Schrubar H, Wanner G, Westhoff P. Transcriptional control of plastid gene expressionin greening sorghum seedlings. Planta 1990;183:101–11.

Schubot FD, Chen CJ, Rose JP, Dailey TA, Dailey HA, Wang BC. Crystal structure of thetranscription factor sc-mtTFB offers insights into mitochondrial transcription.Protein Sci 2001;10:1980–8.

Schwacke R, Fischer K, Ketelsen B, Krupinska K, Krause K. Comparative survey ofplastid and mitochondrial targeting properties of transcription factors in Ara-bidopsis and rice. Mol Genet Genomics 2007;277:631–46.

Schweer J, Loschelder H, Link G. A promoter switch that can rescue a plant sigmafactor mutant. FEBS Lett 2006;580:6617–22.

Schweer J, Geimer S, Meurer J, Link G. Arabidopsis mutants carrying chimeric sigmafactor genes reveal regulatory determinants for plastid gene expression. PlantCell Physiol 2009;50:1382–6.

Schweer J. Plant sigma factors come of age: flexible transcription factor network forregulated plastid gene expression. Endocytobio Cell Res 2010;20:1–20.

Schweer J, Türkeri H, Kolpack A, Link G. Role and regulation of plastid sigma factorsand their functional interactors during chloroplast transcription—recent lessonsfrom Arabidopsis thaliana. Eur J Cell Biol 2010a;89:940–6.

Schweer J, Türkeri H, Link B, Link G. AtSIG6, a plastid sigma factor from Ara-bidopsis, reveals functional impact of cpCK2 phosphorylation. Plant J 2010b;62:192–202.

Sellaro R, Crepy M, Trupkin SA, Karayekov E, Buchovsky AS, Rossi C, Casal JJ. Cryp-tochrome as a sensor of the blue/green ratio of natural radiation in Arabidopsis.Plant Physiol 2010;154:401–9.

Serino G, Maliga P. RNA polymerase subunits encoded by the plastid rpo genesare not shared with the nucleus-encoded plastid enzyme. Plant Physiol1998;117:1165–70.

Severinov K, Mustaev A, Kukarin A, Muzzin O, Bass I, Darst SA, Goldfarb A. Structuralmodules of the large subunits of RNA polymerase. Introducing archaebacterialand chloroplast split sites in the beta and beta’ subunits of Escherichia coli RNApolymerase. J Biol Chem 1996;271:27969–74.

Sexton TB, Christopher DA, Mullet JE. Light-induced switch in barley psbD-psbC pro-moter utilization: a novel mechanism regulating chloroplast gene expression.EMBO J 1990;9:4485–94.

Shen Y-Y, Wang X-F, Wu F-Q, Du S-Y, Cao Z, Shang Y, Wang X-L, Peng C-C, Yu X-C,Zhu S-Y, Fan R-C, Xu Y-H, Zhang D-P. The Mg-chelatase H subunit is an abscisicacid receptor. Nature 2006;443:823–6.

Shiina T, Allison L, Maliga P. rbcL transcript levels in tobacco plastids are independentof light: reduced dark transcription rate is compensated by increased mRNAstability. Plant Cell 1998;10:1713–22.

Shiina T, Tsunoyama Y, Nakahira Y, Khan MS. Plastid RNA polymerases, promot-ers, and transcription regulators in higher plants. Int Rev Cytol 2005;244:1–68.

Shiina T, Ishizaki Y, Yagi Y, Nakahira Y. Function and evolution of plastid sigmafactors. Plant Biotechnol 2009;26:57–66.

Shimizu M, Kato H, Ogawa T, Kurachi A, Nakagawa Y, Kobayashi H. Sigma factorphosphorylation in the photosynthetic control of photosystem stoichiometry.Proc Natl Acad Sci USA 2010;107:10760–4.

Shinozaki K, Sugiura M. The nucleotide sequence of the tobacco chloroplast genefor the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Gene1982;20:91–102.

Shutt TE, Lodeiro MF, Cotney J, Cameron CE, Shadel GS. Core human mitochondrialtranscription apparatus is a regulated two-component system in vitro. Proc NatlAcad Sci USA 2010;107:12133–8.

