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. 2011 Apr 12;156(3):1033–1040. doi: 10.1104/pp.111.175380

Sugar Signaling in Root Responses to Low Phosphorus Availability1

John P Hammond 1,*, Philip J White 1
PMCID: PMC3135921  PMID: 21487049

Over the last decade, major advances have been made in our understanding of how plants sense, signal, and respond to soil phosphorus (P) availability (Amtmann et al., 2006; White and Hammond, 2008; Nilsson et al., 2010; Yang and Finnegan, 2010; Vance, 2010; George et al., 2011). Previously, we have reviewed the potential for shoot-derived carbohydrate signals to initiate acclimatory responses in roots to low P availability. In this context, these carbohydrates act as systemic plant growth regulators (Hammond and White, 2008). Photosynthate is transported primarily to sink tissues as Suc via the phloem. Under P starvation, plants accumulate sugars and starch in their leaves. Increased loading of Suc to the phloem under P starvation primarily functions to relocate carbon resources to the roots, which increases their size relative to the shoot (Hermans et al., 2006). The translocation of sugars via the phloem also has the potential to initiate sugar signaling cascades that alter the expression of genes involved plant responses to low P availability. These include optimizing root biochemistry to acquire soil P, through increased expression and activity of inorganic phosphate (Pi) transporters, the secretion of acid phosphatases and organic acids to release P from the soil, and the optimization of internal P use (Hammond and White, 2008).

Here, we provide an Update to the field of plant signaling responses to low P availability and the interactions with sugar signaling components. Advances in the P signaling pathways and the roles of hormones in signaling plant responses to low P availability are also reviewed, and where possible their interactions with potential sugar signaling pathways.

SUGAR SIGNALING

Shoot-derived carbohydrates are transported from their source tissues to sinks within the plant via the phloem, together with other metabolites, nutrients, and signaling molecules (Turgeon and Wolf, 2009). Shoot-derived carbohydrates have been shown to fulfill a dual role in plants, as both metabolites and signaling molecules (Smeekens et al., 2010). Shoot-derived carbohydrates act as intermediary substrates for metabolism, providing carbon for growth and enabling sink tissues to grow and develop. These carbohydrates also possess the ability to act as growth-promoting or growth-inhibiting signaling molecules. Growth-promoting signaling cascades include the hexokinase Glc sensor and trehalose 6-phosphate signal. Signaling systems that inhibit growth and have inputs from carbohydrates include the SNF1-Related Protein Kinase1 (SnRK1) and bZIP transcription factor signaling network (Smeekens et al., 2010). Of the carbohydrates present in phloem sap, the most common (in most plants) is Suc. As yet, a Suc-specific sensor has not been identified, although Suc-dependent signaling pathways have been observed (Wind et al., 2010). Since Suc can be converted to hexoses, which themselves have signaling roles, it is difficult to partition the effect to Suc, although in the absence of similar effects with Glc and Fru, a Suc-specific signaling pathway can be speculated (Wind et al., 2010).

For shoot-derived carbohydrates to act as causal intermediary signals in coordinating root responses to P starvation, they must meet the following criteria (compare with White, 2000): (1) root physiological and biochemical responses must be preceded by an increase in the biosynthesis of shoot carbohydrates and their translocation via the phloem to the root; (2) blocking the biosynthesis or translocation of shoot carbohydrates must eliminate, or attenuate, the root physiological and biochemical responses to P starvation; and (3) artificial changes in carbohydrate concentrations in the root, similar to those experienced in P-starved plants, must initiate similar responses to those induced by P starvation (Hammond and White, 2008).

P SIGNALING PATHWAYS

In many soils, the phytoavailability of P is extremely low (Kirkby and Johnston, 2008). Consequently, plants have evolved mechanisms to cope with low P availability. Plant adaptations to low P availability are thought to be initiated through both local and systemic signaling pathways (Thibaud et al., 2010). Local signaling of soil P availability appears to regulate adaptive responses to localized patches of soil P (Linkohr et al., 2002). Adaptations under the regulation of local signaling pathways include increased root hair length (Bates and Lynch, 1996), reduced activity of the primary root meristem (Ticconi et al., 2004; Sánchez-Calderón et al., 2006; Jain et al., 2007a; Svistoonoff et al., 2007; Fang et al., 2009), and increased density and elongation of lateral roots in regions of high P availability (López-Bucio et al., 2002; Reymond et al., 2006).

