Metabolic Reprogramming in Nodules, Roots, and Leaves of Symbiotic Soybean in Response to Iron Deficiency

Plant Cell Environ. 2019 Nov;42(11):3027-3043. doi: 10.1111/pce.13608. Epub 2019 Jul 29.

Abstract

To elucidate the mechanism of adaptation of leguminous plants to iron (Fe)-deficient environment, comprehensive analyses of soybean (Glycine max) plants (sampled at anthesis) were conducted under Fe-sufficient control and Fe-deficient treatment using metabolomic and physiological approach. Our results show that soybeans grown under Fe-deficient conditions showed lower nitrogen (N) fixation efficiency; however, ureides increased in different tissues, indicating potential N-feedback inhibition. N assimilation was inhibited as observed in the repressed amino acids biosynthesis and reduced proteins in roots and nodules. In Fe-deficient leaves, many amino acids increased, accompanied by the reduction of malate, fumarate, succinate, and α-ketoglutarate, which implies the N reprogramming was stimulated by the anaplerotic pathway. Accordingly, many organic acids increased in roots and nodules; however, enzymes involved in the related metabolic pathway (e.g., Krebs cycle) showed opposite activity between roots and nodules, indicative of different mechanisms. Sugars increased or maintained at constant level in different tissues under Fe deficiency, which probably relates to oxidative stress, cell wall damage, and feedback regulation. Increased ascorbate, nicotinate, raffinose, galactinol, and proline in different tissues possibly helped resist the oxidative stress induced by Fe deficiency. Overall, Fe deficiency induced the coordinated metabolic reprogramming in different tissues of symbiotic soybean plants.

Keywords: carbon and nitrogen metabolism; concerted metabolic change; feedback regulation; metabolome; organic acids; oxidative stress; soybean; symbiotic nitrogen fixation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / biosynthesis
  • Ammonium Compounds / metabolism
  • Chromatