Plant evolution: AGC kinases tell theauxin taleCarlos S. Galvan-Ampudia and Remko Offringa

Leiden University, Institute of Biology, Molecular and Developmental Genetics, Clusius Laboratory, Wassenaarseweg 64, 2333 AL

Leiden, The Netherlands

Opinion TRENDS in Plant Science Vol.12 No.12

The signaling molecule auxin is a central regulator ofplant development, which instructs tissue and organpatterning, and couples environmental stimuli to devel-opmental responses. Here, we discuss the function ofPINOID (PID) and the phototropins, members of theplant specific AGCVIII protein kinases, and their role intriggering and regulating development by controllingPIN-FORMED (PIN) auxin transporter-generated auxingradients and maxima. We propose that the AGCVIIIkinase gene family evolved from an ancestral phototro-pin gene, and that the co-evolution of PID-like and PINgene families marks the transition of plants from waterto land. We hypothesize that the PID-like kinases func-tion in parallel to, or downstream of, the phototropins toorient plant development by establishing the direction ofpolar auxin transport.

Plant development directed by the hormone auxinThe development of flowering plants is dualistic: on the onehand, it follows strict programs producing uniform flowersand embryos; on the other hand, it can be flexible, particu-larly during vegetative development. In view of the pre-dominantly sessile nature of plants, this flexibledevelopment is crucial to enable adaptation to changesin the environment. The plant hormone auxin is wellrecognized as a central regulator of both flexible growthresponses, such as tropisms, and strict developmentalprograms, such as organ formation and patterning [1–5].A characteristic of this signaling molecule is that it isactively transported in a directional manner, for examplefrom young developing aerial organs to the root system.This polar auxin transport (PAT) generates auxin maximaand gradients, which are instrumental in directing growthand in positioning the formation of new organs. The PIN-FORMED (PIN) auxin efflux carriers have been charac-terized as central rate-limiting components that determinethe direction of auxin transport through their asymmetricsubcellular localization (Box 1 and reviewed in Refs [6–8])[6–10].

The only component in the polar targeting of PINproteins that has so far been identified is the PINOID(PID) protein kinase [11]. The PID gene was identifiedthrough Arabidopsis pid loss-of-function mutants, whichphenocopy a mutant in the PIN-FORMED1 (PIN1) auxinefflux carrier gene. The phenotype of the pid mutant

Corresponding author: Offringa, R. (r.offringa@biology.leidenuniv.nl).

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already suggested a role for PID as a regulator of PAT[12,13]. Recently, it was shown that PID is necessary forproper apical localization of PIN1 proteins in epidermalcells of the inflorescence meristem, which is required togenerate auxin maxima in the meristem that are initiationpoints for lateral organ formation. In pid loss-of-functionmutants, PIN1 localizes at the basal membrane, whichdeprives themeristem of auxin, and prevents the initiationand positioning of new lateral organs, thus resulting in thepin-shaped inflorescences that are characteristic of the pidmutant [11]. The action of PID does not seem to berestricted to the polar targeting of PIN1, because over-expression of PID results in a basal-to-apical (bottom-to-top) switch of PIN1, as well as PIN2 and PIN4, in rootmeristem cells. The fact that different PIN proteins areapicalized in response to PID and that PID expression isupregulated by auxin, suggests that PID is involved infeedback control of PAT [11,12,14–16].

A previous comparison of the PID protein kinase withknown kinases indicated that it belongs to the plant-specific AGCVIII protein serine-threonine kinase family[12,17]. AGC kinases are named after protein kinase A(PKA), cyclic GMP-dependent protein kinases (PKG) andprotein kinase C (PKC), three classes of animal proteinkinases that are involved in receptor-mediated growthfactor signal transduction. We have performed a detailedbioinformatic analysis of the Arabidopsis AGCVIII kinasefamily, which, besides PID, also comprises the well-knownphototropins [18], and have studied their evolutionaryorigin and function in plant development. We hypothesizethat AGCVIII kinases evolved from an ancestral photo-tropin, and that the acquisition of PID and the PIN trans-porters in plant evolution marks the transition of plantsfrom water to land. Below we summarize the data thatsupport our hypothesis.

