JIPB

Journal of Integrative Plant Biology

Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants Zhaoliang Zhang1, Hong Liao2 and William J. Lucas1*

Invited Expert Review

1

Department of Plant Biology, College of Biological Sciences, University of California, Davis, California 95616, USA, 2State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Root Biology Center, South China Agricultural University, Guangzhou 510642, China

William J. Lucas *Correspondence: [email protected]

Free Access

Abstract As an essential plant macronutrient, the low availability of phosphorus (P) in most soils imposes serious limitation on crop production. Plants have evolved complex responsive and adaptive mechanisms for acquisition, remobilization and recycling of phosphate (Pi) to maintain P homeostasis. Spatio‐temporal molecular, physiological, and biochemical Pi deficiency responses developed by plants are the consequence of local and systemic sensing and signaling pathways. Pi deficiency is sensed locally by the root system where hormones serve as important signaling components in terms of developmental reprogramming, leading to changes in root system architecture. Root‐to‐shoot and shoot‐to‐root signals, delivered

INTRODUCTION A wide range of mineral nutrients is required by plants in order to carry out the complex processes involved in the biochemical, cellular, physiological, and developmental processes underlying growth, the ultimate goal of which is the production of viable seeds. Phosphorus (P) is one such essential nutrient, and based on its involvement as a component in numerous molecules, it falls into the macronutrient category. Examples of molecules containing P include DNA and RNA, proteins, lipids, sugars, ATP, ADP, and NADPH; that is, the element P is central to a majority of the molecular constituents required for the functioning of plant cells. Soils contain P in various forms, including inorganic orthophosphate (Pi) and organic phosphates, and it is the responsibility of the plant root system to mine the soil environment to acquire adequate supplies of this macronutrient to support growth and development. In many soils, low levels of available P place constraints on general biomass production and yield potential. Modern agricultural practice has sought to overcome this problem through application of P, in the form of fertilizer, and this approach has contributed substantially to increased crop yields. However, as available P March 2014 | Volume 56 | Issue 3 | 192–220

through the xylem and phloem, respectively, involving Pi itself, hormones, miRNAs, mRNAs, and sucrose, serve to coordinate Pi deficiency responses at the whole‐plant level. A combination of chromatin remodeling, transcriptional and posttranslational events contribute to globally regulating a wide range of Pi deficiency responses. In this review, recent advances are evaluated in terms of progress toward developing a comprehensive understanding of the molecular events underlying control over P homeostasis. Application of this knowledge, in terms of developing crop plants having enhanced attributes for P use efficiency, is discussed from the perspective of agricultural sustainability in the face of diminishing global P supplies. Keywords: Adaptation; crop engineering strategies; hormone networks; local and long‐distance sensing; phosphate; P use efficiency; stress responses; systemic signaling; transcriptional regulation; transport systems Citation: Zhang Z, Liao H, Lucas WJ (2014) Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J Integr Plant Biol 56: 192–220. doi: 10.1111/jipb.12163 Edited by: Leon V. Kochian, Cornell University, USA Received Dec. 3, 2013; Accepted Jan. 6, 2014 Available online on Jan. 14, 2014 at www.wileyonlinelibrary.com/ journal/jipb © 2014 Institute of Botany, Chinese Academy of Sciences

resources are limited, to ensure future high levels of agricultural productivity, it will be necessary to develop a better understanding of the molecular events involved in controlling P homeostasis in plants. In this review, we evaluate advances currently being made toward achieving insights into the physiological, biochemical, cellular, developmental, and genetic reprogramming that plants use to adapt to limiting P growth conditions. Application of this knowledge has already opened the door for development of crops with enhanced P use efficiency. These advances are discussed in terms of the challenges ahead that need to be overcome in order to ensure that global agriculture has the capacity to provide the food and fiber needs of all mankind.

PHYSIOLOGICAL AND BIOCHEMICAL REPROGRAMMING IN RESPONSE TO Pi STRESS To adapt to Pi stress, plants have evolved physiological and biochemical responses either to acquire more P from the environment and/or to remobilize P within the body of the plant. www.jipb.net

Phosphate sensing and signaling in plants When plants experience soil conditions in which P availability is limiting, the root system can undergo a range of adaptive phosphate stress responses (PSRs), including changes in root morphology and architecture, exudation of organic acids and phosphatases into the soil, induction or enhancement in expression of high‐affinity Pi transporters, and establishment of symbiotic association with arbuscular mycorrhizal fungi (AMF). In order to mine their soil environment for regions containing higher levels of Pi, plants may form axial roots with shallower growth angles, higher root‐to‐shoot ratios, greater dispersion of lateral roots, denser root hairs and, in some species, the formation of “cluster roots” to increase topsoil foraging and/or root exploration of soils (Lambers et al. 2011; Lynch 2011). It is important to recognize that genotypic differences exist in terms of Pi acquisition from the soil. Studies have shown that for bean, soybean, and maize, P‐efficient plant lines employ shallower root growth angles that allow them to acquire more Pi from the P‐rich topsoil, thereby allowing better growth under P‐limiting conditions compared to less efficient genotypes (Zhao et al. 2004; Calderón‐Vázquez et al. 2009; Lynch 2011). In barley, genotypes having the ability to develop longer root hairs, and thereby achieve enhanced root penetration and root‐soil contact, through increased surface area, similarly exhibit higher yield potential in P‐limited soils (Gahoonia and Nielsen 2004; Haling et al. 2013). Cluster roots are characterized by large numbers of branch rootlets, as well as dense root hairs on mature cluster roots, both of which combine to expand P acquisition volume in the rhizosphere (Cheng et al. 2011a, 2011b; Lambers et al. 2011) (Figure 1). In Arabidopsis, a reduction of primary root growth has been widely observed in response to P deficiency. For example, in a study involving some 73 ecotypes, approximately 50% showed reduced primary root growth under low P conditions (Chevalier et al. 2003). However, as similar responses have not been observed in other species, including important crops such as rice and maize, this indicates that various adaptive strategies exist in terms of root morphological changes in response to Pi‐limiting conditions (Mollier and Pellerin 1999; Shimizu et al. 2004; Niu et al. 2012). Under P deficiency conditions, another important strategy for increasing P acquisition from P‐limited soils is the release of organic acids and acid phosphatases from roots into the soil. Inorganic P in soils is generally bound, and becomes available to plants only when solubilized by Hþ or organic anions. Cluster roots of white lupin secret organic acid chelators (mainly citrate) into the rhizosphere to aid in exploiting insoluble P compounds (Cheng et al. 2011a, 2011b; Lambers et al. 2011). Likewise, soil organic P is also not directly available to plants unless hydrolyzed or mineralized into Pi by phosphatases. Recent studies have demonstrated that secretion of purple acid phosphatase can facilitate utilization of organic P in the rhizosphere (Wang et al. 2009b; Robinson et al. 2012a). Membrane transporters have great potential to improve P acquisition (Schroeder et al. 2013). Some PHT1 (high‐affinity Pi transporter) family members with functions in Pi uptake have been identified in rice, wheat, and soybean roots (Ai et al. 2009; Miao et al. 2009; Qin et al. 2012a, 2012b). Recently, localization of both low‐ and high‐affinity Pi transporters on the plasma membrane has been shown to require PHF1 (Phosphate Transporter Traffic Facilitator 1). Here, PHF1 mediates in the www.jipb.net

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exit of Pi transporters from the endoplasmic reticulum for targeting to the plasma membrane. In this way, PHF1 serves to regulate the level of transport activity involved in P acquisition and, therefore, homeostasis (González et al. 2005; Bayle et al. 2011; Chen et al. 2011b). Further studies are required to elucidate the mechanism(s) by which PHF1 acts to control P acquisition through the functioning of Pi transporters. Mycorrhizal fungi can also enhance the capacity of plants to acquire P from soils by extending root uptake volume, dissolving insoluble inorganic P, and mineralizing organic P (Richardson and Simpson 2011). AMF colonization opens an effective pathway to acquire Pi that does not involve direct uptake through the root epidermis and root hairs. Rather, in mycorrhizal associations, Pi is translocated rapidly into root cortical cells, thereby avoiding the slow diffusion‐driven movement of Pi through the soil solution to the root surface (Smith et al. 2011). Furthermore, AMF symbiosis activates expression of a series of Pi‐starvation‐inducible (PSI) genes, including P‐type Hþ‐ATPases, AM‐inducible Pi transporters and acid phosphatases (Xu et al. 2007; Chen et al. 2011a; Li et al. 2011a; Yang et al. 2012), the combination of which enhances P acquisition by the root system. Remobilization of P within the plant is also an important biochemical and physiological response to P stress. This can involve specific reprogramming, observed in terms of alteration of P allocation between the shoot and root, the release of vacuolar Pi, and by the replacement of phospholipids in membranes by sulfolipids and galactolipids (Dörmann and Benning 2002; Kelly et al. 2003; Morcuende et al. 2007; Cheng et al. 2011a). As discussed above, two forms of P exist in plants, inorganic orthophosphate (Pi) and organic phosphate. Of these, Pi concentration responds more rapidly to P stress. In several plant species, it has been shown that the Pi concentration drops much more quickly and sharply than organic phosphate with decreasing P supply (Veneklaas et al. 2012). This suggests that in plants experiencing P stress, a reduction in Pi concentration might be a general response. However, under severe P stress, leaf Pi concentration may remain relatively high, due to stunting of shoot growth, such as found in Spirodela oligorrhiza (Bieleski 1968), barley (Mimura et al. 1996), and Arabidopsis (Rouached et al. 2011). Plants can remobilize over 50% of P from senescing leaves (Aerts 1996); thus, translocation of P from the metabolically inactive older leaves to developing leaves or apical tissues is a quantitatively important source of P for new growth, especially at later growth stages or under P deficiency conditions. The purple acid phosphatase AtPAP26 has been shown to play an important role in P remobilization during leaf senescence (Robinson et al. 2012b). Phosphate transporters are also critical for P allocation and remobilization within plants (Nagarajan et al. 2011) (Figure 1).

PHOSPHATE STRESS SENSING AND SIGNALING In order to adapt to the heterogeneous nutrient availability in soils, plants have developed complex mechanisms to integrate local (within tissues and organs) and systemic sensing and signaling systems for maintenance of cellular nutrient March 2014 | Volume 56 | Issue 3 | 192–220

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Figure 1. Overview of local and systemic sensing and signaling‐mediated Pi‐starvation responses Root‐ and shoot‐specific responses to Pi deficiency are the results of local and systemic sensing and signaling pathways. Systemic signals are delivered through the xylem transpiration stream and the phloem translocation stream.

homeostasis, at the whole‐plant level. Roots perceive fluctuations in extracellular nutrient levels and send signals to the shoot, via the xylem, as a warning of impending limitation in the supply of the particular nutrient. Shoots sense these root‐ derived nutrient signals and send signals both to the shoot apices and roots, via the phloem, to adjust developmental processes and nutrient uptake (Lough and Lucas 2006; Liu et al. 2009; Lucas et al. 2013). Local Pi sensing and signaling can initiate adjustments in root system architecture (RSA) to enhance Pi acquisition, whereas the systemic, or long‐distance signaling pathways act to regulate Pi uptake, mobilization and redistribution (Linkohr et al. 2002; López‐Bucio et al. 2003; Svistoonoff et al. 2007; Thibaud et al. 2010; Chiou and Lin 2011; Nagarajan and Smith 2012). Pi itself, the phytohormones auxin, ethylene, cytokinins (CKs), abscisic acid (ABA), gibberellins (GA), and the strigolactones (SLs), along with sugars, miRNAs and Ca2þ have all been implicated in Pi local and systemic sensing and signaling pathways (Chiou and Lin 2011). Local Pi sensing and signaling It has been proposed that Pi is sensed by root‐localized mechanisms, and currently there are two ways by which plants are thought to sense Pi availability in the rhizosphere: external Pi concentration changes sensed by a root cell membrane‐localized sensor, or internal nutrient status sensed by an intracellular sensor (Forde and Lorenzo 2001; Chiou and Lin 2011; Nagarajan and Smith 2012) (Figure 2). March 2014 | Volume 56 | Issue 3 | 192–220

However, very little experimental information is available to indicate how Pi status is locally sensed by plants in either their roots or shoots. How is Pi deficiency sensed locally in roots? It has been shown that root tips are the site where Pi deficiency is sensed (Svistoonoff et al. 2007). When the root tip encounters a region of low Pi, a primary signal or stimulus (most likely Pi concentration in the apoplasm of the root tip) is perceived by a plasma‐membrane‐localized sensor. Alternatively, an internal Pi deficiency signal (such as Pi concentration in the cytoplasm) is perceived by internal sensors in root tip cells. To date, neither external nor internal Pi‐stress sensors have been identified. In a tomato cell culture assay, the external Pi concentration in the medium was held constant, while the internal Pi concentration was decreased by incubating the cells with D‐mannose and other metabolites, which are known to sequester Pi, intracellularly, into organic compounds. In these experiments, various RNase transcripts were induced, a situation which normally only occurs under Pi deprivation. Certainly these findings support the existence of an intracellular Pi sensing mechanism (Köck et al. 1998). Studies on the induction of phosphate starvation responsive (PSR) genes have also provided insight into Pi‐stress sensing in the root system. Plants grown in 125 mmol/L or 2.5 mmol/L Pi were subsequently transferred to Pi‐ depleted medium, and gene expression analysis indicated www.jipb.net

