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The Response of Carbon Metabolism and Antioxidant Defenses of Alfalfa Nodules to Drought Stress and to the Subsequent Recovery of Plants^1,2,[W],[OA]

Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas, 50080 Zaragoza, Spain (L.N., J.R., M.B.); Departamento de Ciencias del Medio Natural, Universidad Pública de Navarra, Campus de Arrosadía, 31006 Pamplona, Spain (R.L., E.M.G., C.A.-I.); and Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Dyfed SY23 3EB, United Kingdom (F.R.M.)

Alfalfa (Medicago sativa) plants were exposed to drought to examine the involvement of carbon metabolism and oxidative stress in the decline of nitrogenase (N₂ase) activity. Exposure of plants to a moderate drought (leaf water potential of –1.3 MPa) had no effect on sucrose (Suc) synthase (SS) activity, but caused inhibition of N₂ase activity (–43%), accumulation of succinate (+36%) and Suc (+58%), and up-regulation of genes encoding cytosolic CuZn-superoxide dismutase (SOD), plastid FeSOD, cytosolic glutathione reductase, and bacterial MnSOD and catalases B and C. Intensification of stress (–2.1 MPa) decreased N₂ase (–82%) and SS (–30%) activities and increased malate (+40%), succinate (+68%), and Suc (+435%). There was also up-regulation (mRNA) of cytosolic ascorbate peroxidase and down-regulation (mRNA) of SS, homoglutathione synthetase, and bacterial catalase A. Drought stress did not affect nifH mRNA level or leghemoglobin expression, but decreased MoFe- and Fe-proteins. Rewatering of plants led to a partial recovery of the activity (75%) and proteins (>64%) of N₂ase, a complete recovery of Suc, and a decrease of malate (–48%) relative to control. The increase in O₂ diffusion resistance, the decrease in N₂ase-linked respiration and N₂ase proteins, the accumulation of respiratory substrates and oxidized lipids and proteins, and the up-regulation of antioxidant genes reveal that bacteroids have their respiratory activity impaired and that oxidative stress occurs in nodules under drought conditions prior to any detectable effect on SS or leghemoglobin. We conclude that a limitation in metabolic capacity of bacteroids and oxidative damage of cellular components are contributing factors to the inhibition of N₂ase activity in alfalfa nodules.

² Dedicated to Dr. Frank R. Minchin on the occasion of his retirement.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Manuel Becana (becana{at}eead.csic.es).

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.107.099648

^* Corresponding author; e-mail becana{at}eead.csic.es; fax 34–976–716145.

Received March 15, 2007; accepted April 13, 2007; published April 27, 2007.

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