Phosphate sensing in root development

Available online at www.sciencedirect.com

Phosphate sensing in root developmentSteffen Abel

Phosphate (Pi) and its anhydrides constitute major nodes in

metabolism. Thus, plant performance depends directly on Pi

nutrition. Inadequate Pi availability in the rhizosphere is a

common challenge to plants, which activate metabolic and

developmental responses to maximize Pi usage and

acquisition. The sensory mechanisms that monitor

environmental Pi and transmit the nutritional signal to adjust

root development have increasingly come into focus. Recent

transcriptomic analyses and genetic approaches have

highlighted complex antagonistic interactions between

external Pi and Fe bioavailability and have implicated the stem

cell niche as a target of Pi sensing to regulate root meristem

activity.

Address

Leibniz-Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany

Corresponding author: Abel, Steffen ([email protected])

Current Opinion in Plant Biology 2011, 14:303–309

This review comes from a themed issue on

Physiology and metabolism

Edited by Ute Kramer and Anna Amtmann

Available online 14th May 2011

1369-5266/$ – see front matter

# 2011 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.pbi.2011.04.007

IntroductionSustaining crop yields in shifting climate and edaphic

conditions will critically depend on optimal development

of the root system, which provides soil anchorage, a

conduit for water and nutrient uptake, and a surface for

biotic interactions with the rhizosphere [1]. Dynamic

remodeling of root system architecture, as guided by

fluctuating soil properties, is accomplished by adjusting

primary root extension rate, degree of lateral branching,

and frequency of root hair formation to intensify soil

engagement. Whereas intrinsic pathways controlling root

patterning and meristem activity are increasingly under-

stood, the sensory mechanisms that monitor and transmit

environmental cues to inform root development remain to

be elucidated [2–5].

About 30 elements are required for vigorous plant growth

[6]. In many ecosystems, inadequate bioavailability of P

is often the second most limiting factor for biomass

production, a nutritional constraint explained by P

chemistries in cells and soils. In contrast to C, S or N

www.sciencedirect.com

assimilation, the low electronegativity of P essentially

prohibits biological reduction of its fully oxidized and

most readily utilized form, which is inorganic phosphate

(H2PO4� or Pi). Its abundance and accessibility in the

rhizosphere directly impact plant performance because Pi

and its conjugate esters and anhydrides are ideally suited

to take key structural and regulatory roles at the nexus of

bioenergetics and metabolism [7]. However, free Pi in soil

solutions is exceedingly low (<10 mM), as a consequence

of insoluble Pi salts and complexes, slow Pi diffusion, and

substantial fractions of organically bound P (up to 80%),

which necessitates application of concentrated mineral

P fertilizers in agriculture [8].

As global deposits of high-grade phosphate rock are finite

and mined at an accelerating pace with forecasts of

production to peak in a few decades [9], the need arises

to fundamentally understand metabolic and developmen-

tal responses of plants to external Pi supply and to design

crops that more efficiently acquire and utilize the macro-

nutrient. Comprehensive plant responses to Pi limitation

and their regulation at the cellular and organismal level

have recently been reviewed [10–12]. This short article

focuses on progress, made largely in the Arabidopsis

model system, which begins to uncover mechanisms of

Pi sensing by the root apical meristem (RAM).

Local sensing at root tipsWhen challenged by Pi shortage, plants adjust root sys-

tem architecture to maximize interception of the nutrient,

which tends to build up in topsoil layers [13]. Thus, Pi

deficiency stimulates formation of a shallow root system

and expansion of root surface area by attenuating primary

root extension, promoting development of secondary and

higher-order roots, and intensifying root hair formation

[14–16]. Physiological and molecular studies using Ara-

bidopsis mutants and transgenic reporter lines monitoring

cell division indicate that external Pi availability is locally

sensed by root tips to adjust RAM activity accordingly. As

demonstrated in horizontal ‘split-root’ growth assays,

primary root extension slows considerably as soon as

the downward growing tip leaves behind a Pi-rich sub-

strate and comes into contact with a Pi-depleted patch

[17]. Likewise, lateral root primordia on segments of pdr2roots (see Table 1 for genetic loci) exposed to Pi-deficient

agar medium arrest growth shortly after emergence and

meristem activation, providing genetic evidence for a

Pi-sensitive checkpoint in root development at the stage

of meristem maintenance [18]. Using a vertical ‘split-root’

design (each half of the intact root system is in contact

with a different growth medium), comparison of tran-

scriptional responses to Pi deprivation revealed that about


mailto:[email protected]

http://dx.doi.org/10.1016/j.pbi.2011.04.007

304 Physiology and metabolism

Table 1

Abbreviations of genes with roles in Pi sensing described in text

Gene locus Full gene name Protein function Reference

PDR2 (At5g23630) PHOSPHATE DEFICIENCY RESPONSE 2 P5-type ATPase [18,29��,49]

