Linking Development and Determinacy with Organic Acid Efflux from Proteoid Roots of White Lupin Grown with Low Phosphorus and Ambient or Elevated Atmospheric CO2 Concentration1

Watt, Michelle; Evans, John R.

doi:10.1104/pp.120.3.705

Cited by 208 publications

(186 citation statements)

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“…Here, we have established a novel mechanistic link between reversible in vivo PEPC phosphorylation and the concentrations of sucrose and its signalling molecule Tre6P (Yadav et al, 2014), while correlating this interesting phenomenon with the diurnal control of organic anion exudation and Pi uptake by CRs of ÀPi white lupin plants (Watt and Evans, 1999;Hocking and Jeffery, 2004;Liu et al, 2005;Cheng et al, 2014). It is notable that a direct relationship between Tre6P levels, anaplerotic carbon flux and PEPC's in vivo phosphorylation status was recently established in transgenic arabidopsis plants overexpressing Escherichia coli Tre6P synthase (Figueroa et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…Diurnal control of citrate exudation and Pi uptake by mature CRs of ÀPi lupin has also been reported; i.e. citrate release and Pi uptake were significantly reduced during darkness, then showed marked increases during the daytime (Watt and Evans, 1999;Hocking and Jeffery, 2004;Liu et al, 2005;Cheng et al, 2014). Transcriptional expression of various Pi-responsive genes in white lupin CRs (including that encoding the dominant PEPC isozyme LaPEPC3 (PEPC isozyme-3 from L. albus)) also increased in the light and decreased in the dark, suggesting that light-driven changes in the supply of photosynthate (sucrose) from the leaves to the CRs regulated expression of these genes in the latter (Liu et al, 2005;Cheng et al, 2011Cheng et al, , 2014.…”

Section: Introductionmentioning

confidence: 98%

“…2A); and (3) this developmental pattern largely parallels the relative abundance of 107-kDa immunoreactive PEPC polypeptides (Fig. 2B), as well as rates of organic acid anion exudation by CRs of illuminated plants (Johnson et al, 1996;Watt and Evans, 1999;Neumann et al, 2000).…”

Section: Cluster Root Pepc Of Illuminated White Lupin Plants Is Phospmentioning

confidence: 99%

“…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). This adaptive strategy is especially prevalent in highly specialized cluster (proteoid) roots (CRs), which mediate efficient Pi acquisition by certain plant species acclimating to soluble Pi-impoverished soils (Keerthisinghe et al, 1998;Neumann et al, 2000;Watt and Evans, 1999;Shane and Lambers, 2005;Cheng et al, 2011;Lambers et al, 2011). Of the various plants that form CRs, white lupin (Lupinus albus) stands out as an important agricultural crop, and is the species that has been most intensively investigated with respect to Pi nutrition (Cheng et al, 2011).…”

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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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

Section: Cluster Root Pepc Of Illuminated White Lupin Plants Is Phospmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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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“…This difference likely reflects differences in anatomical structure related directly to the number of primary xylem poles as described for Hakea prostrata (Proteaceae) and Lupinus albus (Fabaceae). The number of longitudinal rows of short lateral roots (rootlets) developed within each cluster root reflects the number of xylem poles, of which there are more in Hakea prostrata (6 to 8) than in Lupinus albus (2 poles) (Lamont 1982;Watt and Evans 1999;Shane and Lambers 2005a). Within the Proteaceae, a few genera also produce (alone or in combination with the simple type) a 'compound' type of cluster roots (Table 1, Protea sp.…”

Section: Introductionmentioning

confidence: 99%

Role of Root Clusters in Phosphorus Acquisition and Increasing Biological Diversity in Agriculture

Lambers¹,

Shane²

Scale and Complexity in Plant Systems Research

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Abstract. Soils in the south-west of Western Australia and South Africa are among the most phosphorusimpoverished in the world, and at the same time both of these regions are Global Biodiversity Hotspots. This unique combination offers an excellent opportunity to study root adaptations that are significant in phosphorus (P) acquisition. A large proportion of species from these P-poor environments cannot produce an association with mycorrhizal fungi, but, instead, produce 'root clusters'. In Western Australia, rootcluster-bearing Proteaceae occur on the most P-impoverished soils, whereas the mycorrhizal Myrtaceae tend to inhabit the less P-impoverished soils in this region. Root clusters are an adaptation both in structure and in functioning; characterized by high densities of short lateral roots that release large amounts of exudates, in particular carboxylates (anions of di-and tri-carboxylic acids). The functioning of root clusters in Proteaceae ('proteoid' roots) and Fabaceae ('cluster' roots) has received considerable attention, but that of 'dauciform' root clusters developed by species in Cyperaceae has barely been explored. Research on the physiology of 'capillaroid' root clusters formed by species in Restionaceae has yet to be published. Root-cluster initiation and growth in species of the Cyperaceae, Fabaceae and Proteaceae are systemically stimulated when plants are grown at a very low P supply, and are suppressed as leaf P concentrations increase. Root clusters in Proteaceae, Fabaceae and Cyperaceae are short-lived structures, which release large amounts of carboxylates, briefly, at a particular stage of root development. The rates of carboxylate release are considerably faster than reported for non-specialized roots of a wide range of species. Root clusters play a pivotal role in mobilization of P from P-sorbing soil. Because the world P reserves are being depleted whilst vast amounts of P are stored in fertilized soils, there is a growing need for crops with a high efficiency of P acquisition. Some Australian and African native species as well as some existing crops have traits that would be highly desirable for future crops. The possibilities of introducing P-acquisition-efficient species in new cropping and pasture systems are explored. In addition, possible strategies to introduce traits associated with a high P-acquisition efficiency into future crop species are discussed.

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The Role of the Rhizosphere in Nutrient Use Efficiency in Crops

Marschner

2011

The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops

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Linking Development and Determinacy with Organic Acid Efflux from Proteoid Roots of White Lupin Grown with Low Phosphorus and Ambient or Elevated Atmospheric CO2 Concentration1

Cited by 208 publications

References 44 publications

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

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

Role of Root Clusters in Phosphorus Acquisition and Increasing Biological Diversity in Agriculture

The Role of the Rhizosphere in Nutrient Use Efficiency in Crops

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