Using an experimental system in which half of the plant’s root system is supplied with adequate P while the other half of the plant’s root system is supplied with little or no P, it has been demonstrated that long-distance systemic signaling pathways also regulate plant responses to low P availability (Fig. 1; Franco-Zorrilla et al., 2005; Thibaud et al., 2010). The primary signal in initiating these systemic pathways has not been identified. However, shoot P concentration is thought to be an important factor, but Pi itself is not considered to be the sole component. The Arabidopsis (Arabidopsis thaliana) MYB transcription factor AtPHR1 was the first component implicated in the systemic P signaling pathway. The AtPHR1 protein binds to an imperfect palindromic sequence (P1BS; GNATATNC) present in the promoter regions of many genes whose expression responds systemically to P starvation (Rubio et al., 2001; Bustos et al., 2010). These genes include several encoding transcription factors, protein kinases, Pi transporters, RNases, phosphatases, metabolic enzymes, and enzymes involved in the synthesis of sulfolipids and galactolipids (Rubio et al., 2001; Hammond et al., 2003; Franco-Zorrilla et al., 2004; Misson et al., 2005; Jain et al., 2007b; Fang et al., 2009; Lin et al., 2009). The functions of the rice (Oryza sativa) orthologs of AtPHR1, OsPHR1 and OsPHR2, have recently been characterized (Zhou et al., 2008a). Mutant rice plants with reduced expression of OsPHR1 or OsPHR2 had reduced expression of genes associated with plant responses to low P availability, while only mutant plants overexpressing OsPHR2 resulted in the excessive accumulation of Pi under P-sufficient conditions (Zhou et al., 2008a). This is consistent with the phenotype of Arabidopsis plants overexpressing AtPHR1 (Zhou et al., 2008a). Other members of the Arabidopsis PHR1-like family have also been implicated in regulating aspects of plant responses to low P availability (Amtmann et al., 2006; Bustos et al., 2010; Lundmark et al., 2011). Another MYB transcription factor, AtMYB62, has also been implicated in P signaling, and its expression increases in leaves of plants lacking P (Devaiah et al., 2009). The overexpression of AtMYB62 altered root architecture, Pi uptake, and acid phosphatase activity and down-regulated several genes involved in plant responses to low P availability (Devaiah et al., 2009). In addition, this mutant had a characteristic GA-deficient phenotype that could be partially reversed by exogenous application of GA (Fig. 1).

Figure 1.

Figure 1.

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Overview of Arabidopsis P signaling pathways. Arrows linking boxes indicate positive regulation, and blunt ends indicate negative regulation. Dashed arrows indicate potential regulation. Arrows within boxes indicate increase or decrease in hormone.

The expression of PHR1 appears to be constitutive, but the PHR1 protein is targeted posttranscriptionally by a small ubiquitin-like modifier (SUMO) E3 ligase (SIZ1), whose expression is increased by P starvation (Miura et al., 2005). The activity of SIZ1 acts as a negative regulator of plant responses to P starvation (Miura et al., 2005) and has also been implicated in abscisic acid signaling, temperature sensing, regulation of flowering (Jin et al., 2008; Penfield, 2008; Miura et al., 2009), and the negative regulation of auxin patterning in roots, altering root system architecture under low P availability (Miura et al., 2011). Interestingly, the transcription factor AtMYB62 contains potential target sites for SUMOylation (Fig. 1; Devaiah et al., 2009).

