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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
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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
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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
Current Opinion in Plant Biology 2011, 14:303–309
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.
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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
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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
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306 Physiology and metabolism
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
Current Opinion in Plant Biology 2011, 14:303–309
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
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Phosphate sensing in root development Abel 307
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
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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.
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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.
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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.
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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.
Current Opinion in Plant Biology 2011, 14:303–309
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.
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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.
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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.
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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.
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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
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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.
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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.
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