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Control of phosphate homeostasis through generegulation in cropsCuiyue Liang, Jinxiang Wang, Jing Zhao,Jiang Tian and Hong Liao
Available online at www.sciencedirect.com
ScienceDirect
Phosphorus (P) is an essential yet frequently deficient element
in plants. Maintenance of phosphate (Pi) homeostasis is crucial
for crop production. In comparison with the model plant
Arabidopsis, crops face wider ranges and larger fluctuations in
P supply from the soil environment, and thus develop more
complicated strategies to improve Pi acquisition and utilization
efficiency. Undergirding these strategies, there are numerous
genes involved in alternative metabolism pathways that are
regulated by complex Pi signaling networks. In this review, we
intend to summarize the recent advances in crops on control of
Pi homeostasis through gene regulation from Pi acquisition and
mobilization within plants, as well as activation of rhizosphere P
and P uptake through symbiotic associations.
Addresses
State Key Laboratory for Conservation and Utilization of Subtropical
Agro-bioresources, Root Biology Center, South China Agricultural
University, Guangzhou 510642, PR China
Corresponding author: Liao, Hong ([email protected])
Current Opinion in Plant Biology 2014, 21:59–66
This review comes from a themed issue on Cell signalling and gene
regulation 2014
Edited by Xiangdong Fu and Junko Kyozuka
http://dx.doi.org/10.1016/j.pbi.2014.06.009
1369-5266X/# 2014 Published by Elsevier Ltd.
IntroductionAs an essential nutrient for plant growth and develop-
ment, phosphorus (P) is also the second most frequently
required fertilizer component after nitrogen (FAOSTAT,
http://faostat.fao.org, 2014). In order to feed the expand-
ing population, crops require ever larger amounts of P to
realize required yields. Most of the P acquired by plants is
taken up as inorganic phosphate (Pi). Although, P ferti-
lizers might meet crop P demands temporally, over the
course of a growing season, P availability is still often
limiting due to the high rate fixation and the slow diffu-
sion of P in most soils. With this in mind, maintaining Pi
homeostasis under fluctuating and often limiting Pi con-
ditions becomes an essential consideration for improving
crop productivity.
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Over the last few decades, the gene regulation network
underlying maintenance of Pi homeostasis has been well
documented in the model plant, Arabidopsis [1,2]. The Pi
signaling network, including candidate signaling mol-
ecules such as Pi, sugars, hormones, and microRNAs
(miRNAs) has also been summarized in the informative
reviews above. However, due to agricultural practices
(e.g. fertilization and cultivation), crops face more fluctu-
ations of the P supply than Arabidopsis does. These
fluctuations might trigger even more complicated phys-
iological, biochemical and molecular responses. The
responses that have been outlined for improved P acqui-
sition include alteration of root morphology and archi-
tecture, increase of root exudation and induction of high-
affinity Pi transporters. Once acquired, P utilization can
be enhanced through modification of metabolic pathways
and reallocation of Pi among different organs and tissues,
as well as sub-cellular compartments. Moreover, symbio-
tic associations with rhizosphere microorganisms, such as
mycorrhizal fungi and rhizobia, also play important roles
in the regulation of crop Pi homeostasis (Figure 1).
Considering the large knowledge gap existing between
crops and Arabidopsis, in this review, we mainly highlight
the recent advances in understanding gene regulation
networks controlling Pi homeostasis in crops. In the
meantime, progress in understanding these processes in
Arabidopsis will be noted.
Gene regulation networks involved in PacquisitionPlants have developed several strategies to enhance P
acquisition from P-limited soils (Figure 1). The most
obvious change is the remodeling of root morphology
and architecture, which provides an ideal structure for
scavenging P. Complementing an optimized root archi-
tecture, increased root exudation can facilitate Pi release
from unavailable soil P forms around roots. Then, the
subsequent induction of high-affinity Pi transporters
works to direct efficient uptake of rhizosphere Pi.