Among the targets of the PHR1 protein are members of the miR399 microRNA family and the SPX (for SYG1/Pho81/XPR1) gene family (Bari et al., 2006; Franco-Zorrilla et al., 2007; Nilsson et al., 2007; Lin et al., 2009). The expression of miR399s is specifically and rapidly up-regulated by P starvation (Chiou, 2007). The target for miR399s is AtUBC24/PHO2, which is down-regulated during P starvation. This gene encodes the ubiquitin E2 conjugating enzyme responsible for the pho2 mutant phenotype, which is thought to down-regulate the transcription of a subset of genes responsive to low P availability through intermediary transcription factors (Chiou, 2007; Fang et al., 2009). Expression of AtUBC24/PHO2 in roots appears to be regulated systemically by shoot P status and the translocation of miR399s in the phloem (Buhtz et al., 2008; Lin et al., 2008; Pant et al., 2008). The rate of their translocation in the phloem is likely to be influenced indirectly by Suc loading and unloading in the shoot and root, respectively. Members of the IPSI1/Mt4/At4 family of noncoding transcripts, whose expression is rapidly and specifically induced in response to P starvation, appear to bind and sequester miR399s, thereby attenuating miR399-mediated transcriptional responses to P starvation (Franco-Zorrilla et al., 2007). In addition to miR399, several other microRNA species have been implicated in regulating plant responses to low P availability (Hsieh et al., 2009; Pant et al., 2009; Gu et al., 2010; Lin et al., 2010; Lundmark et al., 2010; Zhu et al., 2010). These include miR156, miR158, miR163, miR319, miR391, miR447, miR778, miR827, miR866, and miR2111, which increase in abundance in plants during P starvation. Importantly, the presence of miR399, miR2111, and miR827 has been detected in phloem sap under P-limitingconditions, supporting a role for these molecules in long-distance regulation of plant root responses to low P availability (Pant et al., 2008, 2009). While some of these microRNA species are associated with other developmental processes (e.g. miR156 and miR319; Palatnik et al., 2003; Wu and Poethig, 2006; Wu et al., 2009), the function of the other microRNAs is less clear and requires further investigation. Potential targets for some of these microRNA species have been identified and are consistent with plant signaling pathways for low P availability. Targets for miR778 and miR2111 microRNA species include genes involved in the regulation of chromatin, including two histone methyltransferases (At2g23380), and a chromatin-remodeling complex subunit (At2g28290; Pant et al., 2009). A putative role for histone H2A.Z has recently been proposed in the transcriptional suppression of genes that respond to P deficiency in plants (Smith et al., 2010). miR2111, which has a high abundance in the phloem, also targets a root-specific E3 ligase gene (At3g27150), suggesting a role in signaling root modifications to low P availability (Pant et al., 2009). Interestingly, miR827 targets the transcripts of specific SPX domain-containing proteins, but these are dependent on the species. In both rice and Arabidopsis, miR827 is induced by P deficiency. However, in rice, it is preferentially expressed in leaf tissue and targets two SPX-MSF genes, negatively regulating them, but in a differential manner, targeting Os-SPX-MSF1 under low-P conditions and Os-SPX-MSF2 under optimal P conditions (Lin et al., 2010). In Arabidopsis, miR827 is mainly expressed in the roots and targets the transcripts of a SPX-RING protein (At1g02860) involved in ubiquitin-regulated protein degradation in response to nitrogen availability and is involved in anthocyanin production (Fig. 1; Peng et al., 2007; Hsieh et al., 2009; Pant et al., 2009; Lin et al., 2010).

The SPX domain-containing proteins contain a similar domain to the yeast PHO81 protein, the putative sensor of Pi levels in yeast (Lenburg and O’Shea, 1996). Several SPX domain-containing proteins have been implicated in plant responses to low P availability. The expression of genes encoding the SPX domain-containing proteins AtPHO1 and AtPHO1;H1 and a rice ortholog, OsPHO1;2, is up-regulated during P starvation, and these proteins are thought to regulate root-to-shoot translocation of Pi via the xylem (Stefanovic et al., 2007; Secco et al., 2010). Of the two Arabidopsis PHO1 proteins, only AtPHO1;H1 contains a PHR1-binding site and is dependent on PHR1 for its induction. In rice, the OsPHO1;2 genomic locus also contains a natural antisense transcript, which may act to regulate the expression of the gene spatially or in response to P availability (Secco et al., 2010). In Arabidopsis, AtPHO1 is thought to be regulated by the transcription factor WRKY6, which represses AtPHO1 expression under P-replete conditions, and a decrease in the abundance of the AtWRKY6 protein under low-P conditions is thought to be mediated through 26S proteosome proteolysis (Fig. 1; Chen et al., 2009).