PHR1 (At4g28610) PHOSPHATE STARVATION RESPONSE 1 MYB transcription factor [20,21��]

PHL1 (At5g29000) PHR1-LIKE MYP transcription factor [21��]

PHO2 (At2g33770) PHOSPHATE 2 Ubiquitin E2 conjugase (UBC24) [11]

LPR1 (At1g23010) LOW PHOSPHATE ROOT 1 Multicopper oxidase [23,29��,48]

LPR2 (At1g71040) LOW PHOSPHATE ROOT 2 Multicopper oxidase [23,29��,48]

PHT1;8 (At1g20860) PHOSPHATE TRANSPORTER 1;8 Pi uptake [11]

PHT1;9 (At1g76430) PHOSPHATE TRANSPORTER 1;9 Pi uptake [11]

SCR (At3g46600) SCARECROW GRAS transcription factor [2,29��,50]

SHR (At4g37650) SHORT-ROOT GRAS transcription factor [2,29��,50]

RBR (At3g12280) RETINOBLASTOMA-RELATED Transcription factor [2,29��,50]

FRO2 (At1g01580) FERRIC CHELATE REDUCTASE 2 Iron mobilization and reduction to Fe2+ [34,42�]

IRT1 (At4g19690) IRON-REGULATED TRANSPORTER 1 Uptake of iron (Fe2+) [34,40,42�]

FIT1 (At2g28610) FER-LIKE IRON DEFICIENCY-INDUCED

TRANSCRIPTION FACTOR (bHLH029)

bHLH transcription factor [34,42�]

NAS3 (At1g09240) NICOTIANAMINE SYNTHASE 3 Metal chelator synthesis [34,36]

FER1 (At5g01600) FERRITIN 1 Iron storage [34,36,44�]

70% of Pi-responsive genes are locally controlled by

external Pi availability, whereas internal Pi status of

the whole Arabidopsis plant imparts systemic regulation

on the remaining fraction of genes [19��]. Most of the

latter genes are directly regulated by MYB transcription

factor PHR1 via P1BS (PHR1-binding sequence) promo-

ter elements [20]. The encoded proteins function in

metabolic networks that adjust and maintain cellular

and organismal Pi homeostasis by means of reprioritized

Pi allocation, enforced recycling, and enhanced acqui-

sition [19��,20,21��]. Interestingly, locally regulated genes

are largely related to processes associated with altered

root growth (e.g. having presumed functions in hormone

or cell wall biology), which affirms that modulation of

RAM activity and root development is a primary local

effect of external Pi availability [19��].

The same study provided direct and elegant evidence

that external Pi supply rather than internal Pi status

triggers the local root growth response to Pi availability.

Restoration of root Pi content of seedlings grown on low

Pi medium to levels measured in roots of Pi-replete

plants, accomplished by feeding concentrated Pi solution

via leaves, does not alleviate primary root growth arrest

[19��]. Analyses of several Pi-related mutants support this

observation, which reveal that root Pi content and root

growth response to external Pi availability are not necess-

arily correlated [18,22–24].

External Pi is thought to act as a signal because supple-

mentation of Pi-free media with phosphite (H2PO3� or

Phi), which is not metabolized or oxidized to Pi in

tobacco BY-2 cells [25�], simulates a state of Pi suffi-

ciency. Phi application selectively attenuates molecular

and developmental responses to Pi limitation [26–28]

and preserves temporarily the root stem cell niche and

RAM functionality of Pi-starved pdr2 root tips by as yet


unknown mechanisms [18,29��]. The structural sim-

ilarity of both oxyanions and competitive inhibition of

Pi uptake by Phi suggest that high-affinity Pi transpor-

ters move Phi across the plasma membrane [25�].A recent study in yeast supports a role for Pho84 as a

Pi transceptor, which mediates high-affinity Pi uptake as

well as rapid activation of the protein kinase A pathway

during growth induction [30�]. The transport and sig-

naling functions of Pho84 can be experimentally

uncoupled using small organic P esters or methylpho-

sphonate (CH3HPO3�, a derivative of Phi). Thus, it is

tempting to speculate that some members of the PHT1

family of high-affinity Pi/H+ symporters may play dual

roles as Pi transporters and Pi sensors. In this context it

is interesting to note that expression of root-specific

PHT1;8 and PHT1;9 genes is elevated in Pi-replete

pho2 seedlings [11], which overaccumulate Pi in shoots

but not in roots and yet show accelerated primary root

growth in high Pi medium when compared to the wild

type [14,31].