Remodeling of root architecture for better P acquisition
Remodeling of root system architecture (RSA) to cope
with P deficiency is separately or coordinately controlled
by complex regulation networks, which have been well
summarized [1,2]. Functional characterization of crop
species homologues of key Arabidopsis transcription fac-
tors/regulators has revealed molecular mechanisms of
Current Opinion in Plant Biology 2014, 21:59–66
60 Cell signalling and gene regulation 2014
Figure 1
Shoot Pi remobilizationAlternative metabolic pathways
Pi translocation
Pi uptake
Pi uptake
exudatesPi translocation
Lipid remodelingPi recycling
Pi translocation
Rhizobial symbiosis
Mycorrhizal symbiosis
Pi uptake
Root Pi remobilization
Rhizosphere P activation
Root system architecture remodelingLateral/adventitious root branchingRoot hair elongation
Alternative metabolic pathwaysLipid remodelingPi recycling
APaseRNaseOrganic acidH+
Current Opinion in Plant Biology
Mechanisms for maintaining Pi homeostasis under Pi starvation in crop plants. Enhanced P acquisition is achieved by remodeling of root system
architecture, forming symbiotic associations with rhizosphere microorganisms, increasing root exudates and inducing high-affinity Pi transporters.
Increased Pi utilization efficiency can be facilitated by increasing the efficiency of Pi recycling and remobilization.
RSA Pi starvation-responses in crops. These transcription
factors/regulators include OsPHR2, OsPTF1, OsARF12/16,
OsMYB2P-1 and OsMYB4P in rice (Oryza sativa),
GbWRKY1 in cotton (Gossypium barbadense), TaPHR1 in
wheat (Triticum aestivum) and ZmPTF in maize (Zea mays)[1,3–8] (Figure 2). Overexpression of most the above
genes has resulted in augmented root growth under Pi
starvation. Moreover, downstream genes are also reported
to control RSA Pi starvation-responses in several crop
species. Among them, OsLTN1 (OsPHO2) in rice acts as
negative regulator of RSA under Pi starvation, while
GmEXPB2 in soybean (Glycine max), LaGPX-PDE1/2 in
white lupin (Lupinus albus) and the recently identified
PSTOL1 in rice all act as positive regulators [9–11,12��](Figure 2). Remodeling of RSA mediated by the above
transcription factors/regulators in turn improves plant Pi
status as supported by increased shoot Pi concentrations
[3,6,11], which suggests vital roles for these genes in
controlling root development for the purpose of exploring
more to soils, thus increasing Pi acquisition efficiency and
maintaining Pi homeostasis in crops.
Control of rhizosphere P activation
A large fraction of soil P is fixed into organic (e.g. phytate)
or inorganic (e.g. Ca-P, Fe-P, Al-P) forms, which cannot
be directly utilized by plants. It is generally believed that
root exudates, such as acid phosphatases (APases),
RNases, protons (H+) and organic acids, are intricately
Current Opinion in Plant Biology 2014, 21:59–66
involved in P activation from insoluble P pools in the
rhizosphere [13] (Figure 1).
Secreted purple acid phosphatases (PAPs) have been
documented to function in Pi release from other organic
P forms. For example, AtPAP10, AtPAP12 or AtPAP26
release Pi from ADP, glycerol-3-P or DNA in Arabidopsis
[14], while PvPAP1 and PvPAP3 release Pi from dNTPs
in common bean (Phaseolus vulgaris) [15]. Recently,
PvPAP1 and PvPAP3 have been suggested to be down-
stream genes of PvSPX1 in common bean [16]. However,
in Pi starved rice, OsPAP10a expression has been reported
as enhanced by OsMYB2P-1, OsPHR2 and OsSPX-MSF1,
and suppressed by OsSPX1, OsSPX3/5 and OsARF12[4,17,18,19��,20]. This suggests the existence of a com-
plicated gene network that coordinately regulates the
activation of organic rhizosphere P with multiple other
processes in response to low P stress in crops.
Increased exudation of H+ and organic acids has been
found to activate the fixed inorganic P from soils [21]. A
recent study showed that a tomato (Lycopersicon esculen-tum) 14-3-3 member, TFT, functioned as a root plasma
membrane H+-ATPase that increases the release of H+
under low P conditions [22]. However, further work is still
required to fully uncover information at molecular level
on the regulation of Pi starvation responsive H+ and
organic acid exudation.
