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Update on Phosphate Stress in Legumes

Genomic and Genetic Control of Phosphate Stress in Legumes¹

United States Department of Agriculture Agricultural Research Service (M.T., C.P.V.), Department of Agronomy and Plant Genetics (J.L., C.P.V.), and Department of Soil, Water, and Climate (D.L.A.), University of Minnesota, St. Paul, Minnesota 55108

Phosphorus (P), an essential element for growth and development, is taken up by plants as phosphate (Pi), but Pi is unevenly distributed and relatively immobile in soils. As a result, more than 30% of the world's arable land requires the application of P fertilizers for cropping (Vance et al., 2003). Unfortunately, P fertilizers are manufactured from nonrenewable resources that are increasingly becoming more costly and less available. Current estimates indicate that easily mined rock Pi reserves could easily be depleted by 2060 (Steen, 1997; Vance, 2001; Vance et al., 2003). Paradoxically, part of the applied P in intensive cropping systems can enter the waterways through runoff and erosion, contributing to pollution of surrounding lakes and marine environments. Improving P acquisition and use by crops is critical to economical and environmentally friendly crop agriculture.

Plants have evolved a variety of adaptive strategies to improve their acquisition, use, and remobilization of P (Vance et al., 2003; Hammond et al., 2004; Lambers et al., 2006). Plant responses to P stress conditions involve changes in root morphology and architecture (Lynch, 1995; Liao et al., 2001; Lynch and Brown, 2001; Yan et al., 2004; Beebe et al., 2006; Hill et al., 2006; Ochoa et al., 2006), as well as changes in shoot and flower development (Bucciarelli et al., 2006). Among the legumes, white lupine (Lupinus albus), common bean (Phaseolus vulgaris), and to a lesser extent barrel medic (Medicago truncatula) and soybean (Glycine max) have been the focus of P stress research. White lupine, a nonmycorrhizal species, is adaptable to scarce P and displays a highly synchronous suite of molecular and biochemical adaptations to P stress by developing proteoid (cluster) roots, increasing organic acid exudation, and enhancing the expression of many genes, such as secreted acid phosphatase (LaSAP1) and Pi transporters (LaPT1; Vance, 2001; Uhde-Stone et al., 2003a, 2003b; Vance et al., 2003, and refs. therein). Common bean is the most important food legume worldwide, and genetic variability for the capacity to produce grain in low soil P conditions has been documented (Broughton et al., 2003; Ochoa et al., 2006). Moreover, several thousand ESTs derived from P-stressed common bean roots have been characterized (Ramírez et al., 2005). Noteworthy in an accompanying article in this legume focus issue, Hernández et al. (2007) have completed a P stress root transcriptome survey in common bean, identifying some 125 genes responsive to P stress. Recent studies of barrel medic, a model legume for plant biology research, showed that P stress delayed: (1) leaf development and leaf expansion along the main and axillary shoots; (2) axillary shoot emergence and elongation, resulting in stunted plants; and (3) timing and frequency of flower emergence (Bucciarelli et al., 2006). P-stressed barrel medic also formed shorter petioles and shorter blade lengths relative to plants in P-sufficient conditions. Whether or not morphological changes seen in P-starved barrel medic plants are attributable to an overall delay in whole plant development or as a P stress response remains to be seen. However, the lack of a standardized approach to describe plant growth and phenotypic responses to P stress (Bucciarelli et al., 2006), together with the plastic nature of plant morphological traits (Beebe et al., 2006; Ochoa et al., 2006), makes result comparisons from different laboratories difficult.

Because of the subterranean nature of growth, plant roots have been recalcitrant to phenotypic study. Root adaptations to P limitations include reduced extension of primary roots, highly branched roots with increased lateral roots, and an increased density of root hair formation. Consistent with a general stress response by plants, however, P-stressed plants tend to allocate a greater proportion of biomass to root dry matter compared to P-sufficient plants (López-Bucio et al., 2002, 2003; Hammond et al., 2004; Hill et al., 2006). Most pasture species studied showed reduced total root mass as a response to P stress conditions. On average, a 32% to 86% reduction in root mass was observed in most pasture species with decreasing P concentrations (Hill et al., 2006). Owing to inherent root architecture differences, some pasture species did not respond with root mass reduction to P stress (Hill et al., 2006). Similarly, there were no root architecture differences between barrel medic plants grown under P-sufficient and P-deficient conditions until 28 d after planting, when lateral root length and number of P-limited plants showed a decline (Bucciarelli et al., 2006). By contrast, alfalfa (Medicago sativa) roots show changes in architecture when grown under P stress. Genetic regulation of root architecture changes due to P stress within and among species is not understood and offers a fruitful area of emphasis for future research.

Molecular genetic, biochemical, physiological, and morphological responses of plants subjected to P stress have been the subject of many recent reviews (Vance, 2001; López-Bucio et al., 2003; Vance et al., 2003; Franco-Zorrilla et al., 2004; Hammond et al., 2004; Raghothama and Karthikeyan, 2005; Lambers et al., 2006). This Update summarizes the ongoing plant biology research toward the understanding of P stress in legumes such as white lupine, common bean, barrel medic, and soybean. Additional studies using model plant systems such as Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa) have also provided valuable genomic and genetic evidence in understanding plant responses and adaptations to P limitations (Hammond et al., 2003; Yi et al., 2005; Aung et al., 2006; Bari et al., 2006; Müller et al., 2007).