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Figure 2. Models illustrating cellular‐based mechanisms involved in local Pi‐sensing pathways In yeast, Pho84 serves as both a plasma‐membrane (PM)‐localized high‐affinity Pi transporter and as a Pi‐sensing “transceptor.” Under high Pi conditions, Pho84 senses high external Pi levels and activates Protein Kinase A (PKA) that then phosphorylates it, leading to ubiquitination and subsequent recruitment of the endocytic pathway for delivery to the vacuole for degradation. Under low external Pi levels, an internal sensor(s) is thought to upregulate expression of PSI genes, leading to enhanced expression of Pho84 and targeting of Pho84 to the PM. In plants exposed to low Pi levels, inputs from an internal sensor(s) and PHT1 family of PM‐localized Pi transporters activate PSI genes, leading to higher levels of PHT1 in the PM. However, inputs from other PM‐localized sensors cannot be discounted at this time. Under high Pi conditions, similar to the situation in yeast, PM‐localized PHT1s are proposed to sense the high external Pi level, leading to its posttranslational modification and subsequent turnover in the vacuole.

that induction of PSR genes was greatly delayed in the 2.5 mmol/L Pi grown plants compared to those grown in 125 mmol/L Pi (Lai et al. 2007). This result provides further support for the hypothesis that PSRs are mainly triggered by internal Pi status, rather than by external (apoplasmic) Pi concentration. Based on recent progress in the area of nutrient sensing and signaling, a novel concept has been established in which plasma‐membrane‐localized nutrient transporters and related proteins can function as nutrient sensors (Giots et al. 2003; Holsbeeks et al. 2004; Ho et al. 2009; Popova et al. 2010). In yeast, the high‐affinity Pi transporter, Pho84 works as a Pi “transceptor” that can sense the Pi status (Giots et al. 2003; Popova et al. 2010). In Arabidopsis, the nitrite transporter, CHL1 is also a nitrite sensor (Ho et al. 2009). Based on these findings, the possibility exists that a member of the PHT1 family of Pi transporters may sense the external Pi status and function as the external Pi sensor (Figure 2). Thus, future studies are required to resolve the question as to whether Pi deficiency is sensed externally, intracellularly or through a combination therein. Local Pi signaling in roots Upon Pi deficiency perception by the root sensing system, downstream adaptive signaling pathways become activated in the Pi‐stress sensing cells, to generate both cell‐autonomous and systemic signals that amplify the primary Pi deficiency www.jipb.net

signals (Chiou and Lin 2011; Lucas et al. 2013). Although significant progress has been made in terms of understanding PSRs, the root local signal cascades remain to be elucidated at the molecular level. Until the Pi sensor(s) is identified and characterized, it will be difficult to identify the immediate components of Pi sensing in the downstream activation pathway. Secondary signaling through Ca2þ, IPs, and ROS As universal secondary messengers in many signal transduction pathways, Ca2þ, inositol polyphosphates (IPs), and reactive oxygen species (ROS) have been considered as players in Pi sensing and signaling (Chiou and Lin 2011). The level of the plasma‐membrane Ca2þ‐ATPase, which is important for Ca2þ transport, was found to be significantly increased when tomato roots were subjected to Pi‐starvation conditions (Muchhal et al. 1997), suggesting a possible involvement of Ca2þ in Pi‐stress signaling. A role for IPs in Pi stress was established by studies on AtIPK1 that encodes an IP4 and IP5 2‐kinase which phosphorylates IP4 and IP5 as substrates to produce IP5 and IP6 in Arabidopsis. The atipk1 mutant is hypersensitive to Pi levels in the growth medium. Growth of this mutant in medium containing 1 mmol/L Pi gives rise to axially curled, smaller and necrotic leaves and this phenotype was correlated with much higher intracellular Pi concentrations (Stevenson‐Paulik et al. 2005). This atipk1 mutant is also greatly impaired in its ability to sense a change March 2014 | Volume 56 | Issue 3 | 192–220

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in Pi concentration that, in wild‐type plants, would elicit an increase in root hair development. Taken together, these findings indicate that AtIPK1 and its products, IP5 and IP6, are required for Pi sensing and P homeostasis in plants. ROS have been shown to undergo an increase in nitrogen‐, P‐, and Kþ‐deprived roots (Shin and Schachtman 2004; Shin et al. 2005). It has also been established that P deficiency affects ROS distribution in the distal parts of Arabidopsis roots (Tyburski et al. 2009). At high P, the elongation zone and the primary root meristem were the main sites of ROS production; however, at low P, ROS were not detected in the elongation zone, but were present in the proximal part of the lateral root meristem. These findings are consistent with changes in RSA, with inhibition of the primary root and promotion of lateral root growth in Pi deficiency condition, suggestive of a role for ROS in this process. Role of hormones in local Pi signaling Pi deficiency can change hormone production, sensitivity, and transport (Chiou and Lin 2011) to regulate expression of PSR genes and RSA. The problem is that hormones can act both locally and systemically, and sometimes it is even problematic to distinguish between these two modes of action. Here, we first focus on hormone action in roots and their systemic role will be addressed in a later section. It is well documented that under P deficiency conditions, plants show great plasticity in RSA in order to maximize Pi

interception and uptake. In Arabidopsis, Pi deprivation inhibits primary root but promotes lateral root growth and enhances root hair formation (Bates and Lynch 1996; Williamson et al. 2001; Linkohr et al. 2002; López‐Bucio et al. 2002, 2005; Müller and Schmidt 2004; Nacry et al. 2005). Auxin, ethylene, CKs, SLs, GA, and ABA have all been implicated in the regulation of RSA and PSR genes. Auxin has been shown to play an important role in changing RSA in plants grown under Pi deficiency conditions. Exogenous application of auxin is sufficient to cause the enhancement of lateral root and root hair growth and inhibition of primary root growth in Arabidopsis, paralleling that seen under Pi‐deficient conditions (Casimiro et al. 2001; Al‐Ghazi et al. 2003; Nacry et al. 2005). A large body of work has been published on the involvement of auxin in changes in RSA (Figure 3). Given that auxin is involved at so many levels, it is perhaps not too surprising that the findings from these studies are complex and, at times, somewhat confusing. Both exogenous auxin and auxin transport inhibitors have been used to investigate the role of this quintessential plant hormone, in terms of Pi‐induced changes in RSA. In some studies, the findings offer support for a mechanism in which auxin transport, per se, is altered in roots exposed to Pi‐ deficient conditions, a result that could explain the observed change in RSA (Neumann et al. 2000; Al‐Ghazi et al. 2003; Nacry et al. 2005). However, in other studies, the conclusion was drawn that altered auxin signaling or auxin sensitivity, rather

Figure 3. Hormone‐mediated Pi signaling pathways controlling RSA and PSI gene expression in response to Pi‐stress conditions Auxin, ethylene, and SLs levels are induced by low Pi conditions and act as positive regulators of the Pi‐starvation signaling pathways. GA and CKs levels are decreased by low Pi availability and operate as negative regulators of the Pi‐starvation signaling pathways. ABA is induced under low Pi conditions, but acts as a repressor to suppress PSI gene expression. PDR2 and LPR1/2 function to promote and inhibit primary root growth under low Pi conditions, respectively. March 2014 | Volume 56 | Issue 3 | 192–220

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Phosphate sensing and signaling in plants than changes in auxin transport, was the basis for the observed adaptations in RSA in response to Pi deficiency (López‐Bucio et al. 2002, 2005). Mutant plants that are impaired in auxin sensitivity or transport were employed to address this disparity. In one such study, similar responses of root parameters (the ratio of lateral to total root length, and lateral root number/density) to imposed Pi deficiency were observed between wild‐type and mutant plants (Williamson et al. 2001). This finding argues against a role for auxin in the observed changes in RSA. Interestingly, in another study, it was reported that most of the effects of low Pi on RSA were dramatically modified in these mutants, or in auxin treated wild‐type plants (Nacry et al. 2005). These authors concluded that auxin plays a major role in the P starvation‐induced changes of root development. The hypothesis was also offered that low P availability modifies local auxin concentrations, within the root system, through changes in auxin transport rather than auxin synthesis (Nacry et al. 2005). A modulation in auxin sensitivity, rather than a change in auxin transport, has also been proposed to explain Pi deficiency‐induced alterations in lateral root formation (Pérez‐Torres et al. 2008). Pi deficiency induces expression of TIR1 (TRANSPORT INHIBITOR RESPONSE 1), the auxin receptor which stimulates degradation of auxin response repressor AUX/IAA proteins. Induction of this degradation process could then allow the auxin response factor 19 (ARF19), and probably other ARFs, to activate or repress a set of auxin‐ responsive genes, thereby promoting lateral root growth. Consistent with this notion, OsARF16 and OsARF12 have also been shown to be associated with auxin signaling and the PSR in rice (Shen et al. 2012; Wang et al. 2014). A small ubiquitin‐related modifier (SUMO) E3 ligase, SIZ1, has been shown to be associated with PSRs (Miura et al. 2005). A role for SIZ1 in RSA was established by studies conducted on siz1 mutant plants (Miura et al. 2011). In wild‐type Arabidopsis, at the onset of a Pi‐stress treatment, auxin was shown first to accumulate in the primary root tip and then later at lateral root primordia. In the siz1 mutant, this Pi‐stress‐induced temporal pattern of auxin accumulation was found to occur earlier than in wild‐type roots. These studies indicate that SIZ1 functions to negatively regulate Pi‐stress‐induced RSA remodeling by controlling the pattern of auxin accumulation in the primary versus lateral root systems (Miura et al. 2011) (Figure 3). Collectively, these auxin and Pi‐stress studies are consistent with the hypothesis that auxin‐dependent (auxin transport or auxin sensitivity) and auxin‐independent processes coexist in the root system to regulate the alteration of RSA in response to Pi deficiency (López‐Bucio et al. 2002; Chiou and Lin 2011). Ethylene has also been shown to regulate Pi deficiency‐ induced RSA remodeling. Under Pi deficiency conditions, the enhancement of both ethylene synthesis and responsiveness in roots has long been known (He et al. 1992; Borch et al. 1999; Gilbert et al. 2000; Lynch and Brown 2001; Kim et al. 2008; Li et al. 2009b). Exogenous application of ethylene precursors to Pi‐sufficient medium can induce similar changes in RSA as observed under Pi‐deficient condition, whereas application of ethylene inhibitors prevents these changes (Borch et al. 1999; Gilbert et al. 2000; Ma et al. 2003; Zhang et al. 2003). The role played by ethylene in modulating root growth has also been extensively documented (Borch et al. 1999; López‐ www.jipb.net

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Bucio et al. 2002; Ma et al. 2003; Zhang et al. 2003; He et al. 2005; Kim et al. 2008; Chacón‐López et al. 2011). Application of 2‐aminoethoxyvinyl glycine (AVG), an inhibitor of ethylene synthesis, can increase lateral root density under Pi deficiency conditions, and reduce it under Pi‐sufficient conditions; these effects of AVG can be reversed by exogenous ethylene application (Borch et al. 1999). A similar finding was obtained with application of 1‐methylcyclopropene (MCP), an ethylene action inhibitor, in that it can increase primary root elongation under high Pi and inhibit it under low Pi conditions, and these affects can also be negated by treatment with the ethylene precursor, 1‐aminocyclopropane‐1‐carboxylic acid (ACC) (Ma et al. 2003). Studies conducted on ethylene insensitive mutants (etr1, ein2, ein3) demonstrated that, when grown under Pi‐limiting conditions, lateral root number and density were significantly higher in these mutants compared to wild‐type plants (López‐ Bucio et al. 2002). However, when grown under high Pi conditions, these two parameters were comparable between wild‐type and the ert mutant plants. In tomato, adventitious root formation is promoted under low Pi conditions, a response that was absent in the ethylene insensitive “Never‐ ripe” (Nr) line (Kim et al. 2008). As ethylene production was reduced in adventitious roots, under low Pi conditions, for both genotypes, these authors concluded that ethylene perception, rather than ethylene production, regulates the promotion of adventitious root formation in response to low Pi. Root meristem organization of plants grown under sufficient Pi can be dramatically disrupted by exogenous ethylene application, which mimics the effects of Pi deficiency on meristem development (Chacón‐López et al. 2011). In these studies, treatment with either AVG or Agþ, acting as an ethylene signaling inhibitor, limited the effects of low Pi treatment on the root meristem. Ethylene has also been shown to influence root hair development in response to low Pi (Zhang et al. 2003; He et al. 2005). This process appears to be ethylene signaling‐ independent and Pi deficiency may directly activate primary ethylene response genes involved in epidermal cell differentiation (Schmidt and Schikora 2001; Nagarajan and Smith 2012). CKs are well documented as negative regulators of PSR genes (Figure 3). Of importance here is the fact that endogenous CK levels decrease under Pi‐deficient conditions (Salama and Wareing 1979; Horgan and Wareing 1980; Kuiper et al. 1988). Exogenous CK application represses the induction of many phosphate starvation‐induced (PSI) genes, such as AtIPS1, At4, and AtPT1 (Martín et al. 2000; Franco‐Zorrilla et al. 2002; Karthikeyan et al. 2002). A microarray analysis conducted on rice indicated that CK treatment similarly represses induction of many PSI genes (Wang et al. 2006). However, mutations in CYTOKININ RESPONSE 1 (CRE1) or ARABIDOPSIS HISTIDINE KINASE 3, both encoding CK receptors, relieved this CK‐based repression, leading to restoration of PSI gene induction under Pi‐stress conditions (Franco‐Zorrilla et al. 2002, 2005). Interestingly, exogenous CKs do not repress the stimulation of root hair development by Pi starvation, which is dependent on local Pi concentration rather than whole‐plant Pi status. This finding led to the proposal that CKs act as negative systemic signals to regulate PSR genes (Martín et al. 2000). However, results from split‐root experiments have shown that systemic repression of PSI gene induction still takes place in the cre1/ahk3 March 2014 | Volume 56 | Issue 3 | 192–220

