PhysiologyLegume nodules from nutrient-poor soils exhibit high plasticity of cellular phosphorus recycling and conservation during variable phosphorus supply
Introduction
Phosphorus (P) is an essential nutrient for plant growth and a key structural constituent for nucleic acids, phospholipids, sugar phosphates and other catalytic cofactors, apart from the role it plays in metabolic regulation and energy transfer (Bosse and Köck, 1998). Plants thus depend heavily on P for plant growth and development, especially legume plants since P is required for biological nitrogen fixation (BNF) (Schulze et al., 1999) and has been reported to affect the energy costs of BNF (Valentine et al., 2010), as well as nodule formation and function (Israel, 1987). Soil P is however, limited and its availability is contingent on various factors such as diffusion rates in the soil and solubilisation of P containing compounds (Vance et al., 2003).
Plants have evolved an array of morphological and biochemical mechanisms to obtain adequate P or Pi (the metabolic form of P) under P deficient conditions (Vance et al., 2003, Tran et al., 2010). Morphological responses include transformed root architecture (Williamson et al., 2001), increasing root hair density and length which is common in legumes, and producing specialized roots known as proteoid roots for nutrient acquisition (Johnson et al., 1996, Neumann et al., 1999). Biochemical changes encompass increasing the abundance of Pi transport proteins and alternate enzymes to bypass Pi- or adenylate dependant reactions of glycolysis and mitochondrial respiration (Theodorou and Plaxton, 1993, Plaxton, 2004, Sieger et al., 2005, Tran et al., 2010). These alternate enzymes promote Pi recycling and the synthesis of organic acids, and Pi is a by-product of their reactions. P deficiency causes a decline in cytosolic Pi and adenylates (Rychter et al., 1992) and under these conditions the increased engagement of these alternative routes, eliminate the necessity for adenylates and Pi (Duff et al., 1989, Nagano et al., 1994).
Plants also increase their efficiency of Pi use during P deficiency by inducing phosphohydrolases such as ribonucleases (RNases) and acid phosphatases (APases) which scavenge Pi from P-esters (Raghothama, 1999, Tran et al., 2010, Hurley et al., 2010). APase activity has been used as a marker for P deficiency. APases release P (Miller et al., 2001) and have been implicated in the synthesis of glycolate and glycerate especially those associated with carbon metabolism (Duff et al., 1991, Vance et al., 2003). Extracellular APases cause the cessation of organic phosphate monoesters in the soil, while intracellular APases remobilize and scavenge Pi from internal sources (Duff et al., 1994, Marschner, 1995). Many organic P compounds occur in soil, with soil phytate (inositol hexaphosphates) forming a major component (around 25%), which could be hydrolyzed by APases or phytases. The latter represent a special group of phosphatases that are able to hydrolyze phytate to myo-inositol and phosphate (Richardson et al., 2000).
The correlation between P deficiency and BNF is not consistent among legumes, and nodular P metabolism is fairly understudied. In addition, many of the legume studies examining the effect of P deficiency on BNF focuses on model legumes (Tang et al., 2001, Le Roux et al., 2006, Schulze et al., 2006, Sulieman et al., 2013, Thuynsma et al., 2014). The P poor soils of the Cape Floristic Region (CFR) in South Africa has a high legume diversity (Goldblatt and Manning, 2002), yet not much is known about the functional adaptations they elicit with nutrient fluctuations.
The aim of this study was therefore to investigate the effects of P stress on BNF through response mechanisms of recycling and conservation inside the nodules of Virgilia divaricata (Adamson) (Fig. 1). This legume is native to the CFR and is distributed over a wide range of variably P poor soils, from relatively richer forest margins to poorer Fynbos soils (Coetsee and Wigley, 2013).
Section snippets
Seed germination, bacterial inoculation and growth
V. divaricata seeds (Silverhill Seeds, Kenilworth, South Africa) were germinated as described in Vardien et al. (2014). Following the initial leaf emergence (Fig. 1a), seedlings were transferred to and inoculated with a locally sourced strain of Burkholderia. Inoculum was prepared as previously documented (Vardien et al., 2014). Three treatment categories, based on P concentration, were used: low P, high P (control), and resupplied P (four weeks of low P followed by three weeks of high P). All
Plant growth and biomass
Total plant biomass accumulation was significantly reduced in P deficient plants compared to the control and previously starved plants that were supplied with sufficient P (Fig. 2) owing to decreased shoot, root and nodule growth (Fig. 2). Plants grown under P deficient conditions produced less than half the amount of nodules that was produced under P sufficient conditions but maintained a higher root: shoot ratio, a morphological response characteristic of low P exposure (Fig. 3).
Mineral nutrition and fixation efficiency
The
Discussion
During variable P supply, V. divaricata nodules display flexible internal P recycling and metabolism, which may prevent excessive changes in BNF during P deficiency and P resupply. This is the first report on the plasticity of the biochemical and physiological mechanisms of P recycling in legume nodules. The implications of these adaptations are discussed in relation to N acquisition during fluctuations in soil P concentration.
The decline in V. divaricata biomass during P deficiency and its
Acknowledgements
We express gratitude to DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) for funding and Anathi Magadlela for assistance with plant growth as well as in the laboratory.
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