	QUANTITATIVE TRAIT LOCI ASSOCIATED WITH ROOT ARCHITECTURE FOR P STRESS TOLERANCE AND ADAPTATION

TOP QUANTITATIVE TRAIT LOCI... P STRESS-INDUCED ESTS P STRESS-RESPONSIVE... P STRESS-RESPONSIVE MICRORNAS SUGARS MODULATE THE EXPRESSION... PHYTOHORMONES AND P STRESS... ARBUSCULAR MYCORRHIZAL SYMBIOSES CONCLUDING REMARKS LITERATURE CITED

 
Genetic variability with contrasting degree of root architecture responses to P-limiting conditions has been known for a wide range of plant species (Chevalier et al., 2003; Rubio et al., 2003; Yan et al., 2004). Lynch (1995) has noted a direct correlation between plant productivity and root architecture. As a result, P stress tolerance and adaptation have begun to be analyzed in common bean and Arabidopsis through the identification of quantitative trait loci (QTL) approach (Beebe et al., 2006; Ochoa et al., 2006; Reymond et al., 2006). Ochoa et al. (2006) generated recombinant inbred lines (RIL) from a cross of two common bean accessions with contrasting root architecture traits for adventitious roots. Screening 86 F_5:7 RIL under P stress and P-sufficient conditions resulted in the identification of 19 QTLs for adventitious root formation (Ochoa et al., 2006). Because Pi availability is expected to be greater in topsoil compared to subsoil, selection for root trait QTL markers associated with adventitious rooting and topsoil foraging may enhance P acquisition. In a previous study, QTL analysis applied to RIL of a cross of G19833 and DOR 364 common beans showed that root hair formation and root organic acid exudation are important traits for marker-assisted selection and breeding of P stress tolerance and adaptation (Yan et al., 2004). Common bean G19833 is a landrace of the Andean gene pool with superior growth and yield in P stress conditions, and DOR 364 is a Mesoamerican gene pool with low P accumulation efficiency in P-limiting conditions. Recently, a composite interval mapping approach identified 26 more QTLs associated with basal root development and greater P acquisition efficiency in P stress conditions (Beebe et al., 2006). In a recent study involving a RIL population of Arabidopsis, three QTLs involved in root growth response to P stress were identified (Reymond et al., 2006). One of the QTLs, LPR1, explained 52% of the variation associated with primary root length response. QTL analysis of P stress tolerance appears to be a useful approach in determining which root traits are associated with P uptake. With the soon-to-be-completed sequencing of the genomes of Medicago and Lotus accompanied by the strikingly conserved synteny among legume genomes, using positional cloning, it should be possible to identify specific genes that contribute to QTLs affecting adaptation to P stress. The selection and development of P-efficient legume plants using QTL markers would not only be beneficial to low-input agricultural systems but also would enhance environmentally friendly cropping in intensively cultivated systems.

	P STRESS-INDUCED ESTS

TOP QUANTITATIVE TRAIT LOCI... P STRESS-INDUCED ESTS P STRESS-RESPONSIVE... P STRESS-RESPONSIVE MICRORNAS SUGARS MODULATE THE EXPRESSION... PHYTOHORMONES AND P STRESS... ARBUSCULAR MYCORRHIZAL SYMBIOSES CONCLUDING REMARKS LITERATURE CITED

 
Following international collaborations in recent years, more than 25,000 partially sequenced cDNA inserts or ESTs derived from P-starved tissues of four legume species (barrel medic, soybean, common bean, and white lupine) are currently deposited in the public domain (http://compbio.dfci.harvard.edu/tgi/). Microarray and macroarray analysis of P stress in plants showed increased transcript abundance of genes with homology to Pi transporters, organic acid synthesis, purple acid phosphatase, mulitdrug and toxin efflux (MATE), transcription factors, signaling, and defense (Hammond et al., 2003; Uhde-Stone et al., 2003a, 2003b; Wu et al., 2003; Misson et al., 2005; Ramírez et al., 2005; Müller et al., 2007). Gene indices at http://compbio.dfci.harvard.edu/tgi/ derived from EST sequencing efforts of P-stressed tissues have been used as tools for gene discovery, molecular marker generation, and gene transcript pattern analysis. By evaluating available microarray and macroarray data and utilizing bioinformatic analysis of publicly available EST sequencing projects, Graham et al. (2006) identified 52 candidate genes clustered in 22 groups that appear to respond in common to P stress in four legume species and Arabidopsis. This in silico analysis identified P stress-responsive genes that are overrepresented in the gene indices. Transcripts identified annotate to various important functional categories, including MYB and WRKY transcription factors, signal transduction proteins (Ser/Thr kinases, mitogen-activated protein kinases, and calcium-dependent protein kinases), transporters (Pi transporter and ATP-binding cassette transporter family), and purple acid phosphatases. Current research is aimed at: (1) using P stress-induced ESTs in marker-assisted selection for genotypes having improved tolerance to P deficiency; (2) characterizing the functional significance of P stress-induced genes; and (3) identifying candidate genes that may be used to enhance P efficiency.

	P STRESS-RESPONSIVE TRANSCRIPTION FACTORS IN LEGUMES

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Research in Arabidopsis and rice suggests that an important step in regulation of gene expression during plant stress appears to be the transcriptional activation or repression of genes (Chen et al., 2002; Wu et al., 2003). Transcription factors are key global regulators of gene expression and are known to play critical roles in many biological processes, including the regulation of plant responses to numerous biotic and abiotic stresses (Rubio et al., 2001; Tang et al., 2001; Chen et al., 2002; Singh et al., 2002). In Arabidopsis alone, approximately 6% (about 1,800) of the total number of genes are composed of transcription factors, including about 72 WRKY family of genes, more than 600 zinc finger proteins, and 133 MYB transcription factors (Eulgem et al., 2000; Riechmann et al., 2000; Stracke et al., 2001; Guo et al., 2005). In a microarray analysis, approximately 30% of the 333 transcription factor genes included in the array were up- or down-regulated 2-fold or more during P stress in Arabidopsis (Wu et al., 2003). Misson et al. (2005) and Müller et al. (2007) also reported up to 80 P stress-responsive transcription factor genes in Arabidopsis. P stress-responsive transcription factors belong to several families, including MYB, SCARECROW, APETALA2 domain, homeobox, WRKY, and zinc fingers. A recent bioinformatic analysis of legume gene indices (Medicago, Glycine, Phaseolus, and Lupinus) queried for genes overrepresented in P-stressed tissue revealed the annotation of several putative transcription factor genes, including WRKY, MYB, and zinc finger family of genes (Graham et al., 2006). Furthermore, leaves and root tissues showed nonoverlapping sets of transcription factor genes (Wu et al., 2003). In addition, distinct sets of genes that may function as early- and late-responsive genes during P stress were observed (Hammond et al., 2003; Misson et al., 2005).