The yin and yang of P and ironAlternatively, external Pi may be sensed indirectly via

complex chemical interactions between Pi and its

associated metal cations in the rhizosphere. Support

for this hypothesis is provided by the common obser-

vation that the growing root tip requires physical

contact with the agar medium to register the low-Pi

cue, whereas airborne roots of germinating Arabidopsis

seedlings extend unabatedly [23]. Unless a hydrotropic

root growth response [32] overrides at least initially

the need of airborne roots for Pi, additional constituents

of the growth substrate probably mediate the develop-

mental response of roots to low Pi. Mounting evidence

points to iron as the leading candidate and to intricate

antagonistic interactions between external Pi and

Fe availability.


Phosphate sensing in root development Abel 305

Iron is an essential trace element required for numerous

cellular functions; however, its solubility and bioavail-

ability is severely restricted, particularly under aerobic

conditions at neutral or alkaline pH. Moreover, the redox

activity of Fe under biological conditions can generate

aggressive hydroxyl radicals via the Fenton reaction [33].

Thus, iron homeostasis in plants must be tightly con-

trolled by coordinated regulation of Fe uptake, transport,

utilization, storage and detoxification [34]. Interestingly,

several studies reported elevated Fe accumulation in

roots and shoots of Pi-starved Arabidopsis and rice plants

[35,36,37�,38��]. Iron overload may be a reactive con-

sequence of increased Fe availability and subsequent

uptake when external Pi concentration drops, or a proac-

tive strategy to cope with Pi deficiency that enhances

mobilization of external Pi by absorbing Pi-complexing

metals. Indeed, Fe removal from Pi-deprived media

counteracts the inhibitory effect of Pi deficiency on

primary root growth [23,29��,37�,39]. Because root length

shows an inverse relationship with root Fe content, but

no correlation with root Pi content or the level of systemic

Pi-responsive gene expression, it has been proposed that

inhibition of RAM activity in low Pi is a consequence of

increased Fe bioavailability and its associated cellular

toxicity [37�].

Non-graminaceous plants like Arabidopsis use the

‘reduction strategy’ for Fe acquisition, which involves

proton release by P-type ATPases to increase Fe3+ solu-

bility, chelation and reduction of Fe3+ to Fe2+ by mem-

brane-bound FRO2, and transport of Fe2+ into the root by

IRT1 [34]. Because the transport specificity of Arabidopsis

IRT1 is broad, extra transition metals (e.g. Zn, Mn, Ni, Co)

are taken up and accumulate under conditions of Fe

deficiency, which must be detoxified by sequestration to

avoid imbalances in ion distribution [40]. Transcriptional

profiling studies in Arabidopsis indicate that the need for

comprehensive metal detoxification is anticipated and

embedded in Fe deficiency response networks regulated

by three basic helix-loop-helix (bHLH) transcription fac-

tors: FIT1 (bHLH029) and bHLH038/039 [41,42�].Remarkably, Pi deficiency also triggers concerted molecu-

lar responses associated with the homeostasis of Fe and

other transition metals [19��,21��,35,36]. This may be

caused by IRT1-dependent metal influx or, similarly as

proposed for Pho84 in yeast [43], by PHT1-dependent

co-transport of Pi and divalent transition metals (Me).

The possibility of stoichiometric MeHPO4 transport in

plants needs to be investigated. As observed in Pi-starved

Arabidopsis seedlings, coordinated repression of IRT1 in

roots and induction of genes in leaves with roles in Fe

transport (e.g. NAS3) or detoxification (e.g. FER1), which

probably reflect negative feedback regulation, are consist-

ent with either scenario [36,44�].

Exhaustive transcriptomic analyses on Arabidopsis

suggest integration of molecular responses to Pi starvation


and concurrently altered homeostasis of transition metals

[19��,21��,42�]. PHR1 together with related MYB factor

PHL1 controls (either directly or independently of P1BS

elements) most transcriptional activation and repression

responses to Pi deficiency, regardless if individual

responses are specific for the low Pi stress [21��]. Whereas

promoters of systemically induced genes are enriched in

P1BS motifs, promoters of repressed genes typically lack

these DNA elements, suggesting that control of transcrip-

tional repression by PHR1 is indirect and may require

activation of transcriptional repressors. About two thirds

of the genes repressed in Pi-deprived wild type seedlings

are markedly de-repressed in Pi-starved phr1phl1 double

mutants. Thus, transcriptional repression is an integral

part of the adaptive response to Pi deficiency [21��]. It is

noteworthy that genes encoding FIT1 and a number of

FIT1-regulated genes with functions related to the

mobilization and uptake of Fe and other transition metals,

including IRT1, are de-repressed in Pi-deprived phr1phl1double mutant seedlings when compared to the wild type

[21��,42�]. This observation suggests that balancing Fe

surplus as a result of increased bioavailability is an anticip-

ated safety measure coordinated with the general

response to Pi deficiency via its central regulator,

PHR1 (Figure 1). If such a scenario applies, the ability

of Phi to mimic Pi and to maintain RAM function in the

absence of Pi may be explained by restricting Fe bioa-

vailability via the formation of insoluble iron phosphite

complexes, a hypothesis that remains to be tested. How-

ever, as previously pointed out [36], Pi deficiency may

also trigger activation of alternative, IRT1-unrelated Fe

transport processes to increase root Fe uptake and thus

local Pi availability.