In Arabidopsis, the expression of AtSPX1 and AtSPX3 is increased by P starvation (Duan et al., 2008). Increased expression of AtSPX1 up-regulates the transcription of several genes, including AtPAP2, AtRNS1, and AtACP5 (Duan et al., 2008). Increased expression of AtSPX3 occurs upon prolonged P starvation and appears to act in feedback regulation of plant responses to P starvation by down-regulating the expression of AtSPX1, At4, and genes encoding several Pi transporters, RNases, and phosphatases (Duan et al., 2008). Functional homologs of these genes have been identified in bean (Phaseolus vulgaris; Tian et al., 2007) and rice (Wang et al., 2009a, 2009b; Liu et al., 2010a). In rice, OsSPX1 is induced by low P availability in the roots and acts downstream of OsPHR2 (Wang et al., 2009a). However, OsSPX1 appears to regulate different subsets of P-responsive genes and regulates other members of the OsSPX family in rice differentially between tissues (Wang et al., 2009b). Recently, OsSPX1 has been shown to negatively regulate the expression of OsPHR2 and, consequently, the expression of the rice Pi transporter OsPT2 (Liu et al., 2010a).

HORMONAL INFLUENCES ON PLANT RESPONSES TO P AVAILABILITY

Changes in the local concentration, transport, or sensitivity of auxin, ethylene, and cytokinin have been implicated in effecting plant responses to low rhizosphere or plant P status, including the development of root hairs, lateral roots, and root clusters, although some studies provide conflicting results (Rubio et al., 2009). Detailed analyses of root system architecture in P-starved Arabidopsis have suggested that a change in the transport of auxins has an important role in initiating lateral root primordia (López-Bucio et al., 2005; Nacry et al., 2005). The expression of the TIR1 gene, which encodes the auxin receptor component of the ubiquitin protein ligase complex SCFTIR1, is increased by P starvation (Pérez-Torres et al., 2008). The up-regulation of TIR1 results in the degradation of AUX/IAA auxin response repressors, allowing the expression of ARF transcription factors, such as ARF19, to modulate the expression of genes enabling the initiation and emergence of lateral roots without increasing root auxin concentrations (Pérez-Torres et al., 2008). More recently, the negative regulation of auxin patterning in plant root systems responding to low P availability has also been associated with the activity of the SUMO E3 ligase SIZ1 (Fig. 1; Miura et al., 2011). Ethylene has also been implicated in the stimulation of root elongation and root hair growth under P starvation (Gilbert et al., 2000; Michael, 2001; Ma et al., 2003; Zhang et al., 2003). Experiments treating Arabidopsis plants with ethylene inhibitors or ethylene precursors suggest that ethylene is important for stimulating lateral root elongation and reducing primary root elongation but not for lateral root initiation during P starvation (López-Bucio et al., 2002; Ma et al., 2003). More recently, the Arabidopsis mutant hsp2 was identified by screening for increased expression of the Arabidopsis Pi transporter AtPT2 (Lei et al., 2011b). Since this mutant lacks a functional CTR1 gene, a negative regulator of plant responses to ethylene, Lei et al. (2011b) concluded that ethylene is important for regulating plant responses to low P availability. Acid phosphatase activity is also increased in the hsp2 mutant (Lei et al., 2011b). Cytokinin concentrations have been observed to decrease in the roots of P-starved plants (Kuiper et al., 1988). Cytokinins have been shown to suppress lateral root initiation in Arabidopsis plants during P starvation (López-Bucio et al., 2002). Therefore, a decrease in root cytokinin concentration during P starvation may serve to release the inhibition of root growth and act as a negative control mechanism for increased root growth and other P starvation responses (Fig. 1; Martín et al., 2000; Franco-Zorrilla et al., 2002).

The role of GA in regulating plant responses to low P availability is less well established. However, the application of exogenous GA and the repression of GA-DELLA signaling components repressed shoot and root Pi starvation responses (Jiang et al., 2007). The GA-deficient phenotype of the Arabidopsis myb62 mutant also implicates GA signaling pathways in plant responses to low P availability (Fig. 1; Devaiah et al., 2009). Strigolactones have been known as rhizosphere signaling molecules for many years (Bouwmeester et al., 2003) and are implicated in the regulation of shoot branching (Gomez-Roldan et al., 2008). Recently, the concentration of strigolactones has been shown to increase in the roots of P-deficient Arabidopsis plants and their exudates and has been implicated in shoot architectural remodeling in response to low P availability (Kohlen et al., 2011).