The plant-specific characteristics of the AGCVIIIkinasesTheArabidopsis genome encodes 37 AGC kinases, of which23 classify to the AGCVIII group (see Figure S1 in theonline supplementary material). Flowering plants do nothave the typical animal PKA, PKC and PKG kinases. TheAGCVIII kinases might therefore represent plant ortho-logs of these animal kinases.

One characteristic ofmembers of the AGCVIII subfamilyis the substitution of the conservedDFGamino acidmotif insubdomain VII of the catalytic domain for the DFD aminoacid triplet (Figure 1a). The DFD triplet is not plant-specific

d. doi:10.1016/j.tplants.2007.10.004

Box 1. Fine tuning PID-dependent polar localization of PIN

proteins

The chemiosmotic hypothesis proposed in the 1970s for auxin

transport predicted that asymmetrically distributed auxin efflux

carriers are the drivers of PAT. Two types of proteins have now been

acknowledged as auxin efflux carriers. First, the PIN family of

transporters was identified through the Arabidopsis pin-formed and

ethylene-insensitive root 1 mutants that phenocopied wild-type

plants grown on PAT inhibitors. These mutants led to the cloning of

PIN1 and PIN2 respectively, and the subsequent identification of six

other PIN genes in the Arabidopsis genome. PIN1, 2, 3, 4 and 7 show

different tissue- and cell-type specific asymmetric subcellular

localizations and have crucial roles in phyllotaxis, tropic growth

and embryo patterning [8]. The localization and function of PIN5, 6

and 8 is still unknown [8]. In addition, several multi-drug-resistant/P-

glycoprotein (MDR/PGP)-type ATP-binding cassette (ABC) proteins

were shown to act as auxin-efflux carriers [37]. In contrast to PIN

proteins, MDR/PGP proteins in most cases do not show a

pronounced asymmetric subcellular localization, and it is as yet

unclear whether they are part of the PIN-dependent, or another

parallel, auxin transport pathway [8,37].

The PID protein kinase is the first, and for now only, identified

determinant of the polar targeting of PIN proteins [11]. PID kinase

activity is regulated by three factors: (i) by phosphorylation of the

catalytic activation loop by 3-phosphoinositide-dependent kinase 1

(PDK1), which enhances PID kinase activity [19,41]; (ii) by phos-

phorylated phosphatidylinositols (PIP2) and phosphatidic acid (PA),

phospholipids that bind PID most strongly and most probably

enable its association with the plasma membrane [19]; and (iii) by

Ca2+-binding proteins, which bind to PID in a calcium-dependent

manner and regulate its kinase activity [40]. At the plasma

membrane, PID partially co-localizes with PIN proteins [15,35].

Overexpression of a functional PID:GFP fusion in Arabidopsis

indicates that the subcellular localization of PID in the root meristem

is cell-type specific (Figure 3d–f). In columella cells, PID shows

random non-polar localization (Figure 3d), similar to PIN3 [39],

whereas in the epidermal cell layer, PID shows apico-basal polarity

(Figure 3d and e) that partially overlaps with PIN2 [11,35]. Recently,

evidence was found for direct phosphorylation of PIN proteins by

PID [35]. How exactly this phosphorylation affects the polar

subcellular localization of PIN proteins is still unknown. It is

probable, however, that PID-dependent polar targeting of PINs is

tightly regulated by a combined action of PDK1, phospholipids and

Ca2+-binding proteins.

542 Opinion TRENDS in Plant Science Vol.12 No.12

and defines a class of AGCprotein kinases that can be foundin all eukaryotes. Another characteristic is the presence ofan amino acid insertion between the conserved subdomainsVII and VIII of the catalytic domain (VII–VIII insertion),which ranges from 36 to 90 residues in the Arabidopsisfamily members (Figure 1a and b). The insertion in combi-nation with the DFD triplet is specific for the plant AGCgroup of protein kinases. Recent data suggest a role for theVII–VIII insertion in the subcellular localization of theseprotein kinases [19] (Box 1).