Signaling to the stem cell nicheGenetic approaches to dissect Pi sensing identified Ara-

bidopsis mutants and accessions with altered sensitivity

to the inhibitory effect of Pi limitation on primary root

growth [31,45–48]. Further studies indicate that the stem

cell niche, comprising the quiescent (or organizing)

center (QC) and its adjoining stem cells, is important

for adjusting RAM activity to external Pi status

[15,23,29��]. Whereas pdr2 roots display a hypersensitive

growth response to low Pi, as demonstrated by early loss

of stem cell identity followed by RAM exhaustion and

stimulation of lateral root formation, lpr1 seedlings

develop longer primary roots in Pi-deficient medium

than the wild type [18,23,29��,47,48]. Mapping of the

LPR1 quantitative trait locus uncovered a role for multi-

copper oxidases (MCOs), LPR1 and LPR2, in Pi sensing

at root tips [23]. PDR2 encodes the single P5-type

ATPase in Arabidopsis (P5-type transport specificities

remain elusive for any organism), which localizes to the

endoplasmic reticulum (ER) membrane [29��,49]. PDR2

is required for maintaining nuclear SCR protein levels

when external Pi is limiting, probably via processes

related to ER quality control [29��]. SCR is a key



Figure 1

ROS?

Root Development Biochemical Responses

Signaling?

FePi

LPR1/2

PDR2

Pi

Pi Pi

Pi

IPS1/AT4

PHR1

P1BS-Genes

Pi Acquisition & EconomyCell Division & Differentiation

miR399 miR399

PHO2

Pi

Phi

SCR

Fe Sequestration

Fe & Transition MetalAccumulation

RBR

Systemic

Local Me

Phi

Phi

Fe -specific IRT1

Trans-ceptors?

PHT1;8PHT1;9PHT1

Current Opinion in Plant Biology

Model of systemic and local inorganic phosphate (Pi) sensing. Internal Pi status regulates the activity of MYB transcription factor PHOSPHATE

STARVATION RESPONSE 1 (PHR1) by unknown mechanisms, possibly by posttranslational sumoylation [24] (not depicted). PHR1 activates

transcription of numerous genes with roles in biochemical responses to Pi limitation via P1BS promoter elements [21��]. A well understood case is the

induction of a circuit of microRNAs (miR399) and non-coding RNAs (IPS1 or AT4), which regulates (PHOSPHATE 2) PHO2 expression at the level of

PHO2 mRNA degradation. Repression of PHO2, a member of the E2 ubiquitin conjugase family (UBC24), causes upregulation of transcript levels of

genes encoding high-affinity Pi/H+ symporters of the PHOSPHATE TRANSPORTER 1 (PHT1) family in roots, PHT1;8 and PHT1;9, followed by

accumulation of Pi in shoots [11]. On the contrary, root development is governed locally by external Pi availability, which is probably antagonized by

external Fe availability (double inhibition arrow). Interestingly, mRNA levels of several genes with functions in mobilization, uptake, and sequestration of

Fe and other transition metals are repressed in Pi-starved wild-type roots but are de-regulated in Pi-deprived phr1phl1 double mutants (e.g. genes

induced by Fe-deficiency such as IRT1) [21��,42�]. This suggests that balancing iron overload as a result of increased Fe bioavailability in low Pi is an

anticipated response during the adaptation to Pi stress. Alternatively, Pi deficiency may trigger induction of IRT1-unrelated, specific Fe transporters to

increase Fe uptake and thus local Pi availability in the rhizosphere [36]. Such signaling mechanisms are currently unknown and may involve PHR1 or

hypothetical Pi transceptors (PHT1 transporters), which is a speculation based on work in yeast (Pho84) [30�]. Likewise, PHT1 members may co-

transport stoichiometric metal–Pi complexes as also reported for Pho84 [43]. Phosphite (Phi) mimics the effect of Pi, either by decreasing external Fe

bioavailability via chemical complex formation, or by cellular uptake via Pi transporters and interference with early Pi signaling events (not depicted).