bHLH Transcription Factors

Recently, a bHLH transcription factor involved in Pi stress in rice (OsPTF1) was cloned and characterized (Yi et al., 2005). Normally, OsPTF1 is constitutively expressed in shoots, but transcript accumulation was induced in roots during P starvation of rice plants (Yi et al., 2005). Under P-limiting conditions, overexpression of OsPTF1 in transgenic rice using the constitutive cauliflower mosaic virus 35S promoter resulted in increased P uptake compared to untransformed rice (Yi et al., 2005). Transgenic rice also displayed longer total root length and larger root surface area, resulting in a 30% higher root and shoot biomass than untransformed rice (Yi et al., 2005). An OsPTF1 gene promoter fused to GUS reporter gene showed strong GUS staining in lateral roots, primary root elongation zone, and leaves of transgenic rice in P-limited conditions (Yi et al., 2005).

HD-Zip and MYB Family of Transcription Factors

Two other transcription factors involved in signaling P-responsive gene expression include the homeodomain Leu zipper (HD-ZIP) protein in soybean (Tang et al., 2001) and the MYB transcription factor in Arabidopsis (Rubio et al., 2001). Although the HD-ZIP protein binds to the sequence 5'-CATTAATTAG-3' present in vacuolar glycoprotein acid phosphatases (Tang et al., 2001), the Arabidopsis MYB transcription factor with sequence homology to a Pi starvation response (PHR1) gene in Chlamydomonas reinhardtii was shown to bind to an imperfect palindromic consensus sequence, 5'-GNATATNC-3' (Rubio et al., 2001). Although transcript abundance of PHR1 gene was not greatly influenced by Pi status (Rubio et al., 2001), a recent report indicated that PHR1 defines a Pi-signaling network in Arabidopsis (Bari et al., 2006). There is limited experimental evidence on the regulation of P stress-responsive genes in legumes. However, we and others have observed the PHR1 imperfect palindromic consensus sequence motif within the 5'-upstream region of many P stress-induced genes, including the white lupine LaPT1 and LaSAP1 (Liu et al., 2001; Miller et al., 2001; Hammond et al., 2003; Müller et al., 2007). Also noteworthy is that contigs encoding orthologs of PHR1 occur in the common bean, Medicago, and soybean gene indices.

Zinc Finger Family of Transcription Factors

The Phaseolus gene index at The Institute for Genomic Research contains 12 ESTs that show homology to zinc finger transcription factor. These P-responsive ESTs were clustered in two tentative consensus sequences (TC564 and TC1862) and eight singletons derived from P stress roots. Using semiquantitative reverse transcription-PCR analysis of 13 ESTs encoding zinc finger transcription factors, we observed increased transcript abundance for two of the ESTs in P-starved roots of common bean (R. Schirmer and C. Vance, unpublished data). The functional importance of P-responsive zinc finger transcription factors remains to be established.

The WRKY Superfamily of Transcription Factors

Another group of transcription factors among the publicly available EST sequences of P-stressed tissues of white lupine, common bean, soybean, and barrel medic showed homology to the WRKY family of genes. This family of genes, defined by a DNA-binding domain that contains the strictly conserved amino acid sequence WRKY, appears to be unique to plants (Eulgem et al., 2000). Upon binding to their cognate W-box binding motif (C/T)TGAC(C/T), members of this family of genes have been shown to be up-regulated in response to a diverse set of stresses, including infection by pathogens and wounding, as well as during senescence (Eulgem et al., 2000). In Arabidopsis microarray analysis, a transcription factor WRKY75 gene was found to be up-regulated during Pi starvation (Misson et al., 2005). A recent study by Devaiah et al. (2007) demonstrated that WRKY75 is a nuclear localized, Pi-responsive transcription factor gene in Arabidopsis. However, RNAi-silenced WRKY75 mutants showed increased lateral root numbers and length and root hair number in both Pi-limited and P-sufficient conditions, indicating that the regulatory effect on root architecture may not be related to P stress. Preliminary observations in our laboratory have found that transcript abundance of selected WRKY genes could be either up-regulated or down-regulated in P-limited root tissues of common bean (Fig. 1 ). In addition, a recombinant WRKY protein derived from a common bean WRKY gene binds to the 5'-upstream promoter of P stress-induced genes from several species (J. Liu and C. Vance, unpublished data). Given the complexity of the WRKY family of transcription factors, these findings were in agreement with suggestions by others that the WRKY family of genes may act as both transcriptional activators and repressors and that their binding sites may differ from the consensus W-box. Many plant genes that respond to P stress contain WRKY boxes in the 5'-upstream regions. Inclusively, there is a wide array of transcription factors involved in modulating gene expression in P-stressed plants. More than likely, regulation of transcription in P stress will result from cross talk between transcription factors. Although significant advances have been made in understanding transcriptional regulation during P stress, much work remains to define the complex interactions involved in transducing P cascade events. The challenge for plant biologists is to identify putative downstream targets for P-responsive transcription factors and determine whether they can be manipulated to improve P tolerance in plants, as suggested by overexpression of the OsPTF1 gene in rice.

View larger version (53K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 1. P-regulated expression of the WRKY family of transcription factor genes in common bean roots. For RNA blots, 15 µg of total RNA was isolated from roots of 3-week-old plants grown under P-sufficient (+P) or P-deficient (–P) conditions as described previously (Ramírez et al., 2005).

