Metabolic Adaptations of Phosphate-Starved Plants

Plaxton, William C.; Tran, Hue T.

doi:10.1104/pp.111.175281

Cited by 516 publications

(464 citation statements)

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“…Among other features reminiscent of Pi limitation stress in plants, the PM fraction of NM roots showed enhanced abundances of sulfite exporter, glycerol-3-phosphate transporter, and phosphoenolpyruvate carboxylase (PEPC) (Calderon-Vazquez et al 2008;Lan et al 2012;Kang et al 2014). Increased levels of PEPC in Pi-limited plants has been linked to enhanced synthesis and excretion of organic acids that increase Pi concentration in the soil solution (reviewed in Plaxton and Tran 2011). Interestingly, a decrease in phospholipid levels in phosphatestarved roots has been correlated with an increase in permeability of root membranes (Ratnayake et al 1978).…”

Section: Am-responsive Proteins As Related To Interface Biogenesis Anmentioning

confidence: 99%

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

Aloui¹,

Recorbet²,

Lemaître‐Guillier³

et al. 2017

Mycorrhiza

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In arbuscular mycorrhizal (AM) roots, the plasma membrane (PM) of the host plant is involved in all developmental stages of the symbiotic interaction, from initial recognition to intracellular accommodation of intra-radical hyphae and arbuscules. Although the role of the PM as the agent for cellular morphogenesis and nutrient exchange is especially accentuated in endosymbiosis, very little is known regarding the PM protein composition of mycorrhizal roots. To obtain a global overview at the proteome level of the host PM proteins as modified by symbiosis, we performed a comparative protein profiling of PM fractions from Medicago truncatula roots either inoculated or not with the AM fungus Rhizophagus irregularis. PM proteins were isolated from root microsomes using an optimized discontinuous sucrose gradient; their subsequent analysis by liquid chromatography followed by mass spectrometry (MS) identified 674 proteins. Cross-species sequence homology searches combined with MS-based quantification clearly confirmed enrichment in PM-associated proteins and depletion of major microsomal contaminants. Changes in protein amounts between the PM proteomes of mycorrhizal and non-mycorrhizal roots were monitored further by spectral counting. This workflow identified a set of 82 mycorrhiza-responsive proteins that provided insights into the plant PM response to mycorrhizal symbiosis. Among them, the association of one third of the mycorrhiza-responsive proteins with detergent-resistant membranes pointed at partitioning to PM microdomains. The PM-associated proteins responsive to mycorrhization also supported host plant control of sugar uptake to limit fungal colonization, and lipid turnover events in the PM fraction of symbiotic roots. Because of the depletion upon symbiosis of proteins mediating the replacement of phospholipids by phosphorus-free lipids in the plasmalemma, we propose a role of phosphate nutrition in the PM composition of mycorrhizal roots.

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Section: Am-responsive Proteins As Related To Interface Biogenesis Anmentioning

confidence: 99%

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

Aloui¹,

Recorbet²,

Lemaître‐Guillier³

et al. 2017

Mycorrhiza

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“…The upregulation of PEPC during Pi starvation has also been linked to the synthesis and exudation of large quantities of organic acid anions (e.g. malate, citrate) by roots of various ÀPi plants (Neumann et al, 2000;Vance et al, 2003;Shane and Lambers, 2005;Plaxton and Tran, 2011;Cheng et al, 2011;Lambers et al, 2011). This greatly increases root Pi acquisition by solubilizing otherwise inaccessible sources of mineralized soil Pi, thus increasing soluble Pi concentrations by up to 1000-fold (Vance et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

“…Activation of the PEPC isozyme AtPPC1 by in vivo phosphorylation in response to Pi deprivation of the model plant arabidopsis (Arabidopsis thaliana) has been well documented (Gregory et al, 2009). AtPPCK1 and AtPPCK2 are amongst the most strongly Pi-starvation-inducible genes of arabidopsis (Gregory et al, 2009;Plaxton and Tran, 2011), and Pi deprivation of arabidopsis cell cultures caused a striking 3-fold enhancement of in vivo flux through the PEPC reaction (Masakapalli et al, 2014). This provides a metabolic bypass with malate dehydrogenase (MDH) and NAD-malic enzyme to cytosolic pyruvate kinase (which is substrate (ADP)-limited in low-Pi plants) to facilitate continued pyruvate supply to the mitochondrial tricarboxylic acid cycle (Duff et al, 1989;Masakapalli et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Phosphorylation by a dedicated Ca 2þ -independent PEPC protein kinase (PPCK) at a conserved N-terminal seryl residue activates PEPC in many plant tissues by relieving its allosteric inhibition by malate while enhancing activation by glucose-6-phosphate (O'Leary et al, 2011). Amongst its numerous and diverse physiological functions, PEPC plays a critical role during plant acclimation to nutritional Pi deprivation, a common abiotic stress that frequently limits plant growth in natural ecosystems (Vance et al, 2003;Plaxton and Tran, 2011). Activation of the PEPC isozyme AtPPC1 by in vivo phosphorylation in response to Pi deprivation of the model plant arabidopsis (Arabidopsis thaliana) has been well documented (Gregory et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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Light-dependent activation of phosphoenolpyruvate carboxylase by reversible phosphorylation in cluster roots of white lupin plants: diurnal control in response to photosynthate supply