Siemenroth A, Wollgiehn R, Neumann D, Börner T. Synthesis of ribosomal RNA inribosome-deficient plastids of the mutant “albostrians” of Hordeum vulgare L.Planta 1981;153:547–55.

Silhavy D, Maliga P. Mapping of the promoters for the nucleus-encoded plastid RNApolymerase (NEP) in the iojap maize mutant. Curr Genet 1998a;33:340–4.

Silhavy D, Maliga P. Plastid promoter utilization in a rice embryonic cell culture. CurrGenet 1998b;34:67–70.

Smith AC, Purton S. The transcriptional apparatus of algal plastids. Eur J Pharmacol2002;37:301–11.

Sriraman P, Silhavy D, Maliga P. The phage-type PclpP-53 plastid promoter comprisessequences downstream of the transcription initiation site. Nucleic Acids Res1998;26:4874–9.

Stegemann S, Bock R. Experimental reconstruction of functional gene transfer from
the tobacco plastid genome to the nucleus. Plant Cell 2006;18:2869–78.
Steiner S, Dietzel L, Schröter Y, Fey V, Wagner R, Pfannschmidt T. The role of phos-phorylation in redox regulation of photosynthesis genes psaA and psbA duringphotosynthetic acclimation of mustard. Mol Plant 2009;2:416–29.

1 t Phys

S

S

S

S

S

S

S

T

T

T

T

T

T

T

T

T

T

T

T

T

T

T

T

T


tephenson PG, Fankhauser C, Terry MJ. PIF3 is a repressor of chloroplast develop-ment. Proc Natl Acad Sci USA 2009;106:7654–9.

tern DB, Goldschmidt-Clermont M, Hanson MR. Chloroplast RNA metabolism. AnnuRev Plant Biol 2010;61:125–55.

uck R, Zeltz P, Falk J, Acker A, Kössel H, Krupinska K. Transcriptionally activechromosomes (TACs) of barley chloroplasts contain the �-subunit of plastomeencoded RNA polymerase. Curr Genet 1996;30:515–21.

urzycki SJ. Genetic functions of the chloroplast of Chlamydomonas reinhardii: effectof rifampin on chloroplast DNA-dependent RNA polymerase. Proc Natl Acad SciUSA 1969;63:1327–34.

uzuki JY, Ytterberg AJ, Beardslee TA, Allison LA, Wijk KJ, Maliga P. Affinity purifi-cation of the tobacco plastid RNA polymerase and in vitro reconstitution of theholoenzyme. Plant J 2004;40:164–72.

wiatecka-Hagenbruch M, Liere K, Börner T. High diversity of plastidial promotersin Arabidopsis thaliana. Mol Genet Genomics 2007;277:725–34.

wiatecka-Hagenbruch M, Emanuel C, Hedtke B, Liere K, Börner T. Impaired functionof the phage-type RNA polymerase RpoTp in transcription of chloroplast genesis compensated by a second phage-type RNA polymerase. Nucleic Acids Res2008;36:785–92.

akahashi K, Kasai K, Ochi K. Identification of the bacterial alarmone guano-sine 5′-diphosphate 3′-diphosphate (ppGpp) in plants. Proc Natl Acad Sci USA2004;101:4320–4.

an X-Y, Liu X-L, Wang W, Jia D-J, Chen L-Q, Zhang X-Q, Ye D. Mutations in theArabidopsis nuclear-encoded mitochondrial phage-type RNA polymerase geneRPOTm led to defects in pollen tube growth, female gametogenesis and embryo-genesis. Plant Cell Physiol 2010;51:635–49.

anaka K, Tozawa Y, Mochizuki N, Shinozaki K, Nagatani A, Wakasa K, Takahashi H.Characterization of three cDNA species encoding plastid RNA polymerase sigmafactors in Arabidopsis thaliana: evidence for the sigma factor heterogeneity inhigher plant plastids. FEBS Lett 1997;413:309–13.