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double mutant. In addition, in a similar split‐root experiment, exogenous CK did not systemically suppress upregulation of PSI genes. These findings argue against a role for CKs in systemic repression of PSR genes (Franco‐Zorrilla et al. 2005). Strigolactones, a new class of plant hormones, are stimulants of seed germination of parasitic plants (Cook et al. 1966) and hyphal branching and root colonization by symbiotic AMF (Akiyama et al. 2005; Besserer et al. 2006). Recently, SLs were also shown to control shoot branching (Gomez‐Roldan et al. 2008; Umehara et al. 2008) and regulate root development, in addition to many other processes (Czarnecki et al. 2013; Koltai 2013). SLs act locally and systemically to regulate the acclimation of plants to Pi starvation (Czarnecki et al. 2013). In terms of their local effects, numerous studies have confirmed that the biosynthesis of SLs is greatly increased in Pi‐ stressed roots of a number of plants, including rice (Umehara et al. 2008, 2010), sorghum (Yoneyama et al. 2007a), red clover (Yoneyama et al. 2007b), tomato (López‐Ráez et al. 2008), and fabaceae species (Yoneyama et al. 2008). Consistent with these findings, rice genes involved in SL biosynthesis (D10, D17, D27) are induced by Pi deficiency, and resupply of Pi then suppresses induction of these genes (Umehara et al. 2010). Studies using SL‐deficient mutants (max3, max4), the SL‐ signaling mutant (max2) and exogenous application of the synthetic SL analog, GR24, suggest that SLs inhibit primary root growth, lateral root and adventitious root formation, and promote root hair elongation (Kapulnik et al. 2011; Ruyter‐Spira et al. 2011; Mayzlish‐Gati et al. 2012; Rasmussen et al. 2012). When Arabidopsis seedlings are germinated under low Pi conditions, at 48 h post‐germination (hpg) the root hair density is significantly increased compared with seedlings grown under sufficient Pi conditions. In contrast, studies with either max2‐1 or max4‐1 mutants indicated that root hair density was significantly lower than that of wild‐type plants grown under low Pi conditions. However, this defect only occurred at 48 hpg, as the root hair densities at 72 and 96 hpg for the max2‐1 and max4‐1 lines grown under low Pi conditions were similar to those of wild‐type seedlings under the same conditions, suggesting these defects in SL signaling were transient in nature (Mayzlish‐Gati et al. 2012). Induction of PSI genes was also reduced in these max2‐1 and max4‐1 mutants (Mayzlish‐Gati et al. 2012). As might be expected, the defects in root hair development and PSI gene expression in the max4‐1 mutant could be rescued by GR24 application, but not in max2‐1 mutant plants. The reduction of primary root growth and increase in lateral root density, by Pi deficiency, were also minimized in the max2‐1 mutant compared to wild‐type plants. Interestingly, in this study, it was also shown that IAA was sufficient to compensate for the deficiency in the max2‐1 and max4‐1 response to low Pi conditions. Taken together, these findings suggest that not only developmental processes, but also Pi deficiency sensing/ signaling responses are also regulated by SLs, probably through cross‐talk with auxin (Figure 3). Recently, GA also has been shown to regulate PSRs in Arabidopsis (Jiang et al. 2007). GA modulates Pi‐starvation‐ induced changes in RSA and anthocyanin accumulation, via a GA‐DELLA‐signaling pathway (Jiang et al. 2007). In this study, it was shown that Pi‐starvation‐induced changes, such as reduction of primary root length, increase in lateral root March 2014 | Volume 56 | Issue 3 | 192–220

density and secondary lateral root formation, an increase in the root‐to‐shoot ratio and enhancement of root hair elongation, were all repressed by exogenous GA, or by mutations conferring a substantial reduction in DELLA function, whereas the reciprocal changes were enhanced in mutants having enhanced DELLA function. Furthermore, this study showed that Pi‐starvation promoted accumulation of DELLA proteins in the nuclei of root cells, probably due to decreased levels of bioactive GA under such low Pi conditions. In contrast to the dependence of Pi‐starvation‐induced changes in RSA on the GA‐DELLA signaling pathway, Pi uptake efficiency and induction of PSI genes were not regulated by GA (Jiang et al. 2007). More recently, it was reported that a Pi‐starvation‐induced transcription factor, MYB62, regulates P homeostasis and GA biosynthesis in Arabidopsis. It is noteworthy that MYB62 expression was detected in leaves and flowers, but Pi starvation only induced its expression in leaves, suggesting MYB62 mainly functions in shoots not roots (Devaiah et al. 2009). A direct relation between ABA and PSRs has not been demonstrated, but its involvement has been speculated as the growth patterns of plants subjected to Pi‐starvation resemble those caused by treatment with ABA (Trull et al. 1997). Under Pi‐deficient conditions, xylem transport of ABA in castor bean is stimulated, but this is not so for phloem transport (Jaschke et al. 1997). The role of ABA in Pi‐stress was examined by comparing the PSR patterns between wild‐type and ABA‐ deficient aba‐1 or ABA‐insensitive abi2‐1 mutants. These studies showed that both aba‐1 and abi2‐1 plants responded normally in terms of their acid phosphatase production, reduction of plant growth and increase in root‐to‐shoot ratio, when compared with wild‐type plants, although the increase in anthocyanin accumulation in the aba‐1 mutant was reduced under low Pi condition (Trull et al. 1997). Thus, basically, these studies did not support a major role for ABA in the general PSR. However, it has been shown that ABA does act to repress the induction of At4, AtPHO1, AtPHO1;H1, AtPHT1, and AtIPS1 expression by Pi deficiency (Shin et al. 2006; Ribot et al. 2008). Hence, ABA may well play a minor role in some aspects of the PSR (Figure 3). Genetic mediators of root Pi sensing and signaling A range of genetic approaches has been employed to identify genes involving in Pi sensing and signaling. In Arabidopsis, the results from mutant analysis, natural variation, and transcriptomics assays indicate that primary root arrest by Pi deprivation is locally controlled by Pi status at the root tip, regardless of internal Pi status (Chevalier et al. 2003; Ticconi et al. 2004; Svistoonoff et al. 2007; Thibaud et al. 2010). Sensing of Pi status occurs at the root tip and the presence of a low Pi concentration at root tip is sufficient to reduce cell elongation, cell division, and root meristem viability, and the result is an inhibition of primary root growth (Ticconi et al. 2004; Svistoonoff et al. 2007). PDR2, encoding a P5‐type ATPase, regulates Pi local sensing. The pdr2 mutant exhibits hypersensitive to Pi deficiency, having a significantly shorter root system than wild‐type plants, although root length is similar to wild‐type plants when they are both grown under Pi‐sufficient conditions. This exaggerated short‐root phenotype is caused by a loss‐of‐root meristem viability. Interestingly, growth of pdr2 mutants under Pi‐deficient conditions leads to initiation of more secondary root meristems, but as the duration of the Pi‐stress increases www.jipb.net

Phosphate sensing and signaling in plants these meristems also die, and as this occurs, tertiary and quaternary root meristems emerge. Here, it is noteworthy that the Pi content in roots of the pdr2 mutant is similar to that in wild‐type roots. Overall, these results indicate that PDR2 serves to negatively regulate the local‐sensing process associated with assessment of Pi status. The sequential abortion of primary, secondary, and tertiary root meristems, in Pi‐stressed pdr2 mutants, provides genetic evidence for the operation of a developmental checkpoint system that monitors Pi availability (Ticconi et al. 2004, 2009) (Figure 3). Naturally occurring variation in the response of RSA to an imposed Pi stress, was explored in a study using 73 Arabidopsis accessions originating from around the world. These accessions were screened in terms of primary root length and lateral root number, two robust parameters in response to Pi deficiency (Chevalier et al. 2003). The findings from these studies revealed that 50% of the accessions exhibited reduced primary root length and an increase in lateral root number, and 25% had only one parameter responding to Pi deficiency, with the remaining 25% failing to respond to the imposed Pi‐stress. This clearly indicates that the changes of RSA to Pi deficiency are genetically controlled (Chevalier et al. 2003). A major quantitative trait loci (QTL) involved in primary root growth response to Pi deficiency, LPR1 (LOW PHOSPHATE ROOT 1), has been identified (Reymond et al. 2006; Svistoonoff et al. 2007) and physical contact with the primary root tip was shown to be necessary and sufficient for root growth arrest. A double mutant carrying lpr1 and lpr2, a close paralogue encoding multicopper oxidases (MCOs), showed reduced Pi‐stress‐induced inhibition of primary root growth, indicating that LPR1 and LPR2 play important roles in Pi deficiency sensing. Consistent with this notion, LPR1 is expressed in the root cap and its function is controlled by cis‐acting AC‐repeats in its promoter (Svistoonoff et al. 2007; Wang et al. 2010b). LPR1 and PDR2 are thought to work in combination to adjust root meristem activity in response to Pi deficiency (Ticconi et al. 2009). PDR2 is required for root stem cell maintenance, and under low Pi conditions, it restricts SHR (SHORT‐ROOT) movement from the endodermis into adjacent cell layers by maintaining SCR (SCARECROW) levels. PDR2 genetically interacts with LPR1/LPR2, which are epistatic to PDR2 (Figure 3). Furthermore, the expression patterns for PDR2 and LPR1 overlap in stem cell niches and the distal root meristem, and subcellular localization studies have established that both proteins localize to the ER. Based on these findings, it has been proposed that an ER‐based PDR2‐LPR1 system functions in sensing Pi deficiency and regulating low Pi‐triggered root developmental changes (Ticconi et al. 2009). However, the possible mechanism by which this PDR2‐LPR1 system might act to regulate root development, under low Pi, remains to be elucidated. Local Pi sensing and signaling in shoots Root‐derived systemic Pi deficiency signals are thought to be transported, via the xylem, to the shoot where they are then perceived by shoot‐specific sensors, thereby triggering adaptive responses within shoots (Lough and Lucas 2006; Chiou and Lin 2011; Lucas et al. 2013). Shoot‐specific Pi deficiency responses, such as reduced photosynthetic activity, increased accumulation of sugars, increased anthocyanin biosynthesis, retardation of shoot development and shoot‐specific gene www.jipb.net

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expression, have all been reported (Fredeen et al. 1989; Jacob and Lawlor 1992; Natr 1992; Raghothama 1999; Wu et al. 2003). Currently, the nature of these proposed shoot‐specific Pi deficiency sensing and signaling systems remains largely unknown. Aspects that need to be addressed in terms of the shoot response to Pi deficiency include identification of the primary and secondary signals, the molecular nature of the local sensor(s), the signaling pathways for regulating biochemical and developmental processes, the regulators/mediators of these processes and the gene regulatory network(s) that orchestrates these processes. It is probable that many signaling pathways will be common between shoots and roots; for example, various aspects involving hormone‐mediated signal transduction. In addition, under Pi deficiency conditions, elevated SL levels are normally accompanied by suppression of bud outgrowth and, hence, shoot branching. As this suppression did not occur in SL‐ deficient or ‐insensitive mutants, these findings provide support for the hypothesis that, in addition to their roles in regulating root architecture, SLs also modify shoot growth and structure (Czarnecki et al. 2013). Understanding the local sensing and signaling in shoots will be critical for building a holistic view of Pi deficiency sensing and signaling in plants.

