Mechanisms of physiological adjustment of N2 fixation in Cicer arietinum L. (chickpea) during early stages of water deficit: single or multi-factor controls

Plant J. 2014 Sep;79(6):964-80. doi: 10.1111/tpj.12599. Epub 2014 Jul 28.

Abstract

Drought negatively impacts symbiotic nitrogen fixation (SNF) in Cicer arietinum L. (chickpea), thereby limiting yield potential. Understanding how drought affects chickpea nodulation will enable the development of strategies to biotechnologically engineer chickpea varieties with enhanced SNF under drought conditions. By analyzing carbon and nitrogen metabolism, we studied the mechanisms of physiological adjustment of nitrogen fixation in chickpea plants nodulated with Mesorhizobium ciceri during both drought stress and subsequent recovery. The nitrogenase activity, levels of several key carbon (in nodules) and nitrogen (in both nodules and leaves) metabolites and antioxidant compounds, as well as the activity of related nodule enzymes were examined in M. ciceri-inoculated chickpea plants under early drought stress and subsequent recovery. Results indicated that drought reduced nitrogenase activity, and that this was associated with a reduced expression of the nifK gene. Furthermore, drought stress promoted an accumulation of amino acids, mainly asparagine in nodules (but not in leaves), and caused a cell redox imbalance in nodules. An accumulation of organic acids, especially malate, in nodules, which coincided with the decline of nodulated root respiration, was also observed under drought stress. Taken together, our findings indicate that reduced nitrogenase activity occurring at early stages of drought stress involves, at least, the inhibition of respiration, nitrogen accumulation and an imbalance in cell redox status in nodules. The results of this study demonstrate the potential that the genetic engineering-based improvement of SNF efficiency could be applied to reduce the impact of drought on the productivity of chickpea, and perhaps other legume crops.

Keywords: Mesorhizobium ciceri; carbon and nitrogen metabolism; chickpea; drought; feedback regulation; nitrogenase activity; oxidative stress.

MeSH terms

  • Carbon / metabolism*
  • Cell Respiration
  • Cicer / genetics
  • Cicer / microbiology
  • Cicer / physiology*
  • Droughts
  • Gene Expression Regulation, Plant*
  • Malates / metabolism
  • Mesorhizobium / physiology*
  • Models, Biological
  • Nitrogen / metabolism*
  • Nitrogen Fixation
  • Nitrogenase / genetics
  • Nitrogenase / metabolism
  • Oxidation-Reduction
  • Oxidative Stress
  • Plant Leaves / genetics
  • Plant Leaves / physiology
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Roots / genetics
  • Plant Roots / physiology
  • Root Nodules, Plant / genetics
  • Root Nodules, Plant / physiology
  • Symbiosis
  • Water / physiology*

Substances

  • Malates
  • Plant Proteins
  • Water
  • Carbon
  • malic acid
  • Nitrogenase
  • Nitrogen