epperman JM, Hwang Y-S, Quail PH. phyA dominates in transduction of red-lightsignals to rapidly responding genes at the initiation of Arabidopsis seedling de-etiolation. Plant J 2006;48:728–42.

hompson RJ, Mosig G. Light affects the structure of Chlamydomonas chloroplastchromosomes. Nucleic Acids Res 1990;18:2625–31.

hum KE, Kim M, Morishige DT, Eibl C, Koop H-U, Mullet JE. Analysis of barley chloro-plast psbD light-responsive promoter elements in transplastomic tobacco. PlantMol Biol 2001;47:353–66.

iller K, Link G. Phosphorylation and dephosphorylation affect functional character-istics of chloroplast and etioplast transcription systems from mustard (Sinapisalba L.). EMBO J 1993;12:1745–53.

immis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organellegenomes forge eukaryotic chromosomes. Nat Rev Genet 2004;5:123–35.

o KY, Cheng MC, Suen DF, Mon DP, Chen LFO, Chen SCG. Characterization of thelight-responsive promoter of rice chloroplast psbD-C operon and the sequence-specific DNA binding factor. Plant Cell Physiol 1996;37:660–6.

okuhisa JG, Vijayan P, Feldmann KA, Browse JA. Chloroplast development at lowtemperatures requires a homolog of DIM1, a yeast gene encoding the 18S rRNAdimethylase. Plant Cell 1998;10:699–712.

opping J, Leaver C. Mitochondrial gene expression during wheat leaf development.Planta 1990;182:399–407.

oulokhonov II, Shulgina I, Hernandez VJ. Binding of the transcription effector ppGppto Escherichia coli RNA polymerase is allosteric, modular, and occurs near the Nterminus of the beta’-subunit. J Biol Chem 2001;276:1220–5.

ozawa Y, Tanaka K, Takahashi H, Wakasa K. Nuclear encoding of a plastid sigmafactor in rice and its tissue- and light-dependent expression. Nucleic Acids Res1998;26:415–9.

racy RL, Stern DB. Mitochondrial transcription initiation: promoter structures andRNA polymerases. Curr Genet 1995;28:205–16.

rifa Y, Privat I, Gagnon J, Baeza L, Lerbs-Mache S. The nuclear RPL4 gene encodesa chloroplast protein that co-purifies with the T7-like transcription complex aswell as plastid ribosomes. J Biol Chem 1998;273:3980–5.

sunoyama Y, Morikawa K, Shiina T, Toyoshima Y. Blue light specific and differen-tial expression of a plastid sigma factor, Sig5 in Arabidopsis thaliana. FEBS Lett
2002;516:225–8.
sunoyama Y, Ishizaki Y, Morikawa K, Kobori M, Nakahira Y, Takeba G, ToyoshimaY, Shiina T. Blue light-induced transcription of plastid-encoded psbD gene ismediated by a nuclear-encoded transcription initiation factor, AtSig5. Proc NatlAcad Sci USA 2004;101:3304–9.

iology 168 (2011) 1345– 1360

van der Biezen EA, Sun J, Coleman MJ, Bibb MJ, Jones JD. Arabidopsis RelA/SpoThomologs implicate (p)ppGpp in plant signaling. Proc Natl Acad Sci USA2000;97:3747–52.

Vera A, Hirose T, Sugiura M. A ribosomal protein gene (rpl32) from tobaccochloroplast DNA is transcribed from alternative promoters—similarities in pro-moter region organization in plastid housekeeping genes. Mol Gen Genet1996;251:518–25.

Wada T, Tunoyama Y, Shiina T, Toyoshima Y. In vitro analysis of light-inducedtranscription in the wheat psbD/C gene cluster using plastid extracts fromdark-grown and short-term-illuminated seedlings. Plant Physiol 1994;104:1259–67.

Wagner R, Pfannschmidt T. Eukaryotic transcription factors in plastids—bioinformatic assessment and implications for the evolution of gene expressionmachineries in plants. Gene 2006;381:62–70.

Warmke HE, Lee SL. Pollen abortion in T cytoplasmic male-sterile corn (Zea mays):a suggested mechanism. Science 1978;200:561–3.