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Phosphate homeostasis in crops Liang et al. 61
Figure 2
Pi starvation
Primary root growth
Lat
eral
/ad
ven
titi
ou
s ro
ot
form
atio
n/g
row
th
GBWRKY1TaPHR1
ZmPTF1
OsPSTOL1
GmEXPB2OsPTF1
OsmiR399OsLTN1
OsARF12OsPHR2
OsMYB2P-1OsMYB4P
AtMYB2
AtERF070AtHPS4
AtAPSR1
Current Opinion in Plant Biology
Regulation of root system architecture modification in Arabidopsis and crops. Black lines represent the regulation network in Arabidopsis, while blue
lines represent the regulation network in crops. Arrows indicate positive effects, whereas lines ending with a short bar indicate negative effects. Solid
lines indicate no effects observed. Dashed lines indicate undefined relations. At, Arabidopsis thaliana; Os, Oryza sativa; Gm, Glycine max; Zm, Zea
mays; Ta, Triticum aestivum; Gb, Gossypium barbadense; La, Lupinus albus.
Transcriptional and posttranscriptional regulation of Pi
transporters
Direct Pi uptake from rhizosphere occurs mainly through
Pi:H+ cotransporters (PHT). After the first PHT genes
(AtPT1 and AtPT2) were cloned from Arabidopsis, numer-
ous PHT homologues have been characterized as regu-
lators of Pi uptake in various crop species. Notable
examples include OsPT1/6/8/9/10 in rice [20,23] and
TaPht1;4 in wheat [24] (Figure 3).
The transcriptional network regulating Pi uptake through
PHTs in Arabidopsis has been recently summarized with
AtPHR1 playing a central role [1]. Similarly, OsPHR2 in
rice, TaPHR1 in wheat and PvPHR1 in common bean
have also been found to upregulate the expression of
PHTs [7,20,25]. Moreover, in other crop species (e.g.
barley and wheat), the PHR binding sequence (P1BS/
P1BS-like) exists in the promoter regions of some PHTs[26], which suggests roles for PHR in direct regulation of
PHTs in these species as well.
The full extent of PHT regulation and connections with
other pathways in crops has yet to be elucidated. In rice,
OsPHR2 enhances the accumulation of OsmiR399 and
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subsequently suppresses the mRNA of OsPHO2.
Mutation of OsPHO2 caused upregulation of several
PHT genes (e.g. OsPT1/8), and thus resulted in an
increase of Pi uptake under low P conditions [11]. Several
PHO2 genes have also been identified as targets of
miR399 in other crops, such as soybean [27]. Whether
PHO2 affects PHTs in these crops, either directly or
indirectly, remains unclear. Furthermore, in Arabidopsis,
other transcription factors, including ZAT6, MYB62,
WRKY75 and WRKY45, have also been reported as
modulators of PHT expression [1,28�] (Figure 3). In crops,
however, their homologues have not been identified or
functionally characterized.
In addition to transcriptional regulation, complex post-
transcriptional regulation networks of PHT proteins have
been gradually uncovered. In Arabidopsis, PHT proteins
are regulated by the PT Traffic Facilitator (AtPHF1)
during intracellular trafficking to the plasma membrane
under low P conditions [1]. Similar activity is found in
rice, where mutation of OsPHF1 results in the retention of
OsPT2 and OsPT8 in the endoplasmic reticulum [29].
Thus, when overexpressing OsPHF1, Pi-uptake capacity
of rice is enhanced [29].
Current Opinion in Plant Biology 2014, 21:59–66
62 Cell signalling and gene regulation 2014
Figure 3
Pi starvation
Pi uptake Pi translocation
Pi starvation
OsSPX3/5OsPHF1
OsmiR827OsPHO1:2
OsSPX-MFS1
OsMYB2P-1OsMYB4P
OsPTs
OsSPX1
OsIPS1/2
OsPHR2OsmiR399
OsPHO2PvPHT1
PvPHO2
PvmiR399
PvPHR1TaPHR1
TaPHT1
AtPHT1:4 AtPHTs
At4/IPS1
AtPHO2
AtPHF1
AtPHO1
AtWRKY6/42
AtmiR399AtNLA
AtmiR827 AtZAT6 AtMYB62 AtWRKY45 AtWRKY75 AtPHR1/PHL1 AtMYB2
AtSIZ1
Pv4
Current Opinion in Plant Biology
Regulation of Pi uptake and translocation in Arabidopsis and crops. Black lines represent the regulation network in Arabidopsis, while red lines
represent the regulation network in crops. Arrows indicate positive effects, whereas lines ending with a short bar indicate negative effects. Solid lines
indicate no effects observed. Dashed lines indicate undefined relations. At, Arabidopsis thaliana; Os, Oryza sativa; Pv, Phaseolus vulgaris; Ta, Triticum
aestivum.