Phylogeny of the Arabidopsis AGCVIII kinasesTo determine the evolutionary relationships between themembers of the Arabidopsis AGCVIII subfamily, thesequences corresponding to the catalytic domain were usedto construct an AGCVIII-specific phylogenetic tree(Figure 1b). In a previous phylogenetic analysis usingthe full length amino acid sequences, the plant AGCkinases were classified into two groups [20]. However, inour analysis, we found that AGCVIII kinases classify intofour distinct groups, which we named AGC1–AGC4(Figure 1). The largest group (AGC1) is formed by 13

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putative protein kinases and comprises orthologs of thefirst protein kinases to be identified in plants; for example,Phaseolus vulgaris protein kinase 1 (PvPK1) [21]. TheAGC4 group is formed by the phototropins PHOT1 andPHOT2, which are characterized by an N-terminal photo-receptor domain with two chromophore-binding LOV(light, oxygen, voltage) domains and a C-terminal proteinkinase domain [22]. PID, AGC3–4,WAG1 andWAG2 [‘wag’after the phenotype of the corresponding mutants, whichhave an enhanced sinusoidal growth of the root, alsoknown as root waving (reviewed in Ref. [23])] form thethird group (AGC3). The kinases within these three sub-groups share conserved residues within the VII–VIII inser-tion, including a conserved AEP amino acid triplet that islocated close to subdomain VIII (Figure 1a). Interestingly,this AEP triplet is not found in the four remaining kinasesthat form the AGC2 group, which demonstrates that theyare more distantly related to phototropins than was pre-viously thought [20] (Figure 1).

The genes encodingAGCVIIImembers are not clusteredor do not show a clear organization in the Arabidopsisgenome [19] (Figure 1b). Five of the genes do not contain anintron, whereas the other 18 genes contain one or moreintrons. Interestingly, one intron is found inmembers of allfour groups at a conserved position in the region encodingkinase subdomain VIa (Figure 1b), indicating that theAGCVIII genes originate from a single ancestral kinase.Arabidopsis PHOT1 and PHOT2 carry multiple introns atidentical positions, corroborating their relatedness.

In conclusion, our analysis of the Arabidopsis AGCVIIIkinases shows that they classify into four groups, andindicates that the encoding gene family originated froma single ancestral kinase gene through multiple indepen-dent duplication steps. Interestingly, each group seems toperform a different function in plants, with AGC1 kinaseshaving a role in cell organization [24], AGC2 kinases instress responses [25,26], AGC3 kinases in the regulation ofPAT [12,27], and AGC4 kinases in chloroplast avoidanceand phototropism [28,29]. The last two subgroups haveclear links with PAT and will therefore be discussed inmore detail.

Phototropins – remnants of the ancestral plantAGCVIII kinasePhototropins, which constitute the AGC4 group, were dis-covered through a screen forArabidopsismutants that lackdirective growth of the hypocotyl of dark-grown seedlingstowards a blue light source [29]. This screen identifiedseveral non-phototropic mutants, one of which is mutatedin the gene encoding the blue light receptor PHOT1 [18,29].The Arabidopsis genome also encodes a homolog of PHOT1known as PHOT2 [18]. PHOT1 is the major player in thephototropic growth of seedling hypocotyls and roots at lowintensity light conditions, whereas PHOT2 functions intriggering the auxin-mediated phototropic response underhigh intensity light conditions. Moreover, the PHOTs havebeen found to function redundantly in blue-light-inducedchloroplast movement and stomatal opening [22].