	P STRESS-RESPONSIVE MICRORNAS

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Putative miRNA399 and UBC homologs have been computationally identified in barrel medic and Lotus (Sunkar and Zhu, 2004; Bari et al., 2006). A potential binding site for miRNA164 has been predicted for the transcription factor NAC1 gene (Rhoades et al., 2002), and we have noted NAC1 EST in white lupine P-stressed proteoid root expression libraries (P. Smith, C. Atkins, and C. Vance, unpublished data). We also have observed up-regulated expression of a NO APICAL MERISTEM gene (a NAC gene family) in P-starved roots of barrel medic and alfalfa (M. Tesfaye and C. Vance, unpublished data). NAC1 gene transduces auxin signals for lateral root development by activating the expression of two downstream auxin-responsive genes, DBP and AIR3, in Arabidopsis (Xie et al., 2000). It remains to be seen if miRNA399, miRNA164, or other plant miRNAs play a significant role in the regulation of P-responsive genes in legumes. The P stress response of plants is often considered to be a systemic event, and it will be informative to ascertain whether miRNAs are the effectors of such systemic responses.

	SUGARS MODULATE THE EXPRESSION OF P STRESS-RESPONSIVE GENES

TOP QUANTITATIVE TRAIT LOCI... P STRESS-INDUCED ESTS P STRESS-RESPONSIVE... P STRESS-RESPONSIVE MICRORNAS SUGARS MODULATE THE EXPRESSION... PHYTOHORMONES AND P STRESS... ARBUSCULAR MYCORRHIZAL SYMBIOSES CONCLUDING REMARKS LITERATURE CITED

 
Our laboratory and others have shown that increased transcript abundance of several genes coincides with P starvation in white lupine and Medicago. Transcript accumulation of white lupine LaPT1, MATE, and LaSAP1 genes was increased in stems and in normal and cluster roots of P-stressed plants, although there was virtually no transcript accumulation of these genes in P-sufficient plants (Liu et al., 2001, 2005; Uhde-Stone et al., 2005). The direct involvement of LaPT1, MATE, and LaSAP1 genes in P starvation has been verified by studies using transgenic lupine and alfalfa plants that contained the promoters and 5'-untranslated intron fused to a reporter GUS gene (Liu et al., 2005; Uhde-Stone et al., 2005). Roots of transgenic alfalfa plants grown under P limitation showed strong GUS staining and enzyme activity. Similar to wild-type P-sufficient alfalfa and lupine plants, no GUS staining was visible in root segments of transgenic plants grown in P-sufficient medium. Other abiotic stress treatments, such as nitrogen (N) starvation, aluminum toxicity, or addition of naphthylacetic acid, did not produce GUS staining or show reporter gene enzyme activity in transgenic plants containing LaPT1 and LaSAP1 genes. However, the expression of the MATE gene was not unique to P stress, as increased transcript accumulation of MATE in proteoid roots was shown during aluminum phytotoxicity as well as in iron, N, and manganese stress conditions (Uhde-Stone et al., 2005).

In white lupine, LaPT1 transcripts are readily detectable at 5 d after germination of plants grown at 16 h of light and 8 h of darkness in a 24-h cycle. However, dark-grown white lupine seedlings showed considerably reduced transcript accumulation of the Pi transporter gene, indicating the importance of light in P metabolism. Sugars, apart from being metabolites, are also recognized as signal molecules in plants. Research in lupine and Arabidopsis revealed that Pi and sugars are integrally related to P deficiency-induced expression of Pi transporter genes (Liu et al., 2005; Karthikeyan et al., 2006). Exogenous application of Suc induced the accumulation of Pi transporter genes in dark-grown and P-sufficient seedlings. Stem-girdling studies in white lupine have also revealed that photosynthates/sugars play a role in mediating increased expression of Pi-responsive genes under Pi deficiency conditions (Liu et al., 2005). Expression of P stress-induced LaPT1, LaSAP1, and LaMATE in cluster roots was reduced in girdled plants. Moreover, when P-stressed plants grown in a 16-/8-h photoperiod were placed in the dark for 24 h, P stress-induced gene expression in roots was abolished but recovered upon 16-h reexposure to light (Liu et al., 2005). To further investigate the relationship between P stress and photosynthates in proteoid roots, we recently evaluated transcript abundance of selected sugar sensing and metabolism genes, including hexokinase, Suc synthase, fructokinase, PPi-dependent phosphofructokinase-1, and trehalose-6-P synthase under dark and light conditions in P-starved white lupine plants. Expression of these genes was enhanced greater than 2-fold in P stress-induced cluster roots of white lupine (Uhde-Stone et al., 2003a). Results in Figure 2 show that the expression of sugar-sensing and metabolism genes was repressed in P-deficient proteoid roots of white lupine after 48 h of continuous dark conditions. Expression of these genes recovered in P-starved proteoid roots of white lupine when dark-treated plants were returned to full light or when leaves were partially exposed to light for 48 h (Fig. 2). These data show a direct cross talk between sugar metabolism and P stress.

View larger version (77K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 2. Pi stress and light affect expression of sugar-related genes in proteoid roots of white lupine. Total RNA isolated from proteoid roots of P-deficient white lupine plants at 14 d after emergence under different light regimes. Treatments: D/D2, plants shaded in continuous dark for 48 h; D/L48, dark-treated plants reexposed to continuous light for 48 h; D/L48ss, one-half of the shoot of dark-grown plants reexposed to light and the other one-half remaining in the dark. SucSyn, Suc synthase; HXK1, hexokinase; FK, fructokinase; PPi-PFK, PPi-dependent phosphofructokinase-1; TPS, trehalose-6-P synthase; Ub, polyubiquitin. Growth conditions were described previously (Liu et al., 2005).