Pi signaling and gene regulation involved in PmobilizationTo maintain Pi homeostasis in plants, P mobilization
must operate efficiently. This includes recycling of P
from old/inactive tissues/cell compartments to young/
active tissues/cell compartments, as well as, translocation
of Pi within the whole plant (Figure 1).
Systemic control of root-shoot Pi translocation
Unlike Pi uptake from the rhizosphere, Pi translocation in
different plant compartments is conducted through both
PHT and SPX domain proteins. The sophisticated regu-
lation network driving this Pi translocation in response to
Pi starvation in Arabidopsis has been discussed by Chiou
and Lin [1]. Here, Pi translocation in crop species is
addressed.
Besides functioning in Pi uptake from soils, three rice
PHTs (OsPT2/6/8) have also been found to play a role in
Pi translocation. Knockdown OsPT2 and OsPT6 results in
decreased long-distance Pi transport from roots to shoots,
Current Opinion in Plant Biology 2014, 21:59–66
while overexpression of OsPT8 increases Pi accumulation
in both roots and shoots [20]. Interestingly, OsPT8 also
mediates Pi translocation from vegetative tissues to repro-
ductive organs. These data shed light on the multiple
functions of PHTs in crops. Additionally, SPX domain
proteins might be also involved in Pi translocation,
especially in the xylem loading of Pi. Evidence for this
comes from the observation that mutation of OsPHO1;2results in the strong reduction of Pi transport from roots to
shoots. In addition, another SPX domain protein OsSPX-
MFS1 has been identified as a Pi transporter functioning
in leaf Pi reallocation [20]. In Arabidopsis, the chloroplast
Pi transporter AtPHT2;1, and Golgi Pi transporter
AtPHT4;6 have been suggested to affect the Pi sub-
cellular compartments [30,31]. However, molecular
mechanisms underlying Pi redistribution among sub-cel-
lular compartments remain largely unknown in crops.
Regulation of Pi translocation has been widely reported
in rice and Arabidopsis (Figure 3). In rice, OsSPX3/5
might be the functional repressors of OsPHR2 and
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Phosphate homeostasis in crops Liang et al. 63
consequently regulate Pi translocation through modu-
lation of the expression of some PHTs (e.g. OsPT2)
[18]. On the other hand, the expression of OsSPX-MFS1 is suppressed by the Pi-starvation induced
OsmiR827, indicating a role in regulation of Pi homeo-
stasis by miRNAs other than miR399 [20]. In Arabidopsis,
the degradation of AtPHO1 is modulated by AtPHO2
[1,2]. In rice, the relation between OsPHO2 and OsPHO1
has not yet been clarified.
Genes involved in P recycling and conservation
Plants also increase P use efficiency during Pi starvation
via promotion of intracellular P recycling by upregulation
of a variety of genes. The resulting responses include
alternation of metabolic pathways, replacement of mem-
brane phospholipids and recycling of P from a broad range
of organic P forms [13].
Phosphoenolpyruvate carboxylase (PEPC)-malate
dehydrogenase-malic enzyme glycolytic bypass, which
reduced the requirement of Pi, is a well documented
alteration of glycolysis under Pi starvation. Upregula-
tion of PEPC and PEPC kinase (PPCK) by P deficiency
has been documented in Arabidopsis, rice, white lupin,
orange (Citrus sinensis L.) and melon (Cucumis melo L.)
[13,32,33]. The expression of PPCKs is repressed by the
basic helix loop helix transcription factor BHLH32 in
Arabidopsis, but upregulated by another BHLH
protein, PTF1, in both rice and maize [3,13]. Thus,
it can be concluded that either multiple BHLH
proteins regulate PPCKs in opposite directions or Ara-
bidopsis and rice have evolved different regulation
pathways in Pi conservation.
Another strategy for P recycling under low P stress is the
conversion of membrane phospholipids to sulfolipids and
galactolipids, which could save Pi for vital metabolisms.
This conversion process consists of two steps: first, the
phospholipids are hydrolyzed to yield diacylglycerol
(DAG) and release free Pi; second, galactolipids and
sulfolipids are synthesized using DAG as a substrate
[34]. Two sets of rice genes involved in the synthesis
of either sulfolipids (SQD1 and SQD2) or galactolipids
(DGD1 and DGD2) are found to be upregulated by Pi
starvation [35]. In white lupin, phospholipids are totally
decomposed under Pi starvation via highly induced
expression of two glycerophosphodiesterase (GPDE)
genes, GPX-PDE1 and GPX-PDE2, thus recycling Pi
for plant growth [9].