SYSTEMIC SIGNALING External Pi status is sensed locally in root tips, but the whole‐ plant Pi level needs to be integrated via systemic sensing and signaling. This consists of xylem‐mediated root‐to‐shoot signaling and phloem‐mediated shoot‐to‐root and source tissue‐to‐vegetative apical tissue/shoot apical meristem signaling (Lough and Lucas 2006; Lucas et al. 2013). Numerous split‐ root experiments, in which the root system of an individual plant is separated and placed into two compartments containing media with different Pi concentrations, have indicated the involvement of systemic signaling in PSRs (Liu et al. 1998; Burleigh and Harrison 1999; Franco‐Zorrilla et al. 2005; Thibaud et al. 2010). Induction of PSI genes (e.g., LePT1 and LePT2 in tomato, Mt4 in Medicago truncatula, At4, ACP5, PHT1;1 in Arabidopsis) in the Pi‐deficient root compartment was shown to be systemically repressed when sufficient Pi was present in the control root compartment (Liu et al. 1998; Burleigh and Harrison 1999; Franco‐Zorrilla et al. 2005). A combination of split‐root experiments and transcriptomic analysis has offered insights into the local and systemic transcriptional responses to Pi starvation in Arabidopsis (Thibaud et al. 2010). Here, ethylene synthesis and response genes, stress‐related response genes and developmentally related genes all appear more likely to be locally regulated, whereas Pi sensing and signaling, recycling, recovery, and metal homeostasis genes seem to be more likely to be systemically regulated by Pi deficiency. Developmental processes, such as the observed lateral root and cluster root growth enhancement by Pi deficiency, were shown to be controlled by systemic Pi deficiency signaling (Linkohr et al. 2002; Shane and Lambers 2006). Leaf development, flowering time regulation, and shoot meristem activity are also thought to be controlled by systemic Pi deficiency signaling (Lough and Lucas 2006; Lucas et al. 2013). Compared with local Pi deficiency sensing and signaling, in March 2014 | Volume 56 | Issue 3 | 192–220

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recent years, considerable progress has been made in the area of Pi systemic signaling. In this part of the review, we will assess progress in the identification and characterization of the root‐to‐shoot and shoot‐to‐root signaling pathways, focusing on the signals, signaling components and regulators of Pi deficiency systemic sensing and signaling. As expected, based on the countless plant processes involving the essential nutrient P, the regulation of Pi signaling is understandably complex in nature. Although we have grouped our treatment of the signaling pathways into local and systemic signaling, the responses are actually the output of interacting signaling networks. Here, we restrict our attention to the long‐distance aspects of these signals, signaling components, and regulators of Pi deficiency. Root‐to‐shoot signaling When Pi deficiency is sensed in the root system of the plant, the stress signals must be sent from root to shoot to elicit a range of adaptive responses in these vegetative tissues. Currently, Pi itself and the hormones, CKs and SLs are thought to function as the major root‐to‐shoot signaling agents. Evidence for Pi serving as a xylem‐transmitted signal Phosphite or phosphonate (Phi) (H2PO3 or HPO32) is a Pi analog which can be transported by Pi transporters, because of its structure similarity with Pi, but it cannot be metabolized and used by plants (Carswell et al. 1996, 1997). External application of Phi suppresses plant growth through its competitive action of inhibiting Pi uptake; however, it can specifically repress PSRs, including reducing the change in root‐ shoot‐ratio, root hair development, anthocyanin accumulation, and induction of PSI genes, all of which support the notion that Pi acts as a signal (Carswell et al. 1996, 1997; Ticconi et al. 2001; Varadarajan et al. 2002; Hou et al. 2005; Kobayashi et al. 2006; Rouached et al. 2011). Analysis of the pho1 mutant, which is defective in loading Pi into the xylem transpiration stream, and, therefore has much lower Pi levels in its shoot (Poirier et al. 1991), does not provide support for this Pi signal hypothesis, given that the PSRs were suppressed even though the Pi levels were low in the pho1 shoot. These findings suggest that PHO1 may well load other Pi‐stress signals, rather than Pi itself, into the xylem as long‐ distance Pi‐stress signaling agents (Rouached et al. 2011). Consequently, the debate continues as to whether Pi itself, is a Pi‐stress signal (Figure 4). Do CKs and SLs serve as xylem‐transmitted signals? Based on our previous discussion concerning the roles played by CKs in repressing PSRs, it is clear that CKs do not serve as shoot‐to‐root systemic signals, but they are good candidates for being root‐to‐shoot signaling agents. Adding CK to the medium dramatically reduces Pi‐starvation‐induced anthocyanin accumulation as well as induction of the PSI gene, IPS1 in shoots (Franco‐Zorrilla et al. 2005), suggesting a long‐distance role for CKs in repressing various PSRs. As previously mentioned, SL biosynthesis is greatly upregulated by Pi deficiency in roots, and root‐derived SLs were detected in xylem sap and the level was upregulated by Pi deficiency in Arabidopsis (Kohlen et al. 2011). Interestingly, under these low Pi conditions, secondary rosette branches were greatly reduced in wild‐type plants, yet the max1, max2, March 2014 | Volume 56 | Issue 3 | 192–220

and max4 mutants did not shown any such reduction, consistent with a systemic role for SLs in repressing branching (Kohlen et al. 2011). Taken together, these findings support the notion that xylem transported SLs are root‐to‐shoot systemic signals to regulate changes in shoot architecture in response to Pi‐limiting conditions being experienced in the root system. Studies with the various max mutants should offer further insights into systemic roles for SLs in Pi‐stress signaling, especially in terms of modulating PSRs within the shoot. Shoot‐to‐root signaling As an efficient conduit for transferring numerous signal molecules to the various organs of the plant, the phloem plays integrative roles in development, nutrient homeostasis and defense. The phloem translocation stream contains photoassimilates, amino acids, mineral nutrients, hormones, proteins, and RNAs (siRNA, miRNA, and mRNA) (Lough and Lucas 2006; Omid et al. 2007; Buhtz et al. 2008; Deeken et al. 2008; Turgeon and Wolf 2009; Guo et al. 2013; Lucas et al. 2013). Phloem‐ mobile RNAs, proteins, sugars, and other metabolites, as well as Pi itself have been considered to function as shoot‐to‐root signaling agents (Chiou and Lin 2011) (Figure 4). MicroRNAs as shoot‐to‐root signals Fujii et al. (2005) first reported that miR399 was induced under Pi‐stress conditions, and subsequently transcript levels of its target gene, a putative ubiquitin E2 conjugase (UBC24) having five complementary sequences to miR399 in its 50 UTR (Sunkar and Zhu 2004; Allen et al. 2005), was suppressed. Constitutive expression of miR399 resulted in down‐regulation of UBC24, even under Pi‐replete conditions, and these transgenic plants accumulated higher levels of Pi and exhibited conditions of leaf necrosis (Fujii et al. 2005). Subsequent studies showed that overexpression of miR399, or a T‐DNA insertion mutant ubc24, caused an increase in Pi uptake and translocation from the root to the shoot, and impaired remobilization from mature leaves to younger tissues, thus implicating miR399 in Pi homeostasis (Chiou et al. 2006). Molecular genetic studies of the pho2 mutant, earlier identified based on its hyper‐accumulation of Pi in its leaves (Delhaize and Randall 1995), also identified PHO2 as the locus for UBC24 (Aung et al. 2006; Bari et al. 2006). Micrografting experiments demonstrated that the root genotype of pho2 was sufficient to cause over‐accumulation of Pi in wild‐type leaves (Bari et al. 2006), suggesting that absence of PHO2 in the root is important for P homeostasis. Interestingly, miR399 was detected in phloem sap collected from rapeseed and pumpkin. Furthermore, its levels in the phloem sap were shown to be strongly and specifically increased under root‐ imposed Pi deficiency conditions (Buhtz et al. 2008; Pant et al. 2008, 2009). In Arabidopsis, grafting of miR399 overexpressing scions onto wild‐type rootstocks resulted in detection of high levels of mature miR399 and a significant decrease in PHO2 in the rootstocks (Pant et al. 2008). In contrast, miR399 primary transcript levels were very low in the roots of wild‐type plants. These studies indicated that miR399 can act as a phloem‐ mobile shoot‐to‐root signal, a conclusion also supported by studies performed on tobacco (Lin et al. 2008). Taken together, these findings offer strong support for a model in www.jipb.net

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Figure 4. Pi systemic sensing and signaling pathways Root‐derived Pi‐stress signals (e.g., Pi, CKs, SLs) are transported to the shoots through the xylem transpiration stream where they elicit Pi‐stress signaling in target cells. Shoot‐derived long‐distance signals (e.g., small RNAs, mRNAs, proteins, sucrose, and potentially other metabolites) are transported through the phloem from source leaves to sinks to regulate plant growth and P homeostasis. Xylem‐mobile SLs inhibit shoot branching and may also regulate other PSRs in the shoot. Xylem‐mobile CKs negatively regulate PSRs in the shoot. In the root system, phloem‐mobile miR399, and probably miR827 and miR2111, target the transcripts of PHO2, NLA, and an E3 ligase, respectively. PHO1, PHT1, and PHF1 are downstream components of these miRNA‐ mediated pathways. Sucrose is also suggested to positively regulate changes in RSA and other PSRs. Phloem‐mobile transcripts of IAA18 and IAA28 inhibit lateral root growth and their levels in the phloem sap are increased under low Pi conditions. In shoot apical tissues, sucrose and other phloem‐mobile signals are thought to regulate vegetative developmental reprogramming in response to Pi deficiency conditions.

which a root‐derived Pi deficiency signal, transported to the shoot through the xylem transpiration stream, induces miR399 expression in the shoot, followed by its delivery to the root where it targets PHO2 transcripts for degradation (Figure 4). As miR399 and PHO2 homologues have been identified in rice, tomato, common bean, and M. truncatula, and the inverse expression patterns between miR399 and PHO2 also have been observed in rice and common bean, it would appear that the miR399‐PHO2 pathway is an evolutionarily conserved regulatory mechanism for P homeostasis among angiosperms (Kuo and Chiou 2011). www.jipb.net

Over‐accumulation of Pi in the pho2 mutant was initially explained by an upregulation in the transcript levels of two high‐affinity phosphate transporters, PHT1;8 and PHT1;9 (Aung et al. 2006; Bari et al. 2006). However, T‐DNA knockouts of these Pi transporters did not affect Pi accumulation in the pho2 mutant background (Kuo and Chiou 2011), arguing against the hypothesis that PHT1;8 and PHT1;9 act downstream of PHO2 to regulate P homeostasis. In addition, PHO2, as an E2 conjugase, should target proteins for ubiquitination and subsequent turnover, and, thus, the upregulation of genes involved in Pi transport, distribution, and remobilization, in the pho2 mutant, March 2014 | Volume 56 | Issue 3 | 192–220

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is likely caused by secondary or indirect effects of PHO2 function (Bari et al. 2006; Liu et al. 2010a; Hu et al. 2011). A genetic screen for suppressors of pho2 identified two alleles carrying missense mutations in PHO1 (Liu et al. 2012b), a gene earlier shown to function in Pi loading into the xylem (Poirier et al. 1991). In the pho2 mutant, PHO1 levels are greatly increased and Pi uptake is enhanced, whereas in the presence of a suppressor mutation in PHO1, Pi uptake is reduced. Furthermore, in response to Pi availability, PHO1 degradation is PHO2‐dependent. Transient expression of PHO1 and PHO2 in a tobacco leaf system suggested a partial colocalization, to the endomembrane system, where PHO2 E2 conjugase activity is required for PHO1 degradation. Experiments using E‐64d, an endosomal cysteine protease inhibitor, indicated that PHO2‐ dependent PHO1 degradation appears to involve multivesicular body‐mediated vacuolar proteolysis (Liu et al. 2012b). Importantly, overexpression of PHO1 in wild‐type Arabidopsis does not result in the Pi toxicity phenotype observed with pho2, suggesting additional targets of PHO2 in the miR399‐ PHO2 regulatory pathway (Liu et al. 2012b). A quantitative membrane proteomics’ approach was applied to the pho2 mutant to detect differentially expressed proteins (in the mutant compared to wild‐type plants) that might be downstream components of PHO2 (Huang et al. 2013). Protein levels for four PHT1 family Pi transporters (PHT1;1, PHT1;2, PHT1;3, and PHT1;4) and PHF1 were shown to be elevated in the pho2 mutant. PHF1 acts to facilitate the exit of PHT1 from the endomembrane system for its targeting to the plasma membrane (González et al. 2005; Bayle et al. 2011). The over‐accumulation of Pi in pho2 shoots was greatly reduced by the loss of PHT1;1, and the loss of PHF1 reduced the shoot Pi levels to those of wild‐type plants. These findings indicate that PHT1;1 and PHF1 function as downstream components of PHO2. It is noteworthy that whereas degradation of PHT1 family Pi transporters was PHO2‐dependent, this was not the case for PHF1. A potential direct interaction between PHT1;1/PHT1;4 and PHO2 was demonstrated using bimolecular fluorescence complementation in tobacco. However, using the split‐ ubiquitin yeast two‐hybrid system, only the interaction between PHO2 and PHT1;4 could be confirmed. Consistent with the interaction between PHO2 and PHT1s, the PHO2‐ mediated ubiquitination of PHT1;1/2/3 was observed in the endomembrane system (Huang et al. 2013). Together, these findings reveal a mechanism by which PHO2 regulates the amount PHT1s in the secretory pathway that targets PHT1s to the plasma membrane. Interestingly, PHO2 expression appears to be restricted to the central vascular tissue of the root, whereas PHT1;1/2/3/4 are expressed outside of the stele in epidermal, root hair, and cortical cells. Thus, a puzzling discrepancy exists between PHO2 transcriptional express and the action of PHO2 on its PHT1 target proteins. To resolve this conundrum, a non‐cell‐autonomous mode of PHO2 was proposed in terms of its regulation of P homeostasis (Huang et al. 2013). Role of miR827 and miR2111 in shoot‐to‐root Pi‐stress signaling It has been reported that in rice, miR827 (Hsieh et al. 2009; Pant et al. 2009; Lin et al. 2010; Lundmark et al. 2010), and miR2111 in Arabidopsis (Pant et al. 2009) also are highly and March 2014 | Volume 56 | Issue 3 | 192–220