Phototropins are the only members of the AGCVIIIfamily so far identified in unicellular green algae. There-fore, they might represent the first descendants of the

Figure 1. The Arabidopsis AGCVIII protein kinase family. (a) Schematic representation of the catalytic kinase domain of the Arabidopsis AGCVIII protein kinases. The eleven

conserved subdomains of the catalytic kinase domain are represented as blue boxes labeled with Roman numbers. The (length of the) amino acid insertion between sub-

domains VII and VIII (red), the typical DFD (Asp-Phe-Asp) signature in sub-domain VII (green), the conserved basic pocket (purple), and the AEP (Ala-Glu-Pro) triplet close to

sub-domain VIII (blue) are indicated. (b) Phylogenetic tree of the 23 Arabidopsis AGCVIII protein kinases based on an alignment of their catalytic kinase domains subdivides

the Arabidopsis AGCVIII kinases into four distinct groups. A comparison of the total protein size, the length of the VII–VIII insertion and the intron positions within the region

coding for the catalytic domain is indicated. The positions of the highly conserved intron (red arrowheads) and the more variable introns (orange, white and yellow

arrowheads) are indicated.

Opinion TRENDS in Plant Science Vol.12 No.12 543

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Table 1. Overview of the occurrence of the AGCVIII kinases and the PIN auxin efflux carriers in different representatives of the plantkingdom

AGC4c

Family Genus PINc PHOT2 PHOT1 AGC3c AGC1c AGC2c

Chlorophyta (green algae) Ostreococcusa � + � � � �Chlamydomonasb � + � � � �Mougeotiab � + � � � �

Embryophyta

Bryophytes (mosses) Physcomitrellab + + � + + ?

Pteridophytes (ferns) Adiantumb + + � + ? ?

Spermatophyta (seed plants)

Gymnosperms Pinusb + + + + + +

Monocots Oryzaa + + + + + +

Zeab + + + + + +

Dicots Medicagoa + + + + + +

Arabidopsisa + + + + + +aComplete genome sequence is available.bAnalysis is based on EST databases.c+ present, � absent, ? not found in databases.

544 Opinion TRENDS in Plant Science Vol.12 No.12

ancestral AGCVIII protein kinase. The PHOT gene of thegreen algaChlamydomonas can partially restore phototrop-ism, chloroplast positioning and stomatal opening inresponse to blue light when expressed in the Arabidopsisphot1 phot2 doublemutant [30], indicating that phototropinfunction and signaling is conserved in plants and algae. Acomparison of catalytic kinase domains of 31 selected photo-tropin-related proteins from14 representative plant speciesrevealed two major groups (see Figure S2 in the online

Figure 2. The phototropins and the AGC3 kinases recapitulate plant evolution. Phylog

biosynthesis, or genes encoding phototropins, AGC3 (PINOID-like) kinases, MDR/PGP

identified in a range of green plants, from unicellular algae to angiosperms, as have ge

genes encoding the AGC3 kinases and PIN auxin efflux carriers occur only later in evolu

ancient AGCVIII protein kinases from which the other AGCVIII kinases evolved. A duplica

PHOT1 gene, which is found only in spermatophytes.

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supplementary material): (i) the PHOT1-like proteins thatare characterized by the conserved CLTSCKPQ amino acidsignature in the VII–VIII insertion; and (ii) the PHOT2-likeproteins. Interestingly, genes encoding PHOT2-like photo-receptors are found inall plant groups,whereas thePHOT1-like genes are restricted to seedplants (Table 1, Figure2; seeFigure S2 in the online supplementary material).

Taking all these observations into consideration, wespeculate that optimization of light perception mediated

enic tree of the plant kingdom, depicting the presence of genes involved in auxin

transporters and PIN proteins. Auxin and auxin-biosynthesis genes have been

nes encoding PHOT2-like proteins and MDR/PGP transporter proteins. By contrast,

tion in land plants. Therefore, the PHOT2-like proteins probably represent the most

tion of the ancestral PHOT2 gene gave rise to the low-fluence phototropin-encoding

Opinion TRENDS in Plant Science Vol.12 No.12 545

byPHOT2-like proteins, for example thehigh intensity lightavoidance of chloroplasts, is one of the ancient traits in plantevolution. A more detailed analysis and functional charac-terization of phototropins throughout the plant kingdomshould provide further evidence for our hypothesis.