INTEGRATING PHOSPHATE AND SUGAR SIGNALING PATHWAYS

Increases in shoot-derived carbohydrates have been observed in many plant species in response to low P availability (Foyer and Spencer, 1986; Cakmak et al., 1994; Ciereszko et al., 1996; Ciereszko and Barbachowska, 2000; Morcuende et al., 2007; Müller et al., 2007; Lundmark et al., 2010). Increased leaf Suc concentrations lead indirectly to (1) a reduction in photosynthesis through decreased expression of genes encoding many photosystem subunits and small subunits of Rubisco (Lloyd and Zakhleniuk, 2004; Amtmann et al., 2006; Hermans et al., 2006; Rook et al., 2006; Morcuende et al., 2007), (2) an increase in leaf sulfolipid and galactolipid concentrations through the up-regulation of genes involved in their biosynthesis (Dörmann and Benning, 2002; Benning and Ohta, 2005; Gaude et al., 2008), and (3) the production of anthocyanins through a transcriptional cascade involving the transcription factors TTG1-TT8/EGL3-PAP1/PAP2 (Lloyd and Zakhleniuk, 2004; Teng et al., 2005; Amtmann et al., 2006; Solfanelli et al., 2006). An increased leaf Suc concentration also results in the up-regulation of genes encoding transport proteins delivering Suc to the phloem, which facilitates the movement of Suc to the root (Hermans et al., 2006). Metabolism is rerouted by employing reactions that do not require Pi or adenylates, and under severe P starvation, intracellular phosphatases and nucleases are produced to remobilize P from cellular metabolites and nucleic acids (Plaxton and Carswell, 1999; Hammond et al., 2003; Wasaki et al., 2006; Morcuende et al., 2007; Müller et al., 2007).

One consequence of the increased delivery of sugars to plant roots is an increase in the root-shoot biomass ratio (Hermans et al., 2006; Hammond and White, 2008). In addition, the Suc delivered to the root acts as a systemic signal to initiate changes in gene expression, altering root biochemistry and the morphology of the root system (Nilsson et al., 2010; Yang and Finnegan, 2010; George et al., 2011). Increased root Suc concentrations appear to up-regulate genes encoding riboregulators, Pi transporters, RNases, phosphatases, and metabolic enzymes in combination with the PHR1 transcriptional cascade, while its effects on lateral rooting occur through the modulation of auxin transport (Jain et al., 2007a; Pérez-Torres et al., 2008) and those on root hair development are contingent upon changes in auxin transport and the local production of ethylene (Fig. 2; Jain et al., 2007a). However, changes in cytokinin signaling during P starvation appear to be a secondary response, as a consequence of cross talk between sugar and P signaling cascades (Franco-Zorrilla et al., 2005). The proliferation of lateral roots of P-starved plants in regions of increased Pi availability is also contingent upon growth of the primary root apex through these regions (Drew, 1975) but appears to be initiated by changes in auxin transport and perception (Nacry et al., 2005; Sánchez-Calderón et al., 2006; Jain et al., 2007a; Hammond and White, 2008; Pérez-Torres et al., 2008), with greater Suc availability increasing the responsiveness to auxin (Fig. 2; Nacry et al., 2005; Jain et al., 2007a).

Figure 2.

Figure 2.

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Shoot-to-root Suc signaling pathways affecting plant responses to low P availability. Arrows linking boxes indicate positive regulation, and blunt ends indicate negative regulation. Arrows within boxes indicate increase or decrease in hormone.