Shane

Feil

Lunn

et al. 2016

Ann Bot

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Background and Aims Phosphoenolpyruvate carboxylase (PEPC) is a tightly regulated enzyme that controls carbohydrate partitioning to organic acid anions (malate, citrate) excreted in copious amounts by cluster roots of inorganic phosphate (Pi)-deprived white lupin plants. Excreted malate and citrate solubilize otherwise inaccessible sources of mineralized soil Pi for plant uptake. The aim of this study was to test the hypotheses that (1) PEPC is post-translationally activated by reversible phosphorylation in cluster roots of illuminated white lupin plants, and (2) light-dependent phosphorylation of cluster root PEPC is associated with elevated intracellular levels of sucrose and its signalling metabolite, trehalose-6-phosphate.Methods White lupin plants were cultivated hydroponically at low Pi levels ( 1 mM) and subjected to various light/ dark pretreatments. Cluster root PEPC activity and in vivo phosphorylation status were analysed to assess the enzyme's diurnal, post-translational control in response to light and dark. Levels of various metabolites, including sucrose and trehalose-6-phosphate, were also quantified in cluster root extracts using enzymatic and spectrometric methods.Key Results During the daytime the cluster root PEPC was activated by phosphorylation at its conserved Nterminal seryl residue. Darkness triggered a progressive reduction in PEPC phosphorylation to undetectable levels, and this was correlated with 75-80 % decreases in concentrations of sucrose and trehalose-6-phosphate.Conclusions Reversible, light-dependent regulatory PEPC phosphorylation occurs in cluster roots of Pi-deprived white lupin plants. This likely facilitates the well-documented light-and sucrose-dependent exudation of Pi-solubilizing organic acid anions by the cluster roots. PEPC's in vivo phosphorylation status appears to be modulated by sucrose translocated from CO 2 -fixing leaves into the non-photosynthetic cluster roots.

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“…Plant adaptation to low soil P availability consists of several physiological mechanisms and morphological characteristics (Tesfaye et al, 2007;Plaxton & Tran, 2011). Common bean genotypes better adapted to limited P supply have exhibited larger root systems (Yan et al, 1995), a branched root system with numerous basal roots (Lynch & van Beem, 1993), and changes in the gravitropic response of basal roots, resulting in a shallower root system to forage surface soil horizons (Bonser et al, 1996;Ge at al., 2000).…”

Section: Introducionmentioning

confidence: 99%

Variability of root traits in common bean genotypes at different levels of phosphorus supply and ontogenetic stages

Trindade

Araújo

2014

Rev. Bras. Ciênc. Solo

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SUMMARYSelection of common bean (Phaseolus vulgaris L.) cultivars with enhanced root growth would be a strategy for increasing P uptake and grain yield in tropical soils, but the strong plasticity of root traits may compromise their inclusion in breeding programs. The aim of this study was to evaluate the magnitude of the genotypic variability of root traits in common bean plants at two ontogenetic stages and two soil P levels. Twenty-four common bean genotypes, comprising the four growth habits that exist in the species and two wild genotypes, were grown in 4 kg pots at two levels of applied P (20 and 80 mg kg -1 ) and harvested at the stages of pod setting and early pod filling. Root area and root length were measured by digital image analysis. Significant genotype × P level and genotype × harvest interactions in analysis of variance indicate that the genotypic variation of root traits depended on soil nutrient availability and the stage at which evaluation was made. Genotypes differed for taproot mass, basal and lateral root mass, root area and root length at both P levels and growth stages; differences in specific root area and length were small. Genotypes with growth habits II (upright indeterminate) and III (prostrate indeterminate) showed better adaptation to limited P supply than genotypes of groups I (determinate) and IV (indeterminate climbing). Between the two harvests, genotypes of groups II and III increased the mass of basal and lateral roots by 40 and 50 %, respectively, whereas genotypes of groups I and IV by only 7 and 19 %. Values of the genotypic coefficient of determination, which estimates the proportion of phenotypic variance resulting from genetic effects, were higher at early pod filling than at pod setting. Correlations between shoot mass and root mass, which could indicate indirect selection of root systems via aboveground biomass, were higher at early pod filling than at pod setting. The results indicate that selection for root traits in common bean genotypes should preferentially be performed at the early pod-filling stage.Index terms: growth habit, Phaseolus vulgaris, phosphorus efficiency, root system.

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Metabolic Adaptations of Phosphate-Starved Plants

Cited by 516 publications

References 47 publications

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

Light-dependent activation of phosphoenolpyruvate carboxylase by reversible phosphorylation in cluster roots of white lupin plants: diurnal control in response to photosynthate supply

Variability of root traits in common bean genotypes at different levels of phosphorus supply and ontogenetic stages

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