Enhanced P recycling from a broad range of organic-P in
inactive/senescent tissues/cell compartments is proposed
to be a universal strategy of plant adaptation to Pi
starvation. In this response, intercellular acid phosphatase
(IAPase) and ribonuclease are thought to play crucial
roles. Increased IAPase activity is observed in some P
deficient plants, along with induced expression of various
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IAPase coding genes, such as Cm-PAP10.2 [32]. However,
among the functionally identified IAPase genes, only
AtPAP26 is proven to be involved in P recycling from
senescing leaves [36]. The ribonuclease genes RNS2 from
Arabidopsis have also been found associated with Pi
starvation and senescence [37]. These results indicate
that both acid phosphatases and ribonucleases are import-
ant for P remobilization from senescing leaves, particu-
larly under low P stress.
Regulation of Pi homeostasis in symbiosisTwo important symbiotic associations affecting plant Pi
homeostasis are known as mycorrhizae, and nodules on
legumes. Forming symbiotic relationships with arbus-
cular mycorrhizal fungi (AMF) is an important strategy
by crops in adaptation to P deficiency [38]. Elongation
of AMF extraradical hyphae can extend the P depletion
zone beyond the rhizosphere, and subsequently
improve the Pi-status and growth of host plants
(Figure 1). Maintenance of plant Pi homeostasis in
mycorrizal symbiosis is a complex process involving
the multidirectional regulation of various genes. For
example, the expression of pre-miR399 in Medicago
leaves is upregulated by AM symbiosis [39]. Enhanced
accumulation of miR399 in shoots might increase its
transport to roots, and thus increase mature miR399
abundance in roots. Elevated miR399 in roots is pos-
tulated to keep a low level of MtPho2, and thereby
prevents suppression of symbiotic Pi uptake [39].
The symbiotic Pi uptake mediated by AM-associated Pi
transporters is essential for maintaining Pi homeostasis in
the AM symbiosis system [40], such as OsPT11 and
OsPT13 in rice [41��], LePT3 and LePT4 in tomato
[42], AsPT4 in Astragalus sinicus [43] and ZmPHT1;6
in maize [44]. Interestingly, the P1BS cis-element is
present in the promoter of many AM-related Pi transpor-
ters (e.g. StPT3, StPT4, LePT4, MtPT4, OsPT11 and
OsPT13) [45]. This indicates that these AM-related genes
might be regulated by PHR transcript factors. However,
details of this signaling network remain to be revealed.
Legumes can interact with rhizobia to form nodules for
fixing atmospheric nitrogen. Functional characteriz-
ation of a Pi transporter, GmPT5, indicates that Pi
homeostasis in nodules is largely dependent on Pi
transport from roots rather than direct Pi uptake by
nodules during Pi starvation [46��]. Although a group of
Pi starvation responsive genes and proteins have been
identified through modern transcriptomic and proteo-
mic analysis in nodules [47,48], molecular information
on rhizobial effects on Pi homeostasis remains fragmen-
tary. Further functional characterization of the genes/
proteins identified in these experiments might be help-
ful for constructing a more complete model of the gene
regulation network controlling Pi homeostasis in
nodules.
Current Opinion in Plant Biology 2014, 21:59–66
64 Cell signalling and gene regulation 2014
ProspectsIn order to maintain Pi homeostasis under low P stress,
plants have adapted various strategies involving multi-
dimensional gene regulation networks. However, Pi
homeostasis in plants cannot be taken in isolation from
other nutrient elements. Rather, evidence for coordina-
tion of homeostasis among different nutrients is emer-
ging. In Arabidopsis, Pi starvation downregulates the
expression of RING-type ubiquitin E3 ligase NITROGENLIMITATION ADAPTION (NLA), which is involved in N
recycling during N limitation stress. When Pi is sufficient,
NLA and UBC24 (PHO2) might work in tandem to
mediate polyubiquitination of AtPHT1;4 for degradation
[49,50�]. In addition, P application facilitates N fixation in
soybean nodules [46��]. These results together suggest
that even more complex gene regulation networks work
to maintain Pi homeostasis in plants.