The first molecular components have been identified mediating the adjustment of root meristem activity to local Pi availability, LOW PHOSPHATE

ROOT 1 (LPR1) [23] and PHOSPHATE DEFICIENCY RESPONSE 2 (PDR2) [29��]. The contrasting root phenotypes of recessive lpr1lpr2 and pdr2

mutants under conditions of Pi limitation, as well as the nearly complete epistasis of lpr mutations to pdr2, indicate that PDR2 restricts LPR output,

either by negative regulation of LPR biogenesis or activity, or by elimination of products generated by LPR multicopper oxidase activity. Expression of

LPR1 and PDR2 overlaps in the stem cell niche and distal root meristem, and both proteins are targeted to the endoplasmic reticulum. PDR2 is

necessary for proper post-translational SCARECROW (SCR) expression in low Pi. Because SCR downregulates RETINOBLASTOMA-RELATED (RBR)

in the stem cell niche [50], PDR2/LPR1-dependent growth response to Pi status probably impinges on the SCR-RBR pathway to adjust the balance of

cell division and differentiation in the root meristem. It is possible that LPR multicopper oxidases function as ferroxidases and that Fe-mediated

reactive oxygen species (ROS) production and redox signaling modulates root meristem activity and root development in response to Pi deficiency

[54]. Dotted lines indicate transport processes. Lines and boxes in gray depict tentative (no evidence in plants) transport or signaling processes. The

broken inhibition arrow indicates PHR1-dependent crosstalk between systemic and local Pi sensing. Text in blue denotes components identified in

molecular and genetic approaches to dissect Pi sensing.

transcription factor that, together with SHR and possibly

RBR, controls radial root patterning, QC specification,

and the size of the stem cell pool [50]. LPR1 and PDR2interact genetically and their expression domains overlap

in the stem cell niche and distal root meristem. LPR1 is

also targeted to the ER, suggesting that both proteins

function together in an ER-encompassing pathway that

fine-tunes RAM activity according to external Pi


availability via the stem cell niche. Considering their

epistatic relationship, PDR2 is proposed to restrict LPR1

output, either by negatively regulating LPR1 biogenesis

or function, or by eliminating products generated by its

associated MCO activity [29��].

The largest group in the MCO family across all phyla

includes laccases (polyphenol oxidases) and proteins



related to ferroxidases in yeast, plants, and humans [51]. If

RAM cessation in low Pi is caused by iron overload and

cellular Fe toxicity, the contrasting root phenotypes be-

tween Pi-starved pdr2 seedlings and lpr1lpr2 double

mutants are consistent with the hypothesis that LPR

proteins possess ferroxidase activity. This proposition is

further supported by the observation that loss of PDR2

renders primary root growth hypersensitive to external

decreasing Pi and increasing Fe availability [29��]. Redox

cycling of iron, that is re-oxidation of Fe2+ by ferroxidases

in a complex with specific Fe3+-permeases, is a common

strategy for selective, high-affinity iron uptake in yeast

and algae [51], which may also be important for cell-to-

cell Fe transport in plants [34]. Although the substrate

specificity of LPR MCOs remains to be established, it is

tempting to speculate that PDR2/LPR1-dependent Fe

transport and Fe-mediated redox signaling modulates

RAM activity and root development in response to Pi

deficiency. As recently reported for Arabidopsis, detect-

able ROS accumulation shifts from the QC and root

elongation zone in Pi-replete seedlings to the distal

meristem in Pi-starved roots [52�]. Mounting evidence

suggests that controlled ROS production and detoxifica-

tion regulates the transition from cell division to cell

differentiation [53], and that diverse environmental

inputs utilize ROS signaling modules and their inter-

action with auxin and other hormone signaling pathways

to adjust RAM organization and dynamics [54].

Conclusions and perspectivesAn apparent dichotomy of Pi sensing pathways operates

in plants (Figure 1). Metabolic adjustments to Pi

deficiency are largely controlled by internal Pi status

and are systemically integrated by microRNAs, non-cod-

ing RNAs, and PHO2 downstream of PHR1 [10]. As

revealed in recent studies, developmental responses of

the root system are governed locally by external Pi avail-

ability. It remains to be worked out if and to what extent

local and systemic responses are coordinated and what

role PHR1 assumes in such a crosstalk. PHR1/PHL1-

dependent repression of genes in low Pi that are induced

by Fe deficiency, as well as altered sensitivities of pdr2root growth to external availability of both Pi and Fe

[21��,29��,42�], suggest that dynamic Fe homeostasis in

root meristems mediates local Pi sensing. The primary

cause of tissue Fe accumulation in low Pi and its con-

sequence for Fe redox cycling and signaling in the root

stem cell niche are questions of high importance. This

begs the question how differentials in external Pi con-

centration are sensed at the root tip. Similar to work on

Pho84 in yeast [30�,43], it will be worthwhile to investi-

gate a potential function of PHT1 transporters in Pi

sensing or metal uptake. LPR1 and PDR2 are the first

identified molecular entities with roles in local Pi sensing.

Elucidation of their biochemical activities and of the

mechanisms how PDR2 restricts LPR1 output and

impinges on the SCR-RBR module to adjust root cell


division and differentiation will be important tasks for

the future.