specifically induced under Pi deficiency conditions. Interestingly, the amount of miR827‐like, miR2111, and several miR2111 star strands was shown to be strongly increased in the phloem sap of Pi‐stressed rapeseed (Brassica napus), suggesting they too might function as systemic Pi‐stress signals. In Arabidopsis, miR827 targets NLA (NITROGEN LIMITATION ADAPTATION) transcripts coding a protein with an N‐terminal SPX domain and a C‐terminal RING domain with ubiquitin E3 ligase activity (Peng et al. 2007; Hsieh et al. 2009; Pant et al. 2009). In rice, miR827 also targets the transcripts of two SPX domain containing proteins, OsSPX‐MFS1 and OsSPX‐MFS2 having N‐terminal SPX domains and a C‐terminal MFS domain (Lin et al. 2010). The SPX domain is named after the Suppressor of Yeast gpa1 (Syg1), the yeast Phosphatase 81 (Pho81), and the human Xenotropic and Polytropic Retrovirus receptor 1 (Xpr1), and SPX domain containing proteins have been shown to function in Pi transport, Pi‐stress sensing and signaling in yeast and plants (Secco et al. 2012). NLA was first reported to be involved in adaptive responses to nitrogen limitation in Arabidopsis (Peng et al. 2007). The nla mutant is hypersensitive to nitrogen starvation and displays an early senescence phenotype under low inorganic nitrogen (Peng et al. 2007). However, under both N‐ and P‐limiting conditions, the nla mutant does not develop an early senescence phenotype (Peng et al. 2008). Interestingly, in a genetic screen for nla suppressors, it was found that mutations in PHT1;1 and PHF1 suppressed the early senescence phenotype that was observed in the nla mutant under N starvation conditions. Performance of Pi analysis on nla mutant plants revealed that the early senescence phenotype was being caused by Pi over‐accumulation. Under low Pi conditions, miR827 was induced, whereas NLA was repressed. In addition, miR827 overexpression down‐regulates NLA expression, whereas in the miR827 mutant background, NLA expression is upregulated, thus confirming that miR827 regulates the action of NLA. Consistent with this role, miR827 overexpression can also cause Pi over‐accumulation (Kant et al. 2011). These findings demonstrate an important role for both miR827 and NLA in regulating Pi homeostasis under nitrogen deficient conditions (Figure 4). The nla mutant phenotype and the regulatory pathway consisting of miR827, NLA, PHT1;1 and PHF1 is similar to the miR399‐PHO2‐PHT1;1 pathway, especially when considering that NLA is a RING‐type E3 ubiquitin ligase. Moreover, the pho2 mutant also displays a nitrate‐dependent Pi over‐accumulation phenotype, and the nla pho2 double mutant has a similar Pi over‐accumulation phenotype as the pho2 or nla single mutant, under low nitrate conditions, suggesting that PHO2 and NLA may well be involved in the same P homeostasis regulatory pathway (Kant et al. 2011). Recently, it was reported that NLA can mediate degradation of the PHT1 family Pi transporters (PHT1;1, PHT1;2; PHT1;3, and PHT1;4) (Lin et al. 2013). This study showed that Pi over‐ accumulation in the nla mutant was due to an increase in PHT1 family Pi transporters at the protein rather than the transcript level. These studies indicated that NLA can interact with and mediate ubiquitination of plasma‐membrane‐localized PHT1s that then triggers clathrin‐dependent endocytosis, followed by endosomal sorting to vacuoles for PHT1s degradation (Figure 2). Importantly, this work also showed that NLA and PHO2 function, cooperatively, to regulate the level of PHT1s in www.jipb.net

Phosphate sensing and signaling in plants the plasma membrane and endomembrane system, respectively (Lin et al. 2013). In rice, miR827 is highly induced by Pi deficiency, but the mRNA levels for its two target genes, OsSPX‐EFS1 and OsSPX‐ EFS2 were found to respond differently, with OsSPX‐EFS1 mRNA levels being reduced, whereas those for OsSPX‐EFS2 underwent an increase (Lin et al. 2010). However, in either transgenic rice plants overexpressing miR827 or a T‐DNA knockout mutant, both OsSPX‐EFS1 and OsSPX‐EFS2 were shown to be negatively regulated by miR827. At this point, these findings suggest that in plants subjected to Pi‐stress conditions, miR827 acts in a complex manner to suppress expression of its target genes. Predicted targets of miR2111 are an E3 ligase gene (At3g27150) and a calcineurin‐like phosphoesterase gene (At1g07010) (Hsieh et al. 2009; Pant et al. 2009). In addition, the miR2111 star strand appears to target genes involved in chromatin remodeling or modification (i.e., At2g23380/CURLY LEAF and At2g28290/SPLAYED) (Pant et al. 2009). Currently, only cleavage of At3g27150 by miR2111 has been experimentally confirmed; however, the expected negative correlation between At3g27150 and miR2111 was not observed. Instead, At3g27150 was found to be slightly induced by Pi deficiency (Hsieh et al. 2009). In any event, it may be that miR2111 either regulates At3g27150 spatial expression or functions to fine‐ tune its optimal expression level (Hsieh et al. 2009). As miR2111 is highly abundant in rapeseed phloem sap collected from plants experiencing Pi deficiency, and its target E3 ligase appears to be expressed specifically in roots (Schmid et al. 2005), it may well be a component of yet another interesting systemic regulatory pathway (Pant et al. 2009). Role of mRNAs in shoot‐to‐root Pi‐stress signaling Phloem transcriptomic analyses have revealed that more than 1,000 transcripts with multiple functions are present in phloem sap collected from a number of plant species and, moreover, some 40% of these transcripts appear to be related to stress and defense response signaling (Omid et al. 2007; Deeken et al. 2008; Guo et al. 2013). These findings support the notion that the phloem plays a central role as a long‐distance communication system that integrates abiotic and biotic stress signaling, at the whole‐plant level (Lough and Lucas 2006). However, currently, of these phloem‐located mRNAs only IAA18 and IAA28 have been shown to be involved in modulation of RSA (Notaguchi et al. 2012) (Figure 4). Does sucrose function as a systemic signal? The roles of sugar, especially sucrose in Pi‐starvation responses have been well documented (Hammond and White 2008, 2011). Sucrose has been proposed to be a systemic signal of Pi signaling based on the following observations: (a) shoot‐ derived sucrose translocation in the phloem increases in the early stage of Pi deficiency; (b) Pi deficiency activates sucrose responsive genes; (c) exogenous application of sugars induces many PSR genes and removal of sucrose in the growth medium impaired induction of PSI gene expression; (d) sucrose is required for most, if not all aspects of the Pi‐starvation responses (Zakhleniuk et al. 2001; Lloyd and Zakhleniuk 2004; Franco‐Zorrilla et al. 2005; Liu et al. 2005; Hermans et al. 2006; Karthikeyan et al. 2007; Hammond and White 2008, 2011; Liu et al. 2009, 2010b; Chiou and Lin 2011; Lei et al. 2011; Smith 2013). www.jipb.net

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Exogenous sugar application, dark treatment, and stem girdling have been used to explore the importance of sugar/ photosynthates in Pi deficiency signaling. In white lupin, genes for the Pi transporter, LaPT1 and the secreted acid phosphatase, LaSAP1 were seen to be highly induced when plants were subjected to Pi‐stress conditions (Liu et al. 2005). However, induction was only observed for plants grown under normal photosynthetic conditions; expression of these genes was not upregulated in dark‐treated plants, but was quickly restored upon illumination. Induction of LaPT1 and LaSAP1 expression by Pi deficiency could also be abolished by removal of exogenously applied sucrose. Furthermore, stem girdling to block phloem translocation to the root system also resulted in a significant reduction in LaPT1 and LaSAP1 transcript accumulation (Liu et al. 2005). Parallel experiments conducted on common bean (Phaseolus vulgaris L.) yielded similar findings (Liu et al. 2010b). Taken together, these studies suggest that phloem‐mobile sugar/photosynthates may be crucial for Pi deficiency signaling. The importance of shoot‐to‐root transport of sugar in Pi deficiency responses was also suggested by genetic studies. The pho3 mutant in Arabidopsis was isolated by screening for reduced root acid phosphatase (Apase) activity in plants grown under Pi deficiency conditions. Here, pho3 displayed Pi‐deficient phenotypes; for example, lower shoot and root Pi levels, severely reduced growth, dramatically increased anthocyanin and starch accumulation in leaves, and increased PHT1;4 and PHT1;5 expression (Gottwald et al. 2000; Zakhleniuk et al. 2001; Lloyd and Zakhleniuk 2004). Interestingly, pho3 was mapped to SUC2 (SUCROSE TRANSPORTER2) (Zakhleniuk et al. 2001; Lloyd and Zakhleniuk 2004), a gene earlier shown to be important for sucrose transport into the phloem. More recently, a SUC2 overexpressing mutant, hps1 (hypersensitive to phosphate starvation 1), was isolated that displays hypersensitivity in almost all the aspects of PSRs (Lei et al. 2011). Such studies demonstrate that sugar transport, from shoot to root, is critical for Pi deficiency responses. However, under Pi‐deficient conditions, growth enhancement can exacerbate, whereas growth inhibition can suppress Pi deficiency responses (Lai et al. 2007). Moreover, inhibition of cell‐cycle activity, but not of cell expansion or cell growth, can reduce PSR gene expression. This work suggests that cell division activity can contribute to determining the magnitude of PSRs (Lai et al. 2007). It will be interesting to check the cell‐cycle activity under dark treatment and stem girdling conditions to address the nutrient or signaling roles of sucrose in Pi deficiency signaling. Finally, it is important to emphasize that the experimental conditions employed to study the role of sucrose in Pi deficiency signaling (abolishment of photosynthesis by an imposed dark treatment, application of exogenous sucrose, phloem girdling, genetic defect in sucrose transport into the phloem) may simply serve to block or impede the delivery of an essential phloem‐mobile signal(s). Ca2þ‐related shoot‐to‐root Pi deficiency signals Earlier, we discussed the involvement of Ca2þ in Pi deficiency signaling. The vacuolar Ca2þ/Hþ transporters, CAX1 and CAX3 were shown to negatively regulate PSRs and phosphate uptake. The cax1/cax3 double mutant accumulates high levels of Pi in the shoot and exhibits increased Pi transport activity (Liu et al. 2011b). Interestingly, analysis of Pi levels in cax1/cax3 scions March 2014 | Volume 56 | Issue 3 | 192–220

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grafted onto wild‐type rootstocks indicated similar high Pi levels in these scions as observed in homografted cax1/cax3 plants. These findings suggest that shoot‐derived systemic signals are responsible for the high accumulation of Pi in the cax1/cax3 mutant. It is noteworthy that, under Pi deficiency conditions, both miR399 and PHO2 have similar expression levels in the cax1/ cax3 mutant root as those measured in wild‐type roots. This suggests CAX1/CAX3 act in a miR399‐PHO2 independent signaling pathway (Liu et al. 2011b). Clearly, the identity of these putative shoot‐derived systemic signals is worthy of future studies.

TRANSCRIPTIONAL RESPONSES AND REGULATION OF Pi STARVATION During the adaption to Pi deficiency, changes in expression of many thousands of genes occur in a spatial‐temporal specific manner to coordinate Pi uptake, recycling and stress protection. Transcriptomics analyses, using microarray, suppression subtractive hybridization, and deep‐sequencing methods, provide a basis for holistic understanding of Pi deficiency acclimation. Great progress toward understanding the transcriptional responses to Pi deficiency has been made, due in large part to transcriptomics analyses on Arabidopsis (Hammond et al. 2003; Wu et al. 2003; Misson et al. 2005; Bari et al. 2006; Morcuende et al. 2007; Müller et al. 2007; Lin et al. 2011; Lan et al. 2012), but also for some other species, including rice (Wasaki et al. 2003, 2006; Pariasca‐Tanaka et al. 2009), white lupin (Uhde‐Stone et al. 2003; O’Rourke et al. 2013), maize (Calderón‐Vázquez et al. 2008), tomato (Wang et al. 2002), bean (Hernández et al. 2007), and wild mustard (Hammond et al. 2005). Many PSR genes and regulatory genes involved in such processes, ranging from Pi acquisition, remobilization and recycling, signaling, transcriptional regulation, growth and development, have been identified from such transcriptomics studies. Some important promoter elements enriched in PSR genes have also been identified. In this section of the review, we will address progress in elucidating the spatial‐temporal transcriptional responses associated with regulation of Pi starvation. Transcriptional responses to Pi deficiency Given the vital roles played by Pi in almost all biological processes, Pi withdrawal not only elicits Pi deficiency‐specific signaling events, but it also causes various changes in metabolism, thereby making it quite challenging to distinguish between the primary and secondary effects of Pi deficiency. Hence, it is very important to investigate PSR gene expression over a time course during which the plant is transitioning from a Pi‐replete state to a new static Pi‐stress condition. In this regard, PSR genes have been grouped into early (with hours of Pi withdrawal) and late (over 1 d after Pi withdrawal) responsive categories (Hammond et al. 2003, 2004; Amtmann et al. 2005; Misson et al. 2005). Generally, these transcriptomics analyses have been performed at the organ‐ specific level using entire roots and/or leaves. Early transcriptional responses Early PSR genes are thought to respond rapidly to Pi deficiency, transiently and non‐specifically, in that many stress‐response March 2014 | Volume 56 | Issue 3 | 192–220