On the other hand, in agricultural production, heavy
application of P fertilizers has been carried out to avoid
losses of crop yield due to P deficiency, but it might
lead to P toxicity in crops. Very little attention has been
paid on how crops cope with overwhelming Pi appli-
cation. Recently, it has documented that OsSPX4 could
maintain Pi homeostasis under P sufficient conditions
mainly through inhibition of the targeting of OsPHR2
to the nucleus [51]. However, more studies are still
needed to understand the regulatory network about
maintenance of Pi homeostasis under excess P con-
ditions. Therefore, in order to achieve sustainable
agriculture, further studies need to address not only
how crops adapt to Pi starvation, but also how this fits in
with complex interacting networks regulating homeo-
stasis of multiple nutrients, as well as, how crops can
maintain Pi homeostasis under Pi excessive conditions.
AcknowledgementsThe authors acknowledge Dr Thomas C Walk for critical reading, andfinancial supports from National Key Basic Research Special Funds ofChina (2011CB100301) and the National Natural Science Foundation ofChina (Grant Nos. 31025022 and 31301835).
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� of special interest
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28.�
Wang H, Xu Q, Kong YH, Chen Y, Duan JY, Wu WH, Chen YF:Arabidopsis WRKY45 transcription factor activates PHT1;1expression in response to phosphate starvation. Plant Physiol2014, 164:2020-2029.
This study showed that AtWRKY45 positively regulates Arabidopsis Piuptake by directly enhancing the expression of AtPHT1;1. Results pro-vided new insight to the regulation network of Pi acquisition.
29. Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J, Gan J, Wu Z, Wu P:OsPHF1 regulates the plasma membrane localization of low-and high-affinity inorganic phosphate transporters anddetermines inorganic phosphate uptake and translocation inrice. Plant Physiol 2011, 157:269-278.
30. Versaw WK, Harrison MJ: A chloroplast phosphatetransporter PHT2;1, influences allocation of phosphatewithin the plant and phosphate-starvation responses. PlantCell 2002, 14:1751-1766.
31. Hassler S, Lemke L, Jung B, Mohlmann T, Kruger F,Schumacher K, Espen L, Martinoia E, Neuhaus HE: Lack of theGolgi phosphate transporter PHT4;6 causes strongdevelopmental defects, constitutively activated diseaseresistance mechanisms and altered intracellular phosphatecompartmentation in Arabidopsis. Plant J 2012, 72:732-744.
32. Fita A, Bowen HC, Hayden RM, Nuez F, Pico B, Hammond JP:Diversity in expression of phosphorus (P) responsive genes inCucumis melo L.. PLOS ONE 2012, 7:e35387.
33. Yang LT, Jiang HX, Qi YP, Chen LS: Differential expression ofgenes involved in alternative glycolytic pathways, phosphorusscavenging and recycling in response to aluminum andphosphorus interactions in citrus roots. Mol Biol Rep 2012,39:6353-6366.
34. Nakamura Y: Phosphate starvation and membrane lipidremodeling in seed plants. Prog Lipid Res 2013, 52:43-50.
35. Oono Y, Kawahara Y, Kanamori H, Mizuno H, Yamagata H,Yamamoto M, Hosokawa S, Ikawa H, Akahane I, Zhu Z:
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mRNA-Seq reveals a comprehensive transcriptome profileof rice under phosphate stress. Rice 2011, 4:50-65.
36. Robinson WD, Carson I, Ying S, Ellis K, Plaxton WC: Eliminatingthe purple acid phosphatase AtPAP26 in Arabidopsis thalianadelays leaf senescence and impairs phosphorusremobilization. New Phytol 2012, 196:1024-1029.
37. Hillwig MS, Contento AL, Meyer A, Ebany D, Bassham DC,MacIntosh GC: RNS2, a conserved member of the RNase T2family, is necessary for ribosomal RNA decay in plants. ProcNatl Acad Sci U S A 2011, 108:1093-1098.
38. Smith SE, Jakobsen I, Grønlund M, Smith FA: Roles of arbuscularmycorrhizas in plant phosphorus nutrition: interactionsbetween pathways of phosphorus uptake in arbuscularmycorrhizal roots have important implications forunderstanding and manipulating plant phosphorusacquisition. Plant Physiol 2011, 156:1050-1057.
39. Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A,Schauser L, Scheible W, Krajinski F: Expression patternsuggests a role of MiR399 in the regulation of the cellularresponse to local Pi increase during arbuscular mycorrhizalsymbiosis. Mol Plant Microbe Interact 2010, 23:915-926.