AcknowledgementsI thank the reviewing editor (Ute Kramer) and Marcel Quint for criticalreading of the manuscript, as well as Jens Muller, Katharina Burstenbinderand Carla Ticconi for discussions. Research in my laboratory at theUniversity of California, Davis, was supported by grants awarded by theU.S. Department of Energy.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest�� of outstanding interest

1. Herder GD, Van Isterdael G, Beeckman T, De Smet I: The rootsof a new green revolution. Trends Plant Sci 2010,15:600-607.

2. Petricka JJ, Benfey PN: Root layers: complex regulation ofdevelopmental patterning. Curr Opin Genet Dev 2008,18:354-361.

3. Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L,Beeckman T, Bennett MJ: Arabidopsis lateral rootdevelopment: an emerging story. Trends Plant Sci 2009,14:399-408.

4. Ishida T, Kurata T, Okada K, Wada T: A genetic regulatorynetwork in the development of trichomes and root hairs. AnnuRev Plant Biol 2008, 59:365-386.

5. Osmont KS, Sibout R, Hardtke CS: Hidden branches:developments in root system architecture. Annu Rev Plant Biol2007, 58:93-113.

6. Agren GI: Stoichiometry and nutrition of plant growth in naturalcommunities. Annu Rev Ecol Evol Syst 2008, 39:153-170.

7. Westheimer FH: Why nature chose phosphates. Science 1987,235:1173-1178.

8. Schachtman DP, Reid RJ, Ayling SM: Phosphorus uptake byplants: from soil to cell. Plant Physiol 1998, 116:447-453.

9. Cordell D, Drangert JO, White S: The story of phosphorus: globalfood security and food for thought. Global Environ Change 2009,19:292-305.

10. Rouached H, Arpat AB, Poirier Y: Regulation of phosphatestarvation responses in plants: signaling players and cross-talks. Mol Plant 2010, 3:288-299.

11. Lin WY, Lin SI, Chiou TJ: Molecular regulators of phosphatehomeostasis in plants. J Exp Bot 2009, 60:1427-1438.

12. Yang XJ, Finnegan PM: Regulation of phosphate starvationresponses in higher plants. Ann Bot 2010, 105:513-526.

13. Lynch JP, Brown KM: Topsoil foraging – an architecturaladaptation of plants to low phosphorus availability. Plant Soil2001, 237:225-237.

14. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM: Phosphateavailability regulates root system architecture in Arabidopsis.Plant Physiol 2001, 126:875-882.

15. Sanchez-Calderon L, Lopez-Bucio J, Chacon-Lopez A, Cruz-Ramirez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L:Phosphate starvation induces a determinate developmentalprogram in the roots of Arabidopsis thaliana. Plant Cell Physiol2005, 46:174-184.

16. Muller M, Schmidt W: Environmentally induced plasticity ofroot hair development in Arabidopsis. Plant Physiol 2004,134:409-419.

17. Linkohr BI, Williamson LC, Fitter AH, Leyser HM: Nitrate andphosphate availability and distribution have different effectson root system architecture of Arabidopsis. Plant J 2002,29:751-760.



18. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S: Arabidopsispdr2 reveals a phosphate-sensitive checkpoint in rootdevelopment. Plant J 2004, 37:801-814.

19.��

Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A, Bustos R,Paz-Ares J, Poirier Y, Nussaume L: Dissection of local andsystemic transcriptional responses to phosphate starvation inArabidopsis. Plant J 2010, 64:775-789.

Comprehensive transcriptomic analysis using divided root systems iden-tified groups of genes that are locally or systemically regulated by Pideficiency and are largely associated with altered root development ormetabolic adjustments, respectively. Evidence is provided that internal Pistatus controls systemic gene regulation, but does not correlate with thelocal growth response of root tips.

20. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A,Paz-Ares J: A conserved MYB transcription factor involvedin phosphate starvation signaling both in vascular plantsand in unicellular algae. Genes Dev 2001,15:2122-2133.

21.��

Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Perez-Perez J,Solano R, Leyva A, Paz-Ares J: A central regulatory systemlargely controls transcriptional activation and repressionresponses to phosphate starvation in Arabidopsis. PLoS Genet2010, 6:e1001102.

This study thoroughly demonstrates that MYB transcription factor PHR1together with the PHR1-LIKE protein PHL1 controls most of the tran-scriptional activation and repression responses to Pi deficiency. Inducedgenes are enriched in PHR1-binding DNA sequences (P1BS) and arelargely direct targets of PHR1. Promoters of repressed genes lack theP1BS element, which is necessary and sufficient for Pi starvation-respon-sive gene expression but also acts in concert with other cis elements.Transcriptional repression is probably indirect but an integral part of theadaptive response. Interestingly, a number of genes induced by irondeficiency [42�] and repressed by Pi deficiency are de-repressed in thephr1phl1 double mutant.