genes are also upregulated under these conditions (Hammond et al. 2003, 2004). General stress‐responsive genes, such as those involved in peroxidase, cytochrome P450 and glutathione S‐transferase synthesis, as well as salicylic acid‐, ethylene‐, and JA‐mediated abiotic‐ and biotic‐related genes, are generally rapidly induced within a few hours (Wang et al. 2002; Hammond et al. 2003; Wu et al. 2003; Misson et al. 2005; Lin et al. 2011). Signal transduction‐related genes, such as those encoding MAP kinases, MAP kinase kinases, 14‐3‐3 proteins, calmodulins, Ca2þ‐ or calmodulin‐dependent protein kinases (CDPKs) or CDPK‐related protein kinases are also rapidly induced (Wang et al. 2002; Hammond et al. 2003; Wu et al. 2003; Misson et al. 2005; Lin et al. 2011). Various families of transcription factors, including MYB, ERF/AP2, WRKY, CCAAT‐binding, Zinc finger, bHLH, and NAC, are also upregulated shortly after imposition of a Pi‐stress condition (Hammond et al. 2003; Wu et al. 2003; Misson et al. 2005; Lin et al. 2011). In the root system, the WRKY transcription factors, WRKY18 and WRKY40 are induced by Pi deficiency within 1 h (Lin et al. 2011). Interestingly, in roots, an early characteristic response is the alteration in expression of genes involved in cell wall remodeling, including genes encoding for members of the expansin, extension, xyloglucan fucosyltransferase, chitinase, endochitinase, and pectinesterase families, consistent with roles for cell wall remodeling in Pi deficiency sensing, as well as in changes in RSA (Hammond et al. 2003; Wu et al. 2003; Misson et al. 2005; Lin et al. 2011). However, Pi deficiency‐specific responsive genes, such as those encoding for phosphate transporters, acid phosphatases, ribonucleases, SPX domain containing proteins, etc., are also beginning to undergo induction during this early phase of the PSR (Hammond et al. 2003; Wu et al. 2003; Misson et al. 2005; Morcuende et al. 2007; Lin et al. 2011). Interestingly, and somewhat surprisingly, in Arabidopsis, 6 h after initiation of a Pi‐stress treatment many root hair development‐related genes were found to be repressed (Hammond et al. 2003). Late transcriptional responses Genes that fall into the late transcriptional response category are mainly involved with regulation of downstream genes for Pi uptake, remobilization, recycling, primary and secondary metabolism, photosynthesis and protein synthesis, and turnover. In general, these adaptations serve to improve Pi acquisition from the soil and promote P use efficiency, coordinately, within the body of the plant (Hammond et al. 2004; Amtmann et al. 2005). In both leaves and roots, genes for Pi transporters, phosphatases, RNases, and enzymes involved in metabolic bypasses in glycolysis and lipid metabolism (directing increasing amounts of sulfo‐ and galacto‐lipids instead of phospholipids), are strongly induced in order to restore P homeostasis under the prevailing Pi deficiency condition (Wang et al. 2002; Al‐Ghazi et al. 2003; Hammond et al. 2003; Uhde‐Stone et al. 2003; Wasaki et al. 2003, 2006; Wu et al. 2003; Misson et al. 2005; Morcuende et al. 2007; Calderón‐Vázquez et al. 2008; Lin et al. 2011; Lan et al. 2012; O’Rourke et al. 2013). Expression of genes encoding regulators of protein synthesis is down‐regulated, but meanwhile, expression of genes encoding regulators of protein degradation is upregulated (Hammond et al. 2003; Uhde‐Stone et al. 2003; Wu et al. 2003; Misson et al. 2005; Hernández et al. 2007; Müller et al. 2007). www.jipb.net

Phosphate sensing and signaling in plants In roots, genes encoding enzymes involved with organic acid synthesis and exudation are upregulated by Pi deficiency conditions, as are genes involved in glycolysis; the latter is necessary in order to increase carbon supply for organic acid synthesis (Uhde‐Stone et al. 2003; Wasaki et al. 2006; Morcuende et al. 2007; Calderón‐Vázquez et al. 2008). Consistent with their roles in Pi deficiency signaling and changes in RSA, expression of genes for hormone synthesis, signaling, response, and metabolism is changed by long‐term Pi deficiency. Here, expression of auxin‐responsive genes, Aux/ IAA family genes, auxin‐responsive transcription factors, polar auxin transport genes, auxin synthesis, and degradation genes was observed to be affected in Pi‐starved roots, consistent with their roles in primary root inhibition and lateral root enhancement (Uhde‐Stone et al. 2003; Misson et al. 2005; O’Rourke et al. 2013). Genes involved in ethylene synthesis (ACC synthesis and oxidase) and signaling (EIN 3, ERF/AP2 transcription factors) are induced in roots by Pi deficiency (Uhde‐Stone et al. 2003; Wu et al. 2003; O’Rourke et al. 2013). Expression of CK oxidases that catalyze the degradation of CKs is also induced by Pi deficiency in white lupin roots, consistent with the negative roles played by this hormone in PSRs (Uhde‐ Stone et al. 2003; O’Rourke et al. 2013). In Arabidopsis and white lupin Pi‐starved roots, transcript levels for gibberellin‐ responsive protein CRG16, gibberellin‐regulated protein GASA3, and other gibberellin‐responsive genes were also repressed (Wu et al. 2003; O’Rourke et al. 2013). In shoots, genes involved in primary and secondary metabolic processes are broadly affected by long‐term Pi deficiency. The balance between synthesis and catabolic carbon metabolism is disrupted under Pi‐stress conditions. The expression of representative genes for photosynthesis, such as those involved in photosystem (PS) I, PSII, Rubisco small subunits, Calvin cycle enzymes and chlorophyll A/B‐ binding proteins are all repressed by Pi deficiency, whereas under these same conditions, expression is upregulated for genes involved in glycolysis, such as those that act in starch and sucrose synthesis, glucose‐6‐phosphate dehydrogenase, phosphofructokinase, frucose‐1,6‐bisphosphate aldolase, phosphoenolpyruvate carboxylase, glyceraldehyde‐3‐phosphate dehydrogenase, and sucrose transporters (Uhde‐Stone et al. 2003; Wu et al. 2003; Wasaki et al. 2006; Morcuende et al. 2007; Müller et al. 2007). These changes are assumed to reflect the necessity, under Pi‐deficient conditions, to bypass ATP‐ and Pi‐dependent enzymes and change metabolism required to generate energy and carbon skeletons (Plaxton and Carswell 1999; Amtmann et al. 2005). In addition, expression of genes involved in anthocynin biosynthesis is also upregulated (Hammond et al. 2003, 2004; Wu et al. 2003; Amtmann et al. 2005). The cross‐ talk between Pi deficiency‐ and sugar‐signaling was revealed through leaf transcriptomics analysis (Müller et al. 2007). These studies indicated that many sugar‐responsive genes are regulated by Pi deficiency and Pi deficiency‐responsive genes are also sugar‐inducible. Here, some 150 genes were found to be synergistically or antagonistically regulated by sugar and Pi deficiency. It is noteworthy that the expression of trehalose‐6‐ phophate synthase was found to be repressed in several Pi deficiency studies (Misson et al. 2005; Hernández et al. 2007; Müller et al. 2007; Nilsson et al. 2010). This observation may provide the link between Pi deficiency, sugar signaling, and www.jipb.net

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growth regulation, as trehalose‐6‐phophate has been recognized to be a key regulator of plant development and flowering control (Rolland et al. 2006; Nilsson et al. 2010; Wahl et al. 2013).

TRANSCRIPTIONAL REGULATION OF Pi DEFICIENCY RESPONSES Based on available transcriptomics databases, many transcription factors appear to be differentially expressed under Pi‐ deficient conditions, implicating them in transcriptional regulation of PSR genes. Among these Pi deficiency responsive transcription factors, six families are representative, namely those of the NAC, MYB, ERF/AP2 (Ethylene Response Factor/ APETALA2), zinc finger, WRKY, and CCAAT‐binding families (Nilsson et al. 2010). However, it is of interest to note that, because of the constitutive expression, PHR1, a central transcription factor involved in Pi transcriptional regulation, was not identified by transcriptomics analysis (Rubio et al. 2001). A number of promoter motifs linked to Pi deficiency have also been identified from interrogation of these transcriptomics databases. A number of cis‐elements enriched in early upregulated genes in response to Pi deficiency have been identified: a PHO‐like motif (CGCGTGGG), a TATA‐like motif (TATAAATA) and a known PHO motif (CACGTG/C) (Mukatira et al. 2001; Hammond et al. 2003). In a parallel study, a PHR1 binding site (P1BS: GNATATNC) (Rubio et al. 2001) was shown to be enriched in Pi deficiency‐induced gene promoters (47%) compared with the general occurrence at the whole‐genome level (18%) (Müller et al. 2007). Interestingly, in this study, the PHO motif was enriched in Pi deficiency‐repressed gene promoters (44%) compared with the general occurrence at the whole‐genome level (22%). Beside these transcription factors and Pi‐responsive promoter motifs, chromatin remodeling and posttranslational modification also have been reported to regulate Pi transcriptional responses (Figure 5). PHR1 and PHL1 as central players in Pi‐starvation transcriptional responses In a screen for Pi‐starvation regulators using an AtIPS1::GUS reporter system, an Arabidopsis mutant, phr1 (phosphate starvation response 1) was identified that had reduced GUS activity when plants were subjected to Pi‐stress conditions. Most PSRs, such as PSI gene expression, anthocyanin, sugar, and starch accumulation, Pi content, changes in root‐to‐shoot ratio, are impaired in this phr1 mutant (Rubio et al. 2001; Nilsson et al. 2007). Allocation of P between roots and shoots is also altered in this phr1 mutant (Nilsson et al. 2007). AtPHR1 encodes a conserved MYB transcription factor and its homologue in Chlamydomonas reinhardtii, PSR1 (PHOSPHORUS STARVATION RESPONSE 1) has been shown to regulate Pi‐ starvation transcription responses in this green alga (Wykoff et al. 1999). Consistent with its role as a transcription factor, PHR1 localizes to the nucleus, a process which is independent of Pi status. Different from CrPSR1 whose expression is Pi deficiency‐inducible, AtPHR1 expression is constitutive and only weakly responsive to Pi deficiency. The AtPHR1‐binding sequence is significantly enriched in the promoters a number of Pi‐starvation‐responsive genes, March 2014 | Volume 56 | Issue 3 | 192–220

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Figure 5. Transcriptional and posttranscriptional regulation of PSRs Under low Pi conditions, changes in RSA, PSI gene expression, anthocyanin accumulation, sugar/starch accumulation, Pi uptake, and subsequent xylem loading are transcriptionally and posttranscriptionally regulated by a combination of transcription factors, SIZ1, components of chromatin remodeling complexes and long non‐coding RNAs. including the IPS1/At4 family, Pi transporters, phosphatases, RNases and those involved in protein synthesis in both eudicot and monocot plant species (Rubio et al. 2001; Schünmann et al. 2004). Furthermore, overexpression studies provided additional support for a critical role for AtPHR1 as a key regulatory component of the PSRs. In these AtPHR1 overexpression plants, shoot Pi content underwent a dramatic increase, together with strongly elevated expression of PSI genes (Nilsson et al. 2007) (Figure 5). A close phylogenetic relative of PHR1, PHL1 (PHR‐Like 1) was recently identified and in the phr1 phl1 double mutant defects in the PSRs were further enhanced over the phr1 mutant (Bustos et al. 2010). Transcriptomics analysis indicated that 89% and 79% of the strongly induced Pi‐starvation genes in the shoots and roots, respectively, displayed lower expression levels in the phr1 phl1 double mutant, compared to wild‐type plants under the same Pi‐deficient conditions. Furthermore, some 69% and 48% of the strongly repressed Pi‐starvation genes in the shoots and roots, respectively, displayed lower repression by Pi deficiency, compared to wild‐type plants under these Pi‐deficient conditions. These findings indicate a central role for PHR1 and PHL1 in the control of transcriptional activation and repression responses to Pi starvation in Arabidopsis (Figure 5). These transcriptomics analyses also revealed that P1BS is significantly enriched in Pi‐starvation‐induced genes, but not in Pi‐starvation‐repressed genes, suggesting their role in controlling Pi‐starvation‐repressed gene expression is indirect (Misson et al. 2005; Bustos et al. 2010). It is noteworthy that genes encoding important regulators of P homeostasis, such as AtIPS1/At4, miRNA399, PHF1, SPX domain containing proteins (AtSPX1, AtSPX2, and SPX3, PHO1;H1), are all March 2014 | Volume 56 | Issue 3 | 192–220

targets of PHR1 (Rubio et al. 2001; Bari et al. 2006; Nilsson et al. 2007; Stefanovic et al. 2007; Duan et al. 2008; Bayle et al. 2011). OsPHR2, the functional homologue of AtPHR1 was identified in rice and its overexpression results in Pi over‐ accumulation in shoots, an effect that is correlated with upregulated expression of several Pi transporters and miR399s under Pi‐sufficient conditions (Zhou et al. 2008). Expression of PSI genes was also upregulated in OsPHR2‐overexpression plants and, in addition, root elongation and root hair growth were also enhanced. These findings indicate the important regulatory roles played by OsPHR2 in Pi homeostasis in rice. Although PHR1 transcript levels respond only weakly to Pi deficiency conditions, its protein activity was modified at the posttranslational level. As mentioned earlier, AtSIZ1 is a plant small ubiquitin‐like modifier (SUMO) E3 ligase. The siz1 mutant exhibits exaggerated Pi‐starvation responses, including enhanced changes in RSA, anthocyanin accumulation, and altered PSI gene expression consistent with the notion that SIZ1‐mediated sumoylation may well regulate PSRs. Although PHR1 was shown to be in vitro sumoylated, by SIZ1 (Miura et al. 2005), the function of PHR1 sumoylation needs to be further explored. Other transcription factors involved in Pi‐starvation transcriptional regulation The MYB62 transcription factor regulates PSRs through changes in GA metabolism and signaling. Overexpression of MYB62 alters RSA, anthocyanin accumulation, Pi uptake, and PSI gene expression, consistent with its involvement in these PSRs (Devaiah et al. 2009). Interestingly, this overexpression www.jipb.net