Weihe A, Börner T. Transcription and the architecture of promoters in chloroplasts.Trends Plant Sci 1999;4:169–70.

Weihe A. The transcription of plant organelle genomes. In: Daniell H, Chase CD,editors. Molecular biology and biotechnology of plant organelles. Dordrecht:Kluwer Academic Publishers; 2004. p. 213–37.

Weihe A, Liere K, Börner T. Transcription and transcript regulation in chloroplastsand mitochondria. In: Bullerwell CE, editor. Organelle genetics: evolution oforganelle genomes and gene expression. New York: Springer; in press.

Woloszynska M, Trojanowski D. Counting mtDNA molecules in Phaseolus vulgaris:sublimons are constantly produced by recombination via short repeats andundergo rigorous selection during substoichiometric shifting. Plant Mol Biol2009;70:511–21.

Wu CY, Lin CH, Chen LJ. Identification of the transcription start site for the spinachchloroplast serine tRNA gene. FEBS Lett 1997;418:157–61.

Wurbs D, Ruf S, Bock R. Contained metabolic engineering in tomatoes by expres-sion of carotenoid biosynthesis genes from the plastid genome. Plant J2007;49:276–88.

Xie G, Allison LA. Sequences upstream of the YRTA core region are essential fortranscription of the tobacco atpB NEP promoter in chloroplasts in vivo. CurrGenet 2002;41:176–82.

Xu B, Clayton DA. Assignment of a yeast protein necessary for mitochondrial tran-scription initiation. Nucleic Acids Res 1992;20:1053–9.

Yan B, Pring DR. Transcriptional initiation sites in Sorghum mitochondrial DNA indi-cate conserved and variable features. Curr Genet 1997;32:287–95.

Yang J, Stern DB. The spinach chloroplast endoribonuclease CSP41 cleaves the 3′-untranslated region of petD mRNA primarily within its terminal stem-loopstructure. J Biol Chem 1997;272:12874–80.

Yao J, Roy-Chowdhury S, Allison LA. AtSig5 is an essential nucleus-encoded Ara-bidopsis �-like factor. Plant Physiol 2003;132:739–47.

Yin C, Richter U, Börner T, Weihe A. Evolution of phage-type RNA polymerases inhigher plants: characterization of the single phage-type RNA polymerase genefrom Selaginella moellendorffii. J Mol Evol 2009;68:528–38.

Yin C, Richter U, Börner T, Weihe A. Evolution of plant phage-type RNA polymerases:the genome of the basal angiosperm Nuphar advena encodes two mitochon-drial and one plastid phage-type RNA polymerases. BMC Evolutionary Biology2010;10:379.

Zengel JM, Mueckl D, Lindahl L. Protein L4 of the E. coli ribosome regulates an elevengene r protein operon. Cell 1980;21:523–35.

Zer H, Ohad I. Light, redox state, thylakoid-protein phosphorylation and signalinggene expression. Trends Biochem Sci 2003;28:467–70.

Zoschke R, Liere K, Börner T. From seedling to mature plant: Arabidopsis plastidialgenome copy number, RNA accumulation and transcription are differentiallyregulated during leaf development. Plant J 2007;50:710–22.

Zubo YO, Lysenko E, Aleinikova A, Kusnetsov V, Pshibytko N. Changes in the tran-scriptional activity of barley plastome genes under heat shock. Russ J PlantPhysiol 2008a;55:293–300.

Zubo YO, Yamburenko MV, Selivankina SY, Shakirova FM, Avalbaev AM, KudryakovaNV, Zubkova NK, Liere K, Kulaeva ON, Kusnetsov VV, Börner T. Cytokinin
stimulates chloroplast transcription in detached barley leaves. Plant Physiol2008b;148:1082–93.
Zubo YO, Yamburenko MV, Kusnetsov VV, Börner T. Methyl jasmonate, gibberellicacid and auxin affect transcription and transcript accumulation of chloroplastgenes. J Plant Physiol 2011;168:1335–44.

the transcription machineries of plant mitochondria and chloroplasts

Documents