Inhibition of Suc biosynthesis and/or translocation attenuates plant responses to P starvation (Hammond and White, 2008). The pho3 mutant was isolated by screening for root acid phosphatase activity and was identified as having 30% less acid phosphatase activity, a typical response to low P availability, than wild-type plants and showing attenuated responses to P starvation (Zakhleniuk et al., 2001). The pho3 mutation was identified as a mutation in SUC2, a Suc transporter involved in phloem loading (Lloyd and Zakhleniuk, 2004), although the SUC2 transporter is also capable of transporting other carbohydrate substrates (Chandran et al., 2003). Consequently, the pho3 mutant has constitutively high shoot carbohydrate concentrations compared with wild-type plants due to its limited ability to translocate Suc to the roots (Lloyd and Zakhleniuk, 2004). In addition, the application of 14C-labeled Suc to the leaves of suc2 plants resulted in very little translocation of the labeled Suc to the roots compared with wild-type plants (Gottwald et al., 2000). Since the mutant was originally identified in a screen for mutants with impaired root phosphatase activity, this suggests that a restriction in phloem Suc loading interferes with at least some aspects of plant P starvation responses. Recently, a T-DNA mutant that overexpresses SUC2 has been identified and characterized (Lei et al., 2011a). This mutant (hps1) has high Suc concentrations in both shoot and root tissues as a consequence of the overexpression of SUC2 and enhanced sensitivity to many aspects of plant responses to low P availability when grown under P-replete conditions in medium containing Suc, including increased acid phosphatase activity, anthocyanin accumulation, lateral root production, root hair density, and reduced primary root development (Lei et al., 2011a). Global transcriptome analysis also indicated that 73% of the genes that are induced by Pi starvation in wild-type plants can be induced by elevated levels of Suc in hps1 mutants, even when they are grown under Pi-sufficient conditions (Lei et al., 2011a).

Increasing root carbohydrate concentration enhances root P starvation responses (Hammond and White, 2008). Manipulating plant Suc concentrations in vitro can be achieved by controlling photosynthesis or by application of exogenous carbohydrates. Addition of carbohydrates to the growth medium to simulate increased Suc supply to the root during P starvation has a marked effect on P starvation responses. Arabidopsis root growth and development is influenced greatly by the exogenous supply of Pi and Suc (Nacry et al., 2005; Karthikeyan et al., 2007). Interestingly, this effect was further enhanced by the addition of IAA to the growth medium. However, the presence of Suc in the growth medium appears to have no effect on controlling primary root length, suggesting that this P starvation response is regulated by local P availability or another signaling molecule. In white lupin (Lupinus albus), the formation of specialized cluster roots, used for scavenging P from discrete patches in the soil, increases with the exogenous supply of Suc, even at high levels of external P availability (Zhou et al., 2008b). The abundance of transcripts for some P-responsive genes also increases with the addition of Suc under P starvation compared with P-replete conditions (Fig. 2; Franco-Zorrilla et al., 2005; Liu et al., 2005; Karthikeyan et al., 2007; Müller et al., 2007; Zhou et al., 2008b). However, the abundance of transcripts for some P-responsive genes also appears to be enhanced by Suc under P-replete conditions, suggesting that two signaling pathways might be involved (Zhou et al., 2008b). Recently, the expression patterns of a P-deficient responsive gene, PvHAD1, and miR399 have been characterized in common bean using split-root and split-shoot systems (Liu et al., 2010b). The concept of the split-shoot system was to modify the photosynthate production on one side of the shoot by shading. Using these systems, it was observed that P-induced changes in the expression of PvHAD1 were controlled locally and were not dependent on miR399 expression. However, the P-induced expression of both PvHAD1 and miR399 was sensitive to photosynthate supply from the shoots, indicating that changes in photosynthate act upstream of miR399 in signaling plant responses to P availability and the presence of cross talk between carbon and P pools and signaling mechanisms in the plant (Liu et al., 2010b).

Sugars can act through various signaling pathways (Smeekens et al., 2010). Most evidence supports a direct signaling role for Suc in communicating plant responses to low P availability and little role for the involvement of hexokinase in communicating plant responses to low P availability (Hammond and White, 2008). Recently, the SnRK1 signaling pathway has been implicated in plant responses to low P availability (Fragoso et al., 2009). The activities of two catalytic subunits, AKIN10 and AKIN11, are differentially altered by P availability, with the activity of AKIN10 increasing under low P availability (Fragoso et al., 2009).

SUMMARY

Major advances have been made in our understanding of how plants sense, signal, and respond to soil P availability, through changes in the transcription of genes, the targeted degradation of transcripts and proteins, and changes in the concentrations and tissue sensitivities to plant growth regulators. There is now clear evidence for a role of shoot-derived carbohydrates in signaling plant root responses to low P availability. Further research into how fluxes in carbohydrates from the shoot to the root are effected and perceived by the plant to modulate plant responses to low P availability is now required to complete our understanding of how plants cope with low P availability.

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