Phosphate sensing and signaling in plants of MYB62 resulted in GA deficiency symptoms (growth retardation, dark green and thicker leaves, late flowering), due to reduced expression of GA biosynthetic genes. A late flowering phenotype was partially rescued by exogenous GA application; however, the effects of exogenous GA application on RSA and PSI gene expression remain to be determined. Finally, an additional rice MYB transcription factor, OsMYB2P‐1 was recently reported to be involved in the regulation of PSRs and RSA (Dai et al. 2012). Three WRKY transcription factors, WRKY75, WRKY6, and WRKY42 have also been reported to regulate PSRs (Devaiah et al. 2007a; Chen et al. 2009b). Expression of WRKY75 is differentially induced, in various organs, by Pi starvation. RNAi knockdown studies showed that a reduction in WRKY75 mRNA levels caused early anthocyanin accumulation, impaired PSI gene expression and reduced Pi uptake, under Pi‐starvation conditions (Devaiah et al. 2007a). However, this silencing of WRKY75 also caused an increase in lateral root and root hair growth that was independent of Pi status, suggesting WRKY is a modulator of PSRs and root development. Both WRKY6 and WRKY42 appear to function as negative regulators of PSRs by binding to the PHO1 promoter to suppress its expression in a Pi‐ dependent manner. Under Pi deficiency conditions, WRKY6 binding to the PHO1 promoter is reduced, thereby releasing repression on PHO1 expression (Chen et al. 2009b) (Figure 5). The roles in PSRs of two bHLH transcription factors, bHLH32 in Arabidopsis and OsPTF1 (PSI TF1) in rice, have also been characterized (Yi et al. 2005; Chen et al. 2007). In the bhlh32 mutant, anthocyanin accumulation, PSI gene expression, total Pi content and root hair formation were all significantly increased compared with wild‐type plants, suggesting that bHLH32 acts as a negative regulator of PSRs, although its expression is induced by Pi starvation (Chen et al. 2007). In contrast to bHLH32 whose expression is induced in both roots and shoots, OsPTF1 displays constitutive expression in shoots, but inducible expression by Pi deficiency in roots. Furthermore, OsPTF1 overexpression enhances Pi deficiency tolerance. Surprisingly, in field‐conducted Pi‐deficient experiments, more than a 20% increase in tiller number, panicle weight, and Pi content was observed in OsPTF1 overexpression lines, compared to wild‐type plants. Microarray data showed that expression of a large number of PSR genes was altered in these OsPTF1 overexpression plants grown under Pi‐sufficient conditions (Yi et al. 2005). A C2H2 (cysteine‐2/histidine‐2) zinc finger transcription factor, ZAT6 (ZINC FINGER OF ARABIDOPSIS THALIANA 6) is induced by Pi deficiency (Devaiah et al. 2007b). RNAi suppression of ZAT6 is lethal to plants, indicating a critical role in plant growth and development. Transgenic plants overexpressing ZAT6 exhibit reduced seedling growth and altered RSA that is independent of Pi status. In addition, under an imposed Pi‐stress, ZAT6 overexpression also causes anthocyanin accumulation, reduced Pi content, and PSI gene expression is reduced during the early stages of development. These findings support the hypothesis that ZAT6 functions as a regulator of root development and P homeostasis (Figure 5). Recently, OsARF16 and OsARF12, two rice transcription factors in the ARF (auxin‐responsive factor) gene family were shown to regulate PSRs and P homeostasis (Shen et al. 2012; Wang et al. 2014). Induction of OsARF16 expression is mediated by both IAA and Pi deficiency and gene knockouts lead to www.jipb.net

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reduced sensitivity of RSA and PSI gene expression in response to Pi deficiency conditions (Shen et al. 2012). Insight into the role of OsARF12 in P homeostasis was gained from experiments conducted with the osarf12 mutant. In these plants, upregulation of Pi transporters gave rise to hyper‐accumulation of Pi in leaves and an increase in the expression levels of PSI genes. Moreover, expression levels of OsPHR2 and its downstream components, such as OsmiR399, OsPHO2, OsMiR827, OsSPX‐ MFS1, and OsSPX‐MFS2 were also affected by knocking out OsARF12 (Wang et al. 2014). This involvement of OsARF16 and OsARF12 in PSRs and P homeostasis provides further support for the presence of cross‐talk between auxin and Pi deficiency signaling systems (Figures 3, 5). Chromatin remodeling mediated transcriptional regulation of PSRs A conserved actin‐related protein, ARP6 is an essential component of the SWR1 chromatin remodeling complex that regulates transcription through deposition of the H2A.Z histone variant into chromatin (Choi et al. 2005; Deal et al. 2007). Under Pi‐sufficient conditions, expression of PSI genes is upregulated in arp6 mutants, a finding that was correlated with aggravated PSRs, including enhanced root hair growth and increased starch accumulation and phosphatase activity in shoots (Smith et al. 2010). Chromatin immunoprecipitation assays also indicated significant enrichment of H2A.Z within a group of PSI genes in wild‐type plants grown under Pi‐ sufficient conditions, but this enrichment was absent in arp6 mutant plants grown under these same conditions. More importantly, under Pi‐deficient conditions, H2A.Z enrichment in these candidate genes was significantly reduced. This work provides insight into a mechanism by which PSI gene expression is controlled through an ARP6‐mediated deposition of H2A.Z at specific genetic loci (Smith et al. 2010). The per2 (Pi deficiency root hair defective 2) mutant was shown, under Pi‐stress conditions, to have a defect in root hair elongation, as well as changes in primary root growth, lateral root number, anthocyanin accumulation, and Pi content (Chandrika et al. 2013). PER2 encodes a homeodomain protein, AL6 (ALFIN‐LIKE 6) that is a member a small family of nuclear‐ localized plant homeodomain (PHD)‐containing putative transcription factors. PHD fingers have been shown to function as “readers” of “histone code,” binding to H3K4me3 and H3K4me2 (Santos‐Rosa et al. 2002; Schneider et al. 2003; Bernstein et al. 2005). AL6 was shown to control the transcription of a number of growth‐related genes, especially those involved in root hair development. This study reveals yet another example by which PSRs are regulated at the chromatin level. Most certainly, future studies will likely uncover important effects of DNA methylation and histone modification in terms of regulating specific sets of PSR genes.

LONG NON‐CODING RNA REGULATION OF Pi HOMEOSTASIS Transcriptomics analyses using deep sequencing and tilling arrays have revealed that a significant number of long non‐ coding RNAs (lncRNAs) are transcribed from locations throughout the eukaryote genome, and their key functions in regulating gene expression are now beginning to be recognized (Kim and March 2014 | Volume 56 | Issue 3 | 192–220

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Sung 2012; Yoon et al. 2012; Kung et al. 2013). In animals and plants, these lncRNAs apply diverse regulatory mechanisms to control gene expression in trans or in cis at both the transcriptional and posttranscription levels. Flowering time control, photoperiod‐sensitive male sterility, cellulose biosynthesis, sperm cell development, CK synthesis, and abiotic or biotic stress responses have all been shown to be regulated by lncRNAs (Borsani et al. 2005; Katiyar‐Agarwal et al. 2006; Zubko and Meyer 2007; Held et al. 2008; Amor et al. 2009; Ron et al. 2010; Ding et al. 2012b; Ietswaart et al. 2012). Roles for lncRNAs in Pi homeostasis are also being uncovered. Two homologues, Mt4 (M. truncatula 4) and TPS1 (TOMATO PHOSPHATE STARVATION‐INDUCED GENE 1) and their orthologues in Arabidopsis At4 and IPS1 (INDUCED BY PI STARVATION 1), are highly Pi‐starvation‐induced lncRNAs (Franco‐Zorrilla et al. 2007). Under Pi deficiency, an At4 loss‐of‐function mutation results in a defect in the redistribution of Pi between shoots and roots, and over‐accumulation of Pi in shoots compared with wild‐type plants, whereas overexpression of IPS1 causes lower levels in shoots, suggesting an important role for these At4/IPS1 family genes in P homeostasis (Shin et al. 2006; Franco‐Zorrilla et al. 2007). Members of the At4/IPS1 family have only short, non‐ conserved open‐reading frames; however, they share a conserved 23‐nt‐long motif and, interestingly, this motif shows extensive sequence complementarity with miR399. This complementarity is interrupted by mismatches in the region required for miRNA‐guided target cleavage. Hence, At4/IPS1 lncRNAs bind miR399, but they do not undergo cleavage; this mechanism was coined “target mimicry” (Franco‐Zorrilla et al. 2007). Thus, the At4/IPS1 family lncRNAs negatively fine‐tunes the PHR1‐miR399‐PHO2 signaling pathway. Recently, it was shown that the cis‐natural antisense transcript of PHO1;2 (cis‐NATPHO1;2) acts as a translational enhancer of PHO1;2 and contributes to P homeostasis in rice (Jabnoune et al. 2013). In this crop plant, PHO1;2 is a functional orthologue of the Arabidopsis PHO1, and is constitutively expressed in root and shoot vascular tissues, under both Pi‐sufficient and Pi‐deficient conditions. In contrast, under Pi‐ stress conditions, cis‐NATPHO1;2 becomes greatly induced in shoot and root vascular tissues. Although PHO1;2 is not responsive to Pi deficiency, at the transcript level, its protein level becomes elevated under these conditions. Intriguingly, RNAi knockdown of cis‐NATPHO1;2 caused a decrease in OsPHO1;2 protein level, shoot Pi content and seed yield, whereas cis‐NATPHO1;2 overexpression caused a strong increase in the OsPHO1;2 protein level. These changes occurred under both Pi‐sufficient and deficiency conditions, and in both situations, no changes were observed in the levels of expression, processing or nuclear export of PHO1;2 mRNA (Jabnoune et al. 2013). An increased level of PHO1;2 and cis‐NATPHO1;2 transcripts were delivered to the polysomes under both Pi deficiency conditions or in plants overexpressing cis‐NATPHO1;2 (Jabnoune et al. 2013). These findings indicate that cis‐NATPHO1;2 can enhance PHO1;2 expression, at the translational level. Future studies should address the mechanism by which cis‐NATPHO1;2 controls the association of OsPHO1;2 transcripts with polysomes. One possibility is that cis‐NATPHO1;2 can associate with PHO1;2 through its overlapping region and then the free 30 ‐end of cis‐NATPHO1;2 transcript might recruit initiation factors or free March 2014 | Volume 56 | Issue 3 | 192–220

ribosomes that could then undergo translocation to the 50 ‐end of the PHO1;2 transcript to begin translation (Jabnoune et al. 2013). An Arabidopsis genome‐wide bioinformatics analysis of full‐ length cDNA databases lead to the identification of several lncRNAs, and among them, six lncRNAs were shown to be upregulated and five down‐regulated under Pi deficiency conditions (Amor et al. 2009). Future studies on the functions of these Pi‐starvation‐responsive lncRNAs might well elucidate additional novel modes of regulation for processes involved P homeostasis.

METABOLIC ADAPTATIONS: SUGAR AND LIPID METABOLISM Metabolic changes are also critical for plant adaptation to low P‐stress conditions. Remodeling of both sugar and lipid metabolism are two well‐studied metabolic adaptations to P stress in plants. Photosynthesis generally undergoes an inhibition when plants are grown under Pi‐stress conditions (Fredeen et al. 1989; Wissuwa et al. 2005). This is due to a number of factors, including the limiting effects of Pi availability on ATP generation, Rubisco activation and RuBP regeneration within the chloroplasts (Fredeen et al. 1990; Usuda and Shimogawara 1991; Rao et al. 1993). Increased sucrose biosynthesis in P‐starved leaves has been reported in Arabidopsis, bean, barley, spinach, and soybean (Hammond and White 2008). A rice microarray‐based genome‐ scale analysis indicated that low P can decrease glucose, pyruvate, and chlorophyll levels, while at the same time causing an increase in sucrose and starch levels. This indicates that P nutrition affects diverse metabolic pathways related to glucose, pyruvate, sucrose, starch, and chlorophyll (Park et al. 2012). Pi‐ starvation conditions also result in a decrease in phosphorylated sugar levels in both leaves and roots, most probably due to the lower activities of fructokinase and hexokinase (Dietz and Foyer 1986; Rychter and Randall 1994). Decreased respiration rate is also one of the reasons for accumulation of soluble sugars in P‐deficient plants (Wanke et al. 1998). The concentration of Pi has been shown to control the distribution of newly fixed carbon between starch synthesis in the chloroplasts and transfer of triose phosphate (triose‐P) to the cytoplasm for use in sucrose synthesis. In isolated chloroplasts, low Pi decreases photosynthesis and switches the flow of carbon toward starch (Heldt et al. 1977). Low Pi and high sugars in Pi‐starved plants increase ADP glucose pyrophosphorylase transcription, and, thus, starch accumulation in the chloroplasts of these plants. Furthermore, during photosynthesis, carbon is fixed in the form of triose‐P, which needs to be exported across the chloroplast envelope by means of the triose‐P/Pi antiporter system. Limiting cytosolic levels of Pi can block the function of this antiporter, thereby also redirecting triose‐P into starch production. This accumulation of starch can indirectly impede the rate of photosynthesis through a reduction in the stromal volume available to the Calvin cycle enzymes for CO2 fixation. Finally, although not completely understood at the mechanistic level, Pi‐stress also results in increased translocation of mobile carbohydrates, via the phloem, to the roots (Hermans et al. 2006) to favor root growth for better soil exploration. www.jipb.net