	PHYTOHORMONES AND P STRESS ADAPTATION

TOP QUANTITATIVE TRAIT LOCI... P STRESS-INDUCED ESTS P STRESS-RESPONSIVE... P STRESS-RESPONSIVE MICRORNAS SUGARS MODULATE THE EXPRESSION... PHYTOHORMONES AND P STRESS... ARBUSCULAR MYCORRHIZAL SYMBIOSES CONCLUDING REMARKS LITERATURE CITED

 
The plant hormone auxin (principally indole-3-acetic acid [IAA]) has been implicated in the regulation of many aspects of plant growth and root development, including P stress-induced proteoid (cluster) root development (Gilbert et al., 2000). Nacry et al. (2005) showed that during Pi starvation, IAA concentration increases in the whole primary root and in young lateral roots of Arabidopsis. Without IAA, only primary root growth was observed in Arabidopsis (Karthikeyan et al., 2006). Regardless of Pi status and/or Suc availability, exogenous application of auxin enhanced lateral root formation and suppressed primary root elongation in Arabidopsis (López-Bucio et al., 2002; Karthikeyan et al., 2006). The effect of IAA on lateral root formation was striking under P-sufficient conditions that did not contain Suc (Karthikeyan et al., 2006). Furthermore, exogenous application of auxin to P-sufficient white lupine mimics proteoid cluster root formation as seen under P-deficient conditions (Gilbert et al., 2000). Auxin transport inhibitors added to P-deficient plants dramatically reduced the formation of cluster roots. The data strongly suggest that cluster root development in response to P deficiency in white lupine is controlled by auxin availability.

In Arabidopsis, a NAC1 gene is expressed at high levels in root tips and lateral root initiation sites and at low levels in stems and leaves (Xie et al., 2000). Arabidopsis plants expressing antisense NAC1 showed reduced lateral root emergence, and the lateral root stimulation effect of auxin treatment could not be observed in roots of NAC1-silenced transgenic plants (Xie et al., 2000). Ectopic expression of NAC1 cDNA in transgenic Arabidopsis coincided with increased AIR3 and DBP gene expression and promoted the production of lateral roots (Xie et al., 2000). Evidence suggested that auxin and NAC1 gene expression could have synergistic effects on lateral root initiation in Arabidopsis. Exogenously applied auxin resulted in significantly more lateral roots formed in NAC1 overexpressing plants than wild-type plants. It remains to be seen if the NAC1 gene has a similar role in root architecture traits associated with P stress adaptations in plants.

P deficiency stress is known to stimulate ethylene production in many plant species, including bean (Borch et al., 1999), lupine (Gilbert et al., 2000), and Arabidopsis (Ma et al., 2003). Ethylene regulates the rate of root elongation in both bean and Arabidopsis. Under P deficiency stress, ethylene application maintains primary and lateral root elongation but does not affect lateral root density. Interestingly, P deficiency can restore lateral root density to Arabidopsis ethylene-insensitive mutants. Root hair formation appears to be regulated, in part, by ethylene. Stimulation of ethylene production results in an increase in root hair density and length (Grierson et al., 2001; López-Bucio et al., 2003). It is noteworthy that bean, lupine, and barrel medic plants exposed to P stress have increased density and length of root hairs. Some 40 genes are suggested to be involved in root hair development (Grierson et al., 2001). Graham et al. (2006) reported that a key gene, 1-aminocyclopropane-1-carboxylic acid oxidase, in ethylene biosynthesis is overrepresented in the ESTs derived from P-stressed roots of lupine, bean, and Medicago. These results taken together indicate that ethylene production and/or plant responsiveness to ethylene plays a role in root adaptation to P deficiency.

The role of cytokinins in root growth and P deficiency stress is not resolved. Traditionally, cytokinins are thought to be negative regulators of root growth while having positive effects on shoot growth (Werner et al., 2003; Aloni et al., 2006). Application of cytokinin inhibits root development and abolishes the auxin effect of increased lateral root development. Plants that overexpress the cytokinin oxidase (CKX) genes have reduced cytokinin content and show enhanced root growth due to more lateral and adventitious root formation (Lohar et al., 2004). Both P and N deficiency result in decreased cytokinin content (López-Bucio et al., 2003), accompanied by increased lateral root formation. Exogenously applied cytokinin represses the expression of P stress-induced genes in Arabidopsis roots (Martin et al., 2000). In P-stressed lupine proteoid roots, CKX gene expression showed a 3- to 5-fold increase in expression (Vance et al., 2003). Moreover, application of cytokinin to P-deficient white lupine inhibits proteoid root formation, and kinetin content is increased in proteoid roots (Neumann et al., 2000). Aloni et al., (2006) have proposed a mechanism for lateral root initiation in P-sufficient plants that involves the interaction of auxin, cytokinin, and ethylene. They propose that factors that modulate root tip cytokinin production allow ethylene and auxin to increase at lateral root initiation sites, giving rise to new laterals. This hypothesis would be consistent with the effect that low P has on inhibition of primary root tip growth, thereby reducing or releasing cytokinin-dependent root apical dominance accompanied by increased lateral root formation. It is fairly obvious that changes in phytohormone balance modulate root developmental plasticity in response to nutrient stress. However, the overriding question remains: How do plants integrate P stress signaling, phytohormone balance, and gene induction to achieve plasticity?

	ARBUSCULAR MYCORRHIZAL SYMBIOSES

TOP QUANTITATIVE TRAIT LOCI... P STRESS-INDUCED ESTS P STRESS-RESPONSIVE... P STRESS-RESPONSIVE MICRORNAS SUGARS MODULATE THE EXPRESSION... PHYTOHORMONES AND P STRESS... ARBUSCULAR MYCORRHIZAL SYMBIOSES CONCLUDING REMARKS LITERATURE CITED