22. Gonzalez E, Solano R, Rubio V, Leyva A, Paz-Ares J:PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 isa plant-specific SEC12-related protein that enables theendoplasmic reticulum exit of a high-affinity phosphatetransporter in Arabidopsis. Plant Cell 2005,17:3500-3512.

23. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L,Blanchet A, Nussaume L, Desnos T: Root tip contact with low-phosphate media reprograms plant root architecture. NatGenet 2007, 39:792-796.

24. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS,Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA et al.:The Arabidopsis SUMO E3 ligase SIZ1 controls phosphatedeficiency responses. Proc Natl Acad Sci USA 2005,102:7760-7765.

25.�

Danova-Alt R, Dijkema C, DEW P, Kock M: Transport andcompartmentation of phosphite in higher plant cells–kineticand P nuclear magnetic resonance studies. Plant Cell Environ2008, 31:1510-1521.

This work validates the use of phosphite (Phi) to mimic Pi sufficiency inplants. Phi competitively inhibits Pi transport into tobacco BY-2 cells andis not oxidized to Pi after its uptake.

26. Ticconi CA, Delatorre CA, Abel S: Attenuation of phosphatestarvation responses by phosphite in Arabidopsis. PlantPhysiol 2001, 127:963-972.

27. Varadarajan DK, Karthikeyan AS, Matilda PD, Raghothama KG:Phosphite, an analog of phosphate, suppresses thecoordinated expression of genes under phosphate starvation.Plant Physiol 2002, 129:1232-1240.

28. Stefanovic A, Ribot C, Rouached H, Wang Y, Chong J,Belbahri L, Delessert S, Poirier Y: Members of the PHO1 genefamily show limited functional redundancy in phosphatetransfer to the shoot, and are regulated by phosphatedeficiency via distinct pathways. Plant J 2007,50:982-994.

29.��

Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A,Nussaume L, Desnos T, Abel S: ER-resident proteins PDR2 andLPR1 mediate the developmental response of root meristemsto phosphate availability. Proc Natl Acad Sci USA 2009,106:14174-14179.


Identification of the PDR2 locus, encoding the single P5-type ATPasein Arabidopsis, and its genetic interaction with LPR1, encoding amulticopper oxidase [23], point to a role of processes related to ERquality control in Pi sensing by root meristems. PDR2 is required forstem cell maintenance and proper expression of SCARECROW in Pi-deprived roots. Loss of PDR2 sensitizes the root growth reponse to theinhibitory effect of both decreasing external Pi and increasing externalFe availability.

30.�

Popova Y, Thayumanavan P, Lonati E, Agrochao M, Thevelein JM:Transport and signaling through the phosphate-binding site ofthe yeast Pho84 phosphate transceptor. Proc Natl Acad SciUSA 2010, 107:2890-2895.

This study provides first mechanistic insight into the dual and separablefunctions of Pho84 as a Pi transceptor, which imports Pi and mediatesrapid activation of the protein kinase A pathway upon Pi transport.

31. Chen DL, Delatorre CA, Bakker A, Abel S: Conditionalidentification of phosphate-starvation-response mutants inArabidopsis thaliana. Planta 2000, 211:13-22.

32. Monshausen GB, Gilroy S: The exploring root–root growthresponses to local environmental conditions. Curr Opin PlantBiol 2009, 12:766-772.

33. Aisen P, Enns C, Wessling-Resnick M: Chemistry and biology ofeukaryotic iron metabolism. Int J Biochem Cell Biol 2001,33:940-959.

34. Jeong J, Guerinot ML: Homing in on iron homeostasis in plants.Trends Plant Sci 2009, 14:280-285.

35. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R,Ortet P, Creff A, Somerville S, Rolland N et al.: A genome-widetranscriptional analysis using Arabidopsis thaliana Affymetrixgene chips determined plant responses to phosphatedeprivation. Proc Natl Acad Sci USA 2005, 102:11934-11939.

36. Hirsch J, Marin E, Floriani M, Chiarenza S, Richaud P, Nussaume L,Thibaud MC: Phosphate deficiency promotes modification ofiron distribution in Arabidopsis plants. Biochimie 2006,88:1767-1771.

37.�

Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG: Theeffect of iron on the primary root elongation of Arabidopsisduring phosphate deficiency. Plant Physiol 2008, 147:1181-1191.

The first systematic analysis of the effect of Fe availability on Pi starvationresponses and primary root growth during Pi deficiency. The datasuggest that Fe toxicity as a likely consequence of elevated Fe bioavail-ability in low Pi conditions is the cause of primary root growth inhibition.

38.��

Zheng L, Huang F, Narsai R, Wu J, Giraud E, He F, Cheng L,Wang F, Wu P, Whelan J et al.: Physiological and transcriptomeanalysis of iron and phosphorus interaction in rice seedlings.Plant Physiol 2009, 151:262-274.