AGC3 kinases direct auxin transportThe PID-containing subgroup (AGC3) is composed of fourgenes in both Arabidopsis and the monocot Oryza sativa.Apart from PID, two other AGC3 members in Arabidopsishave been characterized in more detail: WAG1 andWAG2.Homologs of WAG1 were initially discovered in Cucumissativus and Pisum sativum as auxin-induced and light-repressed genes [31–34]. Also the Arabidopsis WAG1 andWAG2 transcript levels were found to be negativelyregulated by light [27,34], and it is therefore probable thatone or both of theWAG genes are auxin-responsive, similarto the Cucumis sativus homolog CsPK3 or the PID gene inArabidopsis [12,31]. Loss-of-function mutations in WAG1or WAG2 result in weak root waving phenotypes, doublemutants show a constitutive root waving phenotype,and root curling is more resistant to the PAT inhibitor1-naphthylphthalamic acid (NPA). Because root waving islinked to PAT [23], and the PAT-inhibitor resistant root-curling phenotype is characteristic for mutants in PAT[35], it is probable that the WAG kinases, similar toPID, are involved in the regulation of auxin transport[23,27].

To corroborate this possible functional relatedness, weanalyzed the subcellular localization of WAG1, WAG2 andPID in Arabidopsis thaliana protoplasts (Figure 3a–c), andfound that all three kinases localize predominantly to theplasma membrane; however, WAGs can also be found inthe nucleus. Our observations are partially in contrast tothose of Zegzouti and co-workers, who concluded that the

Figure 3. PID, WAG1 and WAG2 are plasma membrane-associated kinases. (a–c)

C-terminal fusions of PID, WAG1 and WAG2 with yellow fluorescent protein (YFP)

localize to the plasma membrane (arrowhead) in Arabidopsis protoplasts. (d–e)

Confocal sections of two independent transgenic lines overexpressing PID:GFP

(35S::PID:GFP). (d) Root tip showing non-polar membrane localization of PID in the

columella cells (arrow) and apico-basal localization in the epidermal cell layer

(inset, arrowhead). (e) Detail of the root epidermis, in the distal elongation zone

(between the root tip and the elongation zone), showing apico-basal membrane

localization of PID. (f) The 35S::PID:GFP seedlings show agravitropic growth and

the primary root meristem collapses, demonstrating that the fusion protein is

functional.

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WAG kinases are localized in the nucleus [19]. Becausetheir conclusion was based on the expression of fusionswith the green fluorescent protein (GFP) in yeast cells, ourown observations on functional yellow fluorescent protein(YFP) fusions expressed in Arabidopsis protoplasts aremore likely to reflect the subcellular localization of theWAG kinases in planta. The plasma membrane localiz-ation, together with the phenotypes observed on the loss-of-function mutants and the similarity in amino acidsequence between PID and the WAG kinases, suggest thatthese kinases act in the same or in a parallel pathway toregulate the PAT machinery.

The evolution of auxin-dependent plant development:AGC kinases tell the taleFrom an evolutionary perspective, the phototropins andAGC3 kinases seem to recapitulate plant evolution(Figure 2). It is unsurprising that PHOT2-like genesrepresent the most ancient AGCVIII protein kinases,because the optimization of photosynthesis in responseto light intensities in the first eukaryotic photosyntheticcells was a crucial trait in plant evolution. The essentialfunction of PHOT2-like genes has been well conserved andour analysis indicates that PHOT2-like genes are found inrepresentative species throughout the plant kingdom(Figure 2). By contrast, PHOT1-like genes are only foundin spermatophytes, indicating that PHOT1-mediated tro-pic growth in response to low intensity light evolved lateras an important determinant of proper development of soil-born germinating seedlings (Figure 2).