40. Gu M, Chen A, Dai X, Liu W, Xu G: How does phosphate statusinfluence the development of the arbuscular mycorrhizalsymbiosis? Plant Signal Behav 2011, 6:1300-1304.
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Yang SY, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D,Miyao A, Hirochik H, Kumar CS, Sundaresan V, Salamin N et al.:Nonredundant regulation of rice arbuscular mycorrhizalsymbiosis by two members of the PHOSPHATETRANSPORTER1 gene family. Plant Cell 2012, 24:4236-4251.
This study found that 70% of the Pi uptake is achieved by symbioticpathway in mycorrhizal rice. Two symbiosis-specific phosphate trans-porter genes PT11 and PT13 played a central role during the developmentof AM symbioses. However, only PT11 is necessary and sufficient forsymbiotic Pi uptake.
42. Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M:Mycorrhizal phosphate uptake pathway in tomato isphosphorus-repressible and transcriptionally regulated. NewPhytol 2009, 181:950-959.
43. Xie X, Huang W, Liu F, Tang N, Liu Y, Lin H, Zhao B: Functionalanalysis of the novel mycorrhiza-specific phosphatetransporter AsPT1 and PHT1 family from Astragalus sinicusduring the arbuscular mycorrhizal symbiosis. New Phytol 2013,198:836-852.
44. Willmann M, Gerlach N, Buer B, Polatajko A, Nagy R, Koebke E,Jansa J, Flisch R, Bucher M: Mycorrhizal phosphate uptakepathway in maize: vital for growth and cob development onnutrient poor agricultural and greenhouse soils. Front Plant Sci2013, 4:533.
45. Chen AQ, Gu M, Sun SB, Zhu LL, Hong S, Xu GH: Identificationof two conserved cis-acting elements MYCS and P1BS,involved in the regulation of mycorrhiza-activatedphosphate transporters in eudicot species. New Phytol 2011,189:1157-1169.
46.��
Qin L, Zhao J, Tian J, Chen L, Sun Z, Guo Y, Lu X, Gu M, Xu G,Liao H: The high-affinity phosphate transporter GmPT5regulates phosphate transport to nodules and nodulation insoybean. Plant Physiol 2012, 159:1634-1643.
The authors identify a nodule high-affinity phosphate (Pi) transportergene, GmPT5, whose expression is upregulated by P deficiency. Further-more, they demonstrate that GmPT5 mainly functions in transferring Pifrom roots to plant cells in nodules. This study for first time provides directevidence that legume Pi transporter involves in maintaining Pi home-ostasis in nodules by controlling Pi entry from roots to nodules.
47. Hernandez G, Valdes-Lopez O, Ramlrez M, Goffard N,Weiller G, Aparicio-Fabre R, Fuentes SI, Erban A, Kopka J,Udvardi MK, Vance CP: Global changes in the transcript andmetabolic profiles during symbiotic nitrogen fixation inphosphorus stressed common bean plants. Plant Physiol2009, 151:1221-1238.
48. Chen Z, Cui Q, Liang C, Sun L, Tian J, Liao H: Identification ofdifferentially expressed proteins in soybean nodules under
Current Opinion in Plant Biology 2014, 21:59–66
66 Cell signalling and gene regulation 2014
phosphorus deficiency through proteomic analysis.Proteomics 2011, 11:4648-4659.
49. Lin WY, Huang TK, Chiou TJ: NITROGEN LIMITATIONADAPTATION, a target of MicroRNA827, mediatesdegradation of plasma membrane-localized phosphatetransporters to maintain phosphate homeostasis inArabidopsis. Plant Cell 2013, 25:4061-4074.
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Park BS, Seo JS, Chua NH: NITROGEN LIMITATIONADAPTATION recruits PHOSPHATE2 to target thephosphate transporter PT2 for degradation during the
Current Opinion in Plant Biology 2014, 21:59–66
regulation of Arabidopsis phosphate homeostasis. Plant Cell2014, 26:454-464.
This study showed that NLA and UBC24 (PHO2) might work in tandem tomediate polyubiquitination of AtPHT1;4 for degradation. The resultsprovide additional molecular insight for the Pi signaling/homeostasisregulation.
51. Lv Q, Zhong Y, Wang Y, Wang Z, Zhang L, Shi J, Wu Z, Liu Y,Mao C, Yi K, Wu P: SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2in rice. Plant Cell 2014, 26:1586-1597.
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