 
Mycorrhizal symbioses, which evolved with land plants more than 400 million years ago, are the most important adaptation for plants to acquire scarce P (Parniske, 2004; Harrison, 2005; Oldroyd et al., 2005). More than 80% of angiosperm plants have mycorrhizal symbioses. A major rationale for developing barrel medic, L. japonicus, and soybean as model species is due to the fact that they have symbiotic associations with arbuscular mycorrhizae (AM) fungi and rhizobial bacteria. Similar to legume-rhizobial symbiosis, the legume-AM symbiosis results from elegant signal exchanges between the fungus and host plant (Harrison, 2005; Requena et al., 2007). The legume releases compounds in root exudates that stimulate fungal growth, hyphal branching, and appressoria formation (Akiyama et al., 2005). After infection, plant signals are thought to stimulate arbuscule formation in root cortical cells. The AM fungus stimulates root growth and branching. AM fungal hyphae extend from roots into the soil profile, allowing the symbiosis to mine P and other nutrients for plant growth, while the plant provides the fungus with carbon. The exchange of nutrients and carbon between the symbionts occurs within root cortical cells in which elaborate multilobed-fungal structures called arbuscules develop. The plant cytosol and fungal arbuscule never come into contact with each other due to their separation by the periarbuscular membrane, which is an extension of the cortical cell plasmalemma. As evidenced by this brief description, legume-AM symbiosis is an exquisite, highly regulated interaction between the legume host and AM fungi, requiring coordinated expression of genes from two vastly different organisms. A complete review of AM symbiosis is beyond the scope of this article, and the reader is referred to several excellent recent reviews (Parniske, 2004; Harrison, 2005; Oldroyd et al., 2005; Krajinski and Frenzel, 2007; Kuster et al., 2007; Requena et al., 2007). Herein only salient features of genomic studies of legume-AM symbioses will be addressed.

In recent years, several genetic loci in legumes that affect rhizobial root nodule and AM symbioses have been characterized through positional cloning. Although these loci were defined initially as root nodulation mutants, they also limit AM infection (Parniske, 2004; Harrison, 2005; Oldroyd et al., 2005). Genetic loci identified to date impairing AM symbiosis and nodulation include: a Leu-rich, receptor-like kinase (dmi2, LjSYM2, PsSYM19); a ligand gated ion channel (dmi1); and a calcium-calmodulin dependent kinase (dmi3, PsSYM9/30). Interestingly, orthologs of these loci have been recently identified in nonlegume species (Zhu et al., 2006). Moreover, two proteins with similarity to dmi1, designated CASTOR and POLLUX, and plastid targeted in L. japonicus have been shown to be required for symbiosis (Imaizumi-Anraku et al., 2005). Several other genetic loci affecting AM symbiosis have been identified in various legumes, but they await full characterization (Kistner et al., 2005). Without doubt, however, we now know that AM and root nodule symbioses share some common signaling pathways. In addition, there is a backlog of loci that require attention to fully understand legume control of AM symbiosis.

Using macroarray, microarray, and in silico analyses of EST databases, a large number (at least 200) of plant genes have been identified that respond to AM fungal inoculation and infection (Journet et al., 2002; Liu et al., 2003; Wulf et al., 2003; Grunwald et al., 2004; Liu et al., 2004; Manthey et al., 2004; Hohnjec et al., 2005; Kuster et al., 2007). Several gene families were identified repeatedly as being highly expressed during AM symbiosis, including: lectins; PR proteins; glutathione S-transferases; sugar; and transporters; MYB and zinc finger proteins; Cys proteinases; annexins; metalothionines; and membrane intrinsic proteins. Although the functional significance of most of the proteins induced in legume roots in response to AM symbiosis has not been defined, current approaches utilizing RNAi, TILLING, and insertional mutagenesis will allow functional significance to be tested. For example, the transporter genes LjPT3 from L. japonicus (Maeda et al., 2006) and MtPT4 from barrel medic (Javot et al., 2007) were shown via RNAi and/or TILLING mutants to be required for effective AM symbiosis. Similarly, a calcium-dependent protein kinase that mediates root development in barrel medic was shown to impact AM symbiosis (Ivashuta et al., 2005). These functional analyses represent only the tip of the iceberg. As more genes responding to AM are characterized, the ultimate aim would be to identify genetic strategies that regulate AM symbioses and P acquisition.

	CONCLUDING REMARKS

TOP QUANTITATIVE TRAIT LOCI... P STRESS-INDUCED ESTS P STRESS-RESPONSIVE... P STRESS-RESPONSIVE MICRORNAS SUGARS MODULATE THE EXPRESSION... PHYTOHORMONES AND P STRESS... ARBUSCULAR MYCORRHIZAL SYMBIOSES CONCLUDING REMARKS LITERATURE CITED

 
P is second to N as the most limiting element for plant growth. With the availability of a wide array of genomic and bioinformatic research platforms, P stress research is moving toward an exciting phase centered around signal transduction, regulation of developmental plasticity, gene function, and increased efficiency of use. Sustainable cropping practices require that plant researchers identify and discover mechanisms in plants that improve P acquisition and exploit these P stress adaptations to make better plants that are efficient at acquiring Pi. Efforts that improve soil P availability to plants contribute greatly to the practice of economical and environmentally friendly crop agriculture.

Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers CV543965, CV542870, CV543085, CV542465, CV543813, CV543844, and CV543732 (WRKY1–7, respectively); CA410415 (SucSyn); CA410267 (HXK1); CA410623 (FK); CA409542 (PPi-PFK); and CA410467 (TPS).

	ACKNOWLEDGMENTS

 
We thank Sue Miller, Melinda Dornbusch, Rebecca Schirmer, Renee Schirmer, and Bruna Bucciarelli for technical assistance. This work is a joint contribution from the Plant Science Research Unit, USDA-ARS, and the Minnesota Agricultural Experimental Station. Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the USDA, and does not imply its approval or the exclusion of other products and vendors that might also be suitable.

Received February 1, 2007; accepted April 10, 2007; published June 6, 2007.

	FOOTNOTES

 
¹ This work was supported by the U.S. Department of Agriculture Agricultural Research Service (CRIS no. 3640–21000–024–00D, "Functional Genomics for Improving Nutrient Acquisition and Use in Legumes") and by a U.S. Department of Agriculture Agricultural Research Service/University of Minnesota specific cooperative agreement (no. 58–3640–4–107, "Lupinus, Phaseolus and Medicago Genomics of Plant Nutrition").