Phosphate sensing and signaling in plants Lipid remodeling is well known as a common adaptive mechanism to P depletion in plants. Phospholipids are important components of biological membranes. Under Pi‐stress conditions, in order to reduce the demand of P in lipid metabolism, and to provide a major source for internal Pi, plants can replace some phospholipids with phosphorus‐free galactolipid, sulfoquinovosyldiacylglycerol (SQDG), and digalactosyldiacylglycerol (DGDG) (Nakamura 2013). Increased concentrations of galactolipids have also been reported in low P Arabidopsis leaves (Benning and Ohta 2005; Gaude et al. 2008), and the expression of SQD1 and SQD2, genes encoding enzymes in sulfolipid biosynthesis, is induced both in Arabidopsis and rice seedlings under imposed Pi‐ stress conditions (Misson et al. 2005; Wang et al. 2006). In the Arabidopsis mutant, pho1, with compromised internal Pi translocation, decreases in phospholipids and increases in DGDG and SQDG have been observed in leaves (Poirier et al. 1991; Essigmann et al. 1998). Furthermore, phospholipases (Dz1 and Dz2) are involved in phosphatidylcholine hydrolysis and DGDG accumulation in Pi‐starved plants (Li et al. 2006), which convincingly demonstrates that phospholipid hydrolysis and galactolipid biosynthesis are regulated by P stress in plants. Recently, a new class of plant lipids, glucuronosyldiacylglycerol was identified having levels significantly increased in both Arabidopsis and rice plants that were subjected to Pi‐stress conditions (Okazaki et al. 2013). This important finding revealed that this novel class of lipids likely plays an important role in the plant response to P‐stress conditions.

STRATEGIES TO IMPROVE PHOSPHORUS EFFICIENCY Due to its non‐renewable nature, a limitation of P resources, as well as severe environmental problems associated with P mining and fertilization, an increase in crop P efficiency is currently receiving greater attention in sustainable agriculture systems. Improvement of P efficiency can be achieved either by enhanced P uptake from the soil (P acquisition efficiency) and/or by improved production (biomass or yield) per unit of P acquired (P utilization efficiency). Substantial genetic variation in relation to plant P efficiency has been well documented, and numerous QTLs encoding traits for crop P efficiency have been identified in rice (Ni et al. 1998; Wissuwa et al. 1998; Wissuwa and Ae 2001), maize (Chen et al. 2008, 2009a; Kaeppler et al. 2000), common bean (Liao et al. 2004; Yan et al. 2004; Beebe et al. 2006), soybean (Liang et al. 2010a, 2010b), and other crop species, such as B. napus (Yang et al. 2010, 2011; Ding et al. 2012a). Identification of QTLs and/or the underlying genes now offers an important strategy to improve P efficiency. This could be achieved by conventional or marker‐assisted breeding, genetic engineering with direct gene transformation, or a combination of these strategies. However, it is unfortunate that very few examples of successful improvement for P efficiency in crops have been reported using any of the above‐mentioned approaches. The progress that has been achieved relates to improvements in P uptake efficiency, rather than P use efficiency. Conventional breeding approaches that target P efficiency have made some progress. One example is soybean breeding in South China, where several P‐efficient soybean varieties having better root architectural traits have been nationally certified and www.jipb.net

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commercially released (Wang et al. 2010c). Compared to conventional breeding, the achievements from marker‐assisted breeding for P efficiency have been generally limited. This situation is probably due to significant environmental effects on P efficiency traits, which results in most P‐related QTLs making very small contributions to overall P efficiency. As yet, the only P‐ related QTL available to marker‐assisted breeding is Pup1 (Phosphorus uptake 1) in rice. Pup1 was introgressed into several rice varieties through a marker‐assisted backcrossing approach (Chin et al. 2011), and these lines exhibited a dramatic increase in rice P uptake efficiency, especially on P‐deficient soils. Furthermore, overexpression of PSTOL1, the rice gene responsible for the Pup1 QTL, also enhanced grain yield on P‐deficient soils (Gamuyao et al. 2012), clearly confirming the significant potential for employing Pup1 or PSTOL1 in rice breeding for P use efficiency. With the development of transgenic techniques, numerous genes have been successfully introduced into different crop species with the aim of improving P efficiency (Table 1). Among them, overexpression of phytase and phosphatase genes has generally resulted in an increase in P efficiency of host plants, regardless of the origin of the genes. Notable examples include AtPAP15 in soybean (Wang et al. 2009b), MtPHY1 in clover (Ma et al. 2009), OsPAP10a in rice (Tian et al. 2012), PhyA from Aspergillus niger in clover, cotton, and rapeseed (George et al. 2004; Liu et al. 2011a; Wang et al. 2013c), and appA from Escherichia coli in potato and rapeseed (Hong et al. 2008; Wang et al. 2013c). On a less positive note, transgenic approaches can often yield controversial results. For example, overexpression of a bacterial citrate synthase gene (CS) increased tobacco P uptake, through enhanced citrate exudation on P‐deficient soils (López‐Bucio 2000), but this effect could not be repeated (Delhaize et al. 2001). A very recent study found that overexpressing CS increased P efficiency and Al tolerance of rapeseed through increased exudation and accumulation of both citrate and malate (Wang et al. 2013b). Complexities associated with designing transgenic crops arise from both variations in the genetic background among cultivars, and also among crop species, which can lead to different results of gene transformation among individual transformants. One example is that overexpressing OsPHR2 caused P toxicity in rice (Zhou et al. 2008), but improved P efficiency in wheat (Tong YP, personal communication). Even with promising experimental results, currently, it is unfortunate that no transgenic plant lines produced for P efficiency have yet been released for commercial use. Therefore, improved crop P efficiency through transgenic approaches still has a long way to go, with concerns raised not only in solving technical problems, but also in addressing public opposition to genetically modified food.

ACKNOWLEDGEMENTS We thank Byung‐Kook Ham for assistance in preparation of figures and Zhijian Chen and Jing Zhao for help with the literature survey. Work in our laboratories on P nutrition and Pi‐ stress signaling was supported by grants from the United States Department of Agriculture, National Institute of Food and Agriculture (NIFA 201015479; W.J.L.) and the National Natural Science Foundation of China (31025022; H.L.). March 2014 | Volume 56 | Issue 3 | 192–220

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Table 1. List of genes that have been successfully introduced into different crop species for improving P efficiency Gene introduced Pi acquisition efficiency (PAE) Pi‐starvation‐response regulator OsPHR2 (rice)

Transformed crop species Rice

Main effect under P deficiency

Acid phosphatase and phytase activities appA (E. coli) Secretory phytase PHY (synthetic)

Potato

Involved in Pi‐starvation signaling and increased shoot P content Involved in Pi homeostasis and Pi‐starvation signaling Involved in Pi homeostasis Involved in Pi‐starvation signaling, Pi uptake and transport Pi uptake and translocation Involved in symbiotic Pi uptake Increased P content and plant biomass Increased Pi acquisition and seed yield Enhanced P content and grain yield Involved in Pi‐starvation signaling and increased Pi uptake and homeostasis Increased organic acids synthesis and improved Pi uptake Increased Pi uptake and seed yield Increased Pi uptake and seed yield Increased phytase activity and Pi uptake Increased P content and crop yield Enhanced plant growth and Pi uptake Enhanced uptake of extracellular organic P Increased P content and plant yield Increased Pi uptake and grain yield Increased Pi uptake and grain yield Increased Pi acquisition and utilization Increased Pi uptake and grain production in acid soils Increased Pi uptake through regulated genes expression Increased Pi acquisition and yield

Potato

Accumulated more P in leaves

Phytase phyA (A. niger)

Trifolium subterraneum

Phytase MtPHY1 (Medicago truncatula)

Trifolium repens

Increased Pi uptake when supply with phytate Increased utilization of organic P and plant biomass

SPX (SYG/PHO81/XPR1) domain genes OsSPX1 (rice) Pi transporters OsPht1;8 (rice) Leaf tip necrosis1 LTN1 (rice)

Rice Rice Rice

Pi transporters OsPht1;1 (rice) Pi transporters OsPht1;11 (rice) Pi transcription factor OsPTF1 (rice)

Rice Rice Rice

High‐affinity Pi transporter NtPT1 (tobacco) Pi‐starvation tolerance 1 PSTOL1 (rice) MYB‐like protein BnPHR1 (Brassica napus)

Rice

Citrate synthase CS (Pseudomonas aeruginosa) Phytase phyA (Aspergillus niger)

Brassica napus

Phytase appA (Escherichia coli)

Brassica napus

Phytase AfPhyA (A. ficuum)

Soybean

Acid phosphatase AtPAP15 (Arabidopsis) b‐expansin gene GmEXPB2 (soybean) Purple acid phosphatase PvPAP3 (common bean) Basic helix‐loop‐helix domain ZmPTF1 (maize) H þ ‐pyrophosphatase gene TsVP (Thellungiella halophila) Phosphate starvation response regulator TaPHR1 (wheat) Phytase phyA (A. ficuum)

Soybean

Aluminum resistance gene TaALMT1 (wheat) ath‐miR399d (Arabidopsis)

Barley

Rice Brassica napus

Brassica napus

Soybean Common bean Maize Maize Wheat Cotton

Tomato

References Zhou et al. 2008

Wang et al. 2009a; Liu et al. 2010a Jia et al. 2011 Hu et al. 2011

Sun et al. 2012a Yang et al. 2012 Yi et al. 2005 Park et al. 2007, 2010 Gamuyao et al. 2012 Ren et al. 2012

Wang et al. 2013b Wang et al. 2013c Wang et al. 2013c Li et al. 2009a Wang et al. 2009b Guo et al. 2011 Liang et al. 2010 Li et al. 2011b Pei et al. 2012 Wang et al. 2013a Liu et al. 2011a, 2011b Delhaize et al. 2009 Gao et al. 2010 Hong et al. 2008 Zimmermann et al. 2003 Richardson et al. 2001; George et al. 2004 Ma et al. 2009 (Continued)

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Table 1. (Continued)

Gene introduced Acid phosphatase MtPAP1 (M. truncatula) Malate dehydrogenase neMDH (M. sativa) Phytase MtPHY1 (M. truncatula) Acid phosphatase MtPAP1 (M. truncatula) Pi transporters MtPT4 (M. truncatula) Citrate synthase CSb (P. aeruginosa) Phytase ex::phyA (A. niger) b‐propeller phytase (Bacillus subtilis) Acid phosphatase LASAP2 (white lupin) Malate dehydrogenase amdh (Arabidopsis) Malate dehydrogenase emdh (E. coli) Purple acid phosphatases OsPHY1 (rice) Malate dehydrogenase MDH (Penicillium oxalicum) Phytase LASAP3 (white lupin)

Transformed crop species Trifolium repens Medicago sativa Medicago sativa Medicago sativa Medicago truncatula Tobacco Tobacco Tobacco Tobacco Tobacco Tobacco Tobacco Tobacco Tobacco

Zinc finger transcription factor TaZFP15 (wheat) Acid phosphatase AtPAP18 (Arabidopsis) Pi utilization efficiency (PUE) MYB transcription factor OsMYB2P‐1 (rice)

Tobacco

Acid phosphatases OsPAP10a (rice)

Rice

Type I Hþ‐pyrophosphatase AVP1 (Arabidopsis) High‐affinity Pi transporter GmPT5 (soybean)

Rice and tomato

Tobacco

Rice

Soybean

Main effect under P deficiency Increased utilization of organic P and plant biomass Increased organic acid exudation and Pi acquisition Increased Pi acquisition and biomass yield Increased Pi acquisition and biomass yield Relative to symbiotic Pi acquisition and AM symbiosis Increased shoot P content and leaf and fruit biomass Increased Pi uptake when phytate as substrate Increased shoot P content and shoot biomass Increased Pi uptake and growth Increased P content and plant biomass Increased P content and plant biomass Increased P content and biomass

References Ma et al. 2009 Tesfaye et al. 2003 Ma et al. 2012 Ma et al. 2012 Javot et al. 2007 López‐Bucio et al. 2000 George et al. 2005 Lung et al. 2005 Wasaki et al. 2009 Wang et al. 2010a Wang et al. 2010a Li et al. 2012

Increased P content and utilization Improving Pi mobilization and uptake Increased Pi acquisition and plant biomass Improved Pi metabolism and biomass production

Lü et al. 2012

Involved in Pi‐starvation signaling, increased biomass under lo w P condition Improved ATP hydrolysis and utilization Improved shoot mass and higher yields Maintained Pi homeostasis and regulated nodulation and plant growth

Dai et al. 2012

Maruyama et al. 2012 Sun et al. 2012b Zamani et al. 2012

Tian et al. 2012 Yang et al. 2007 Qin et al. 2012a, 2012b

Modified from Ramaekers et al. (2010).

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March 2014 | Volume 56 | Issue 3 | 192–220

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Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants.

As an essential plant macronutrient, the low availability of phosphorus (P) in most soils imposes serious limitation on crop production. Plants have e...
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