Abstract
Despite its agronomic importance, the metabolic networks mediating phosphorus (P) remobilization during plant senescence are poorly understood. Highly efficient P remobilization (~85%) from senescing leaves and proteoid roots of harsh hakea (Hakea prostrata), a native 'extremophile' plant of south-western Australia, was linked with striking up-regulation of cell wall-localized and intracellular acid phosphatase (APase) and RNase activities. Non-denaturing PAGE followed by in-gel APase activity staining revealed senescence-inducible 120kDa and 60kDa intracellular APase isoforms, whereas only the 120kDa isoform was detected in corresponding cell wall fractions. Kinetic and immunological properties of the 120kDa and 60kDa APases partially purified from senescing leaves indicated that they are purple acid phosphatases (PAPs). Results obtained with cell wall-targeted hydrolases of harsh hakea were corroborated using Arabidopsis thaliana in which an ~200% increase in cell wall APase activity during leaf senescence was paralleled by accumulation of immunoreactive 55kDa AtPAP26 polypeptides. Senescing leaves of an atpap26 T-DNA insertion mutant displayed a >90% decrease in cell wall APase activity. Previous research established that senescing leaves of atpap26 plants exhibited a similar reduction in intracellular (vacuolar) APase activity, while displaying markedly impaired P remobilization efficiency and delayed senescence. It is hypothesized that up-regulation and dual targeting of PAPs and RNases to the cell wall and vacuolar compartments make a crucial contribution to highly efficient P remobilization that dominates the P metabolism of senescing tissues of harsh hakea and Arabidopsis. To the best of the authors' knowledge, the apparent contribution of cell wall-targeted hydrolases to remobilizing key macronutrients such as P during senescence has not been previously suggested.
Highlights
Senescence is a tightly controlled developmental process involving the induction of senescence-associated genes that play key roles in protein, lipid, and nucleic acid breakdown and nutrient recycling (Thomas, 2013)
Results obtained with cell wall-targeted hydrolases of harsh hakea were corroborated using Arabidopsis thaliana in which an ~200% increase in cell wall acid phosphatase (APase) activity during leaf senescence was paralleled by accumulation of immunoreactive 55 kDa AtPAP26 polypeptides
The findings suggest that cell wall thickness, tissue longevity, and rate of senescence exert little influence on P remobilization efficiency between the functionally distinct, short-lived proteoid roots and relatively long-lived or short-lived Arabidopsis foliage (Fig. 1C)
Summary
Senescence is a tightly controlled developmental process involving the induction of senescence-associated genes that play key roles in protein, lipid, and nucleic acid breakdown and nutrient recycling (Thomas, 2013). Studies of the critical process of senescence-induced macromolecule catabolism together with remobilization of released nutrients to developing seeds and growing tissues have focused primarily on nitrogen rather than phosphorus (P) (Buchanan-Wollaston et al., Abbreviations: APase, acid phosphatase; P, phosphorus; PAP, purple acid phosphatase; PEP, phosphoenolpyruvate; Po, organic-P; PUE, P use efficiency; PVP, polyvinylpyrrolidone; PVPP, polyvinyl(polypyrrolidone). Even a small improvement in this capacity would probably lead to an important reduction in the use of non-renewable P-containing fertilizers in agriculture, reducing Pi run-off and pollution of aquatic ecosystems (Veneklaas et al, 2012)
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