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Carroll P. Vance (vance004{at}umn.edu).

www.plantphysiol.org/cgi/doi/10.1104/pp.107.097386

^* Corresponding author; e-mail vance004{at}umn.edu; fax 651–649–5058.

	LITERATURE CITED

TOP QUANTITATIVE TRAIT LOCI... P STRESS-INDUCED ESTS P STRESS-RESPONSIVE... P STRESS-RESPONSIVE MICRORNAS SUGARS MODULATE THE EXPRESSION... PHYTOHORMONES AND P STRESS... ARBUSCULAR MYCORRHIZAL SYMBIOSES CONCLUDING REMARKS LITERATURE CITED

 
Akiyama K, Matsuzaki K-I, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824–827[CrossRef][Medline]

Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot (Lond) 97: 883–893[Abstract/Free Full Text]

Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) Pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141: 1000–1011[Abstract/Free Full Text]

Bari R, Pant BD, Stitt M, Scheible WR (2006) Pho2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141: 988–999[Abstract/Free Full Text]

Bartel B, Bartel DP (2004) Micro RNAs: at the root of plant development. Plant Physiol 132: 709–717[Web of Science]

Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116: 281–297[CrossRef][Web of Science][Medline]

Beebe SE, Rojas-Pierce M, Yan X, Blair MW, Pedraza F, Muñoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci 46: 413–423[Abstract/Free Full Text]

Borch K, Bouma TJ, Lynch JP, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22: 425–431[CrossRef]

Broughton WJ, Hernández G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.): model food legumes. Plant Soil 252: 55–128[CrossRef][Web of Science]

Bucciarelli B, Hanan J, Palmquist D, Vance CP (2006) A standardized method for analysis of Medicago truncatula phenotype development. Plant Physiol 142: 207–219[Abstract/Free Full Text]

Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang H-S, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, et al (2002) Expression profile matrix of Arabidopsis transcription factor genes suggest their putative function in response to environmental stresses. Plant Cell 14: 559–574[Abstract/Free Full Text]

Chen Z, Zhang J, Kong J, Li S, Fu Y, Li S, Zhang H, Li Y, Zhu Y (2006) Diversity of endogenous small non-coding RNAs in Oryza sativa. Genetica 128: 21–31[CrossRef][Web of Science][Medline]

Chevalier F, Pata M, Nacry P, Douma P, Rossignol M (2003) Effects of phosphate availability on the root system architecture: large-scale analysis of the natural variation between Arabidopsis accessions. Plant Cell Environ 26: 1839–1850[CrossRef]

Chiou TJ, Aung K, Lin SL, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18: 412–421[Abstract/Free Full Text]

Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator by phosphate acquisition and root development in Arabidopsis. Plant Physiol 143: 1789–1801[Abstract/Free Full Text]

Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199–206[CrossRef][Web of Science][Medline]

Franco-Zorrilla JM, González E, Bustos R, Linhares F, Leyva A, Paz-Ares J (2004) The transcriptional control of plant responses to phosphate limitation. J Exp Bot 55: 285–293[Abstract/Free Full Text]

Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15: 2038–2043[CrossRef][Web of Science][Medline]

Gilbert GA, Knight JD, Vance CP, Allan DL (2000) Proteoid root development of phosphorus-deficient lupin is mimicked by auxin and phosphonate. Ann Bot (Lond) 85: 921–928[Abstract/Free Full Text]

Graham MA, Ramirez M, Valdes-López O, Lara M, Tesfaye M, Vance CP, Hernandez G (2006) Identification of candidate phosphorus stress induced genes in Phaseolus vulgaris through clustering analysis across several plant species. Funct Plant Biol 33: 789–797[CrossRef]

Grierson CS, Parker JS, Kemp AC (2001) Arabidopsis genes with roles in root hair development. J Plant Nutr Soil Sci 164: 131–140[CrossRef]

Grunwald U, Nyamsuren O, Tamasloukht M-B, Lapopin L, Becker A, Mann P, Gianinazzi-Pearson V, Krajinski F, Franken P (2004) Identification of mycorrhiza-regulated genes with arbuscule development-related expression profile. Plant Mol Biol 55: 553–566[CrossRef][Web of Science][Medline]

Guo A, He K, Liu D, Bai S, Gu X, Wei L, Luo J (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21: 2568–2569[Abstract/Free Full Text]

Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132: 578–596[Abstract/Free Full Text]

Hammond JP, Broadly MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot (Lond) 94: 323–332[Abstract/Free Full Text]

Harrison M (2005) Signaling on the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59: 19–42[CrossRef][Web of Science][Medline]

Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, et al (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144: 752–767

Hill JO, Simpson RJ, Moore AD, Chapman DF (2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant Soil 286: 7–19[CrossRef][Web of Science]

Hohnjec N, Vieweg MF, Puhler A, Becker A, Kuster H (2005) Overlaps in the transcriptional profile of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137: 1283–1301[Abstract/Free Full Text]

Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, et al (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plants. Nature 433: 527–531[CrossRef][Medline]

Ivashuta S, Liu J, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17: 2911–2921[Abstract/Free Full Text]

Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104: 1720–1725[Abstract/Free Full Text]

Jones-Rhodes MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787–799[CrossRef][Web of Science][Medline]

Journet E-P, vanTuinen D, Gouzy J, Crespeau H, Carreau V, Farmer M-J, Niebel A, Schiex T, Jaillon O, Chatagnier O, et al (2002) Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res 30: 5579–5592[Abstract/Free Full Text]

Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2006) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta doi/10.1007/s00425-006-0408-8

Kistner C, Winzer T, Pitschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ, et al (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17: 2217–2229[Abstract/Free Full Text]

Krajinski F, Frenzel A (2007) Towards the elucidation of AM-specific transcription in Medicago truncatula. Phytochemistry 68: 75–81[CrossRef][Web of Science][Medline]

Kuster H, Vieweg MF, Manthey K, Baier MC, Hohnjec N, Perlick AM (2007) Identification and expression of symbiotically activated legume genes. Phytochemistry 68: 8–18[CrossRef][Web of Science][Medline]

