Roots and nodules response differently to P starvation in the Mediterranean-type legume Virgilia divaricata

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Authors

Stevens, Gary G.
Perez-Fernandez, María A.
Morcillo, Rafael J.L.
Kleinert, Aleysia
Hills, Paul
Brand, D. Jacobus
Steenkamp, Emma Theodora
Valentine, Alex J.

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Frontiers Media

Abstract

Virgilia divaricata is a tree legume that grows in the Cape Floristic Region (CFA) in poor nutrient soils. A comparison between high and low phosphate growth conditions between roots and nodules was conducted and evaluated for the plants ability to cope under low phosphate stress conditions in V. divaricata. We proved that the plant copes with low phosphate stress through an increased allocation of resources, reliance on BNF and enhanced enzyme activity, especially PEPC. Nodules had a lower percentage decline in P compared to roots to uphold its metabolic functions. These strategies partly explain how V. divaricata can sustain growth despite LP conditions. Although the number of nodules declined with LP, their biomass remained unchanged in spite of a plant decline in dry weight. This is achieved via the high efficiency of BNF under P stress. During LP, nodules had a lower % decline at 34% compared to the roots at 88%. We attribute this behavior to P conservation strategies in LP nodules that imply an increase in a metabolic bypass that operates at the PEP branch point in glycolysis. The enhanced activities of nodule PEPC, MDH, and ME, whilst PK declines, suggests that under LP conditions an adenylate bypass was in operation either to synthesize more organic acids or to mediate pyruvate via a non-adenylate requiring metabolic route. Both possibilities represent a P-stress adaptation route and this is the first report of its kind for legume trees that are indigenous to low P, acid soils. Although BNF declined by a small percentage during LP, this P conservation was evident in the unchanged BNF efficiency per weight, and the increase in BNF efficiency per mol of P. It appears that legumes that are indigenous to acid soils, may be able to continue their reliance on BNF via increased allocation to nodules and also due to increase their efficiency for BNF on a P basis, owing to P-saving mechanisms such as the organic acid routes.

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Figure S1 : A section of the 13C spectra for (a) roots after 1 h, (b) roots after 2 h grown under high phosphate (500 mM P) conditions of V. divaricata.
Figure S2 : A section of the 13C spectra of (a) roots after 1 h, (b) roots after 2 h grown under low phosphate (5 mM P) conditions of V. divaricata.
Figure S3 : A section of the 13C spectra of (a) nodules after 1 h, (b) nodules after 2 h grown under high phosphate (500 mM P) conditions of V. divaricata.
Figure S4 :| A section of the 13C spectra of (a) nodules after 1 h, (b) nodules after 2 h grown under low phosphate (5 mM P) conditions of V. divaricata.
Figure S5 : A sample of the full 13C spectra of roots after 1 h, from plants grown under high phosphate (500 mM P) conditions of V. divaricata.
Figure S6 : A sample of the full 13C spectra of nodules after 1 h, from plants grown under high phosphate (500 mM P) conditions of V. divaricata.
This work is based on the Ph.D. thesis (University of Stellenbosch) of one of the authors, Gary Grant Stevens (GGS).

Keywords

Legumes, Nodules, Low P, High P allocation of resources, Conservation strategies, Phosphoenolpyruvate carboxylase, Phosphate stress, Virgilia divaricata, Tree legume, Biological nitrogen fixation (BNF), Phosphatase and phosphoenolpyruvate carboxylase (PEPC), Malate dehidrogenase (MDH), Mitochondrial malic enzyme (ME)

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Citation

Stevens GG, Pérez-Fernández MA, Morcillo RJL, Kleinert A, Hills P, Brand DJ, Steenkamp ET and Valentine AJ (2019) Roots and Nodules Response Differently to P Starvation in the Mediterranean-Type Legume Virgilia divaricata. Frontiers in Plant Science 10:73. DOI: 10.3389/fpls.2019.00073.