Control of phosphate homeostasis through gene regulation ... et al-COPB.pdf · fungi and rhizobia, also play important roles the regulation of crop Pi homeostasis (Figure 1). the

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.

www.sciencedirect.com

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


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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


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.


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


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


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].



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


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,


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



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


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.



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:


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.

41.��

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































































































































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.

50.�

Park BS, Seo JS, Chua NH: NITROGEN LIMITATIONADAPTATION recruits PHOSPHATE2 to target thephosphate transporter PT2 for degradation during the


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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Control of phosphate homeostasis through gene regulation ... et al-COPB.pdf · fungi and rhizobia, also play important roles the regulation of crop Pi homeostasis (Figure 1). the