Lambers HY, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot (Lond) 98: 693–713[Abstract/Free Full Text]

Liao H, Rubio G, Yan X, Cao A, Brown KM, Lynch JP (2001) Effect of phosphorus availability on basal root shallowness in common bean. Plant Soil 232: 69–79[CrossRef][Web of Science][Medline]

Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveal genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15: 2106–2123[Abstract/Free Full Text]

Liu J, Blaylock LA, Harrison MJ (2004) cDNA arrays as tools to identify mycorrhiza-regulated genes: identification of mycorrhiza-induced genes that encode or generate signaling molecules implicated in control of root growth. Can J Bot 82: 1175–1185

Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41: 257–268[CrossRef][Web of Science][Medline]

Liu J, Uhde-Stone C, Li A, Vance C, Allan D (2001) A phosphate transporter with enhanced expression in proteoid roots of white lupin (Lupinus albus L.). Plant Soil 237: 257–266[CrossRef][Web of Science]

Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J 38: 203–214[CrossRef][Web of Science][Medline]

López-Bucio J, Cruiz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280–287[CrossRef][Web of Science][Medline]

López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129: 244–256[Abstract/Free Full Text]

Lynch JP (1995) Root architecture and plant productivity. Plant Physiol 109: 7–13[CrossRef][Web of Science][Medline]

Lynch JP, Brown KM (2001) Topsoil foraging: an architectural adaptation of plants to low phosphorus availability. Plant Soil 237: 225–237[CrossRef][Web of Science]

Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131: 1381–1390[Abstract/Free Full Text]

Maeda D, Ashida K, Iguchi K, Chechetka SA, Hijikata A, Okusako Y, Deguchi Y, Izui K, Hata S (2006) Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol 47: 807–817[Abstract/Free Full Text]

Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Puhler A, Perlick AM, Kuster H (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant Microbe Interact 17: 1063–1077[CrossRef][Web of Science][Medline]

Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de la Pena A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24: 559–567[CrossRef][Web of Science][Medline]

Miller SS, Liu JQ, Allan DL, Menzhuber CJ, Fedorova M, Vance CP (2001) Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin. Plant Physiol 127: 594–606[Abstract/Free Full Text]

Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, et al (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102: 11934–11939[Abstract/Free Full Text]

Müller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143: 156–171[Abstract/Free Full Text]

Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138: 2061–2074[Abstract/Free Full Text]

Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Romheld V, Martinoia E (2000) Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Ann Bot (Lond) 85: 909–919[Abstract/Free Full Text]

Ochoa IE, Blair MW, Lynch JP (2006) QTL analysis of adventitious root formation in common bean under contrasting phosphorus availability. Crop Sci 46: 1609–1621[Abstract/Free Full Text]

Oldroyd GED, Harrison MJ, Udvardi M (2005) Peace talks and trade deals. Keys to long-term harmony in legume microbe symbioses. Plant Physiol 137: 1205–1210[Free Full Text]

Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7: 414–421[CrossRef][Web of Science][Medline]

Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274: 37–49[CrossRef][Web of Science]

Ramírez M, Graham MA, Blanco-López L, Silvente S, Medrano-Soto A, Blair MW, Hernández G, Vance CP, Lara M (2005) Sequencing and analysis of common bean ESTs. Building a foundation for functional genomics. Plant Physiol 137: 1211–1227[Abstract/Free Full Text]

Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16: 1616–1626[Abstract/Free Full Text]

Requena N, Serrano E, Ocón A, Breuninger M (2007) Plant signals and fungal perception during arbuscular mycorrhizae establishment. Phytochemistry 68: 33–40[CrossRef][Web of Science][Medline]

Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T (2006) Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ 29: 115–125[CrossRef][Medline]

Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110: 513–520[CrossRef][Web of Science][Medline]

Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratclifffe OJ, Samaha RR, et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105–2110[Abstract/Free Full Text]

Rubio G, Liao H, Yan X, Lynch JP (2003) Topsoil foraging and its role in plant competitiveness for phosphorus in common bean. Crop Sci 43: 598–607[Abstract/Free Full Text]

Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15: 2122–2133[Abstract/Free Full Text]

Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5: 430–436[CrossRef][Web of Science][Medline]

Steen I (1997) Phosphorus availability in the 21st century. Management of a non-renewable resource. Phosphorus and Potassium 217: 25–31

Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447–456[CrossRef][Web of Science][Medline]

Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001–2019[Abstract/Free Full Text]

Tang Z, Sadka A, Morishige DT, Mullet JE (2001) Homeodomain leucine zipper proteins bind to the phosphate response domain of the soybean VspB tripartite promoter. Plant Physiol 125: 797–809[Abstract/Free Full Text]

Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003a) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248: 99–116[CrossRef][Web of Science]

Uhde-Stone C, Liu J, Zinn KE, Allan DL, Vance CP (2005) Transgenic proteoid roots of white lupin: a vehicle for characterizing and silencing root genes involved in adaptation to P stress. Plant J 44: 840–853[CrossRef][Web of Science][Medline]

Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL (2003b) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131: 1064–1079[Abstract/Free Full Text]

Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition: plant nutrition in a world of declining renewable resources. Plant Physiol 127: 390–397[Free Full Text]

Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157: 423–447[CrossRef][Web of Science]

Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15: 2532–2550[Abstract/Free Full Text]

Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW (2003) Phosphate starvation triggers distinct alternations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132: 1260–1271[Abstract/Free Full Text]

Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Kuster H, Krajinski F (2003) Transcriptional changes to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol Plant Microbe Interact 16: 306–314[Web of Science][Medline]

Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14: 3024–3036[Abstract/Free Full Text]

Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138: 2145–2154[Abstract/Free Full Text]

Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265: 17–29[CrossRef][Web of Science]

Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P (2005) OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138: 2087–2096[Abstract/Free Full Text]

Zhu H, Riely BK, Burns NJ, Ane J-M (2006) Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses. Genetics 172: 2491–2499[Abstract/Free Full Text]

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