As for auxin-dependent processes, a tryptophan-de-pendent biosynthesis pathway has been found in greenand brown algae (Chlorophytes and Charophytes) [36]. Bycontrast, no genes encoding PID, PID-like kinases or PINauxin efflux carriers have been identified in the green algalgenomes of Chlamydomonas orOstreococcus (Table 1) and,although auxin transport seems to regulate directionalgrowth and patterning in the brown algae [36], there isno clear evidence for PIN-dependent auxin efflux in theseearly plant forms (reviewed in Ref. [36]). In fact, auxintransport in Charophytes might well be mediated by themulti-drug-resistant/P-glycoprotein (MDR/PGP) type oftransporters (Box 1), which are found throughout theentire plant kingdom, and, like PIN proteins, exhibit auxinefflux activity and sensitivity to PAT inhibitors [8,36,37].

Genes encoding candidate homologs of the AGC3kinases and PIN auxin efflux carriers have been identifiedin the moss Physcomitrella [38] (www.cosmoss.org), and inmany other land plants (Figure 2, Table 1). This, togetherwith the demonstrated functional relationship betweenPID and PINs [11], suggests that these two gene familiesco-evolved, and that AGC3 kinase-regulated PIN-depend-ent PAT might have had an important role in the adap-tation of plants during the transition from water to land(Figure 2, Table 1).

In conclusion, there is a strong correlation betweenthe known functions of the AGC3 and AGC4 kinases inplant development, and their distribution throughoutthe plant kingdom, which suggests that new AGCkinases were acquired during most crucial steps in plantevolution.

546 Opinion TRENDS in Plant Science Vol.12 No.12

Concluding remarks and future perspectivesAlthough there is much information about howdifferential auxin distribution couples environmentalstimuli to developmental responses, such as directionalgrowth, it is still unclear how the different components inthe PAT pathway work coordinately to orient this auxin-directed plant development. Two subgroups of the AGC-VIII protein kinases are directly involved in this process.On the one hand, light-activated phototropins inducerapid Ca2+ release into the cytosol and initiate differen-tial auxin transport leading to auxin accumulation in thecell layers at the dark side of the hypocotyl [39]. On theother hand, PID, and possibly other AGC3 kinases,directs PAT by determining the correct polar localizationof PIN proteins during embryo development and organformation in the shoot apical meristem.

Although none of the AGC3 kinases has been directlyconnected to phototropic growth, the observation that theactivity of PID is regulated by interacting calcium-bindingproteins [40] suggests that these kinases are downstreamcomponents of the phototropin signal transduction path-way. Whether the other AGC3 kinases similar to PIDdirect PAT through direct phosphorylation of PIN proteins,whether one or more AGC3 kinases affect the subcellularPIN localization during phototropism and whether there isa link between PHOT-induced calcium release and regu-lation on the activity of AGC3 kinases through calcium-binding proteins are key questions to be addressed byfuture research.

In conclusion, based on the data presented here, wepropose that those AGCVIII kinases that have an essentialrole in plant development, recapitulate plant evolution.Phototropins represent the most ancient AGCVIII kinaseforms that regulate highly conserved processes in plants,such as optimization of light perception, and AGC3 kinasesco-evolved with PIN auxin transporters in multicellularplants during their colonization of land, and act together,possibly downstream of the phototropins, to orient plantdevelopment by establishing the directionality of auxintransport.

AcknowledgementsWe thank Helene Robert, Christa Testerink and Lazlo Bogre for criticallyreading the manuscript, and Gerda Lamers for assistance in confocalmicroscopy. This work was funded through grants from the ResearchCouncil for Earth and Life Sciences (ALW 813.06.004) and from theNetherlands Organization for Health Research and Development (ZON050–71–023), with financial aid from the Dutch Organization of ScientificResearch (NWO).

Supplementary dataSupplementary data associated with this article can befound, in the online version, at doi:10.1016/j.tplants.2007.10.004.

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