A systematic analysis of growth performance, nutrient concentration (Pi,Fe), and genome-scale expression profiles of roots and shoots from riceseedlings cultivated under four different nutrient conditions (two-factormatrix of Pi and Fe availability). The results provide evidence that thepresence of Pi can affect Fe availability and expression of Fe-responsivegenes.

39. Jain A, Poling MD, Smith AP, Nagarajan VK, Lahner B,Meagher RB, Raghothama KG: Variations in the composition ofgelling agents affect morphophysiological and molecularresponses to deficiencies of phosphate and other nutrients.Plant Physiol 2009, 150:1033-1049.

40. Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB: TheIRT1 protein from Arabidopsis thaliana is a metal transporterwith a broad substrate range. Plant Mol Biol 1999, 40:37-44.

41. Buckhout TJ, Yang TJ, Schmidt W: Early iron-deficiency-induced transcriptional changes in Arabidopsis roots asrevealed by microarray analyses. BMC Genomics 2009, 10:147.

42.�

Yang TJ, Lin WD, Schmidt W: Transcriptional profiling of theArabidopsis iron deficiency response reveals conservedtransition metal homeostasis networks. Plant Physiol 2010,152:2130-2141.

The analysis of transcriptional networks in response to Fe deficiencyindicates that the differential expression of metal transporters undercontrol of the basic helix-loop-helix transcription factor FIT1 probablyreflects an anticipated response rather than a reaction to IRT1-dependentchanges in metal distribution.



43. Jensen LT, Ajua-Alemanji M, Culotta VC: The Saccharomycescerevisiae high affinity phosphate transporter encoded byPHO84 also functions in manganese homeostasis. J Biol Chem2003, 278:42036-42040.

44.�

Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F:Ferritins control interaction between iron homeostasis andoxidative stress in Arabidopsis. Plant J 2009, 57:400-412.

Evidence is presented that ferritins do not constitute the major Fe pool butare essential to protect cells against Fe-mediated oxidative damage.

45. Sanchez-Calderon L, Lopez-Bucio J, Chacon-Lopez A, Gutierrez-Ortega A, Hernandez-Abreu E, Herrera-Estrella L:Characterization of low phosphorus insensitive mutantsreveals a crosstalk between low phosphorus-induceddeterminate root development and the activation of genesinvolved in the adaptation of Arabidopsis to phosphorusdeficiency. Plant Physiol 2006, 140:879-889.

46. Perez-Torres CA, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L: Phosphateavailability alters lateral root development in Arabidopsis bymodulating auxin sensitivity via a mechanism involving theTIR1 auxin receptor. Plant Cell 2008, 20:3258-3272.

47. Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T:Identification of QTL controlling root growth response tophosphate starvation in Arabidopsis thaliana. Plant Cell Environ2006, 29:115-125.

48. Wang X, Du G, Wang X, Meng Y, Li Y, Wu P, Yi K: The function ofLPR1 is controlled by an element in the promoter and is


independentofSUMOE3ligaseSIZ1 in responseto lowPistressin Arabidopsis thaliana. Plant Cell Physiol 2010, 51:380-394.

49. Jakobsen MK, Poulsen LR, Schulz A, Fleurat-Lessard P,Moller A, Husted S, Schiott M, Amtmann A, Palmgren MG:Pollen development and fertilization in Arabidopsis isdependent on the MALE GAMETOGENESIS IMPAIREDANTHERS gene encoding a Type V P-type ATPase. GenesDev 2005, 19:2757-2769.

50. Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I,Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B: TheRETINOBLASTOMA-RELATED gene regulates stem cellmaintenance in Arabidopsis roots. Cell 2005, 123:1337-1349.

51. Kosman DJ: Redox cycling in iron uptake, efflux, andtrafficking. J Biol Chem 2010, 285:26729-26735.

52.�

Tyburski J, Dunajska K, Tretyn A: Reactive oxygen specieslocalization in roots of Arabidopsis thaliana seedlings grownunder phoshate deficiency. Plant Growth Regul 2009, 59:27-36.

Comparison of the pattern of superoxide and hydrogen peroxide in roottips reveals redistribution from the elongation zone in Pi-sufficient seed-lings to the distal meristem in Pi-deprived roots.

53. Tsukagoshi H, Busch W, Benfey PN: Transcriptional regulationof ROS controls transition from proliferation to differentiationin the root. Cell 2010, 143:606-616.

54. De Tullio MC, Jiang K, Feldman LJ: Redox regulation of rootapical meristem organization: connecting root developmentto its environment. Plant Physiol Biochem 2010, 48:328-336.


Phosphate sensing in root development

Documents

Transcript of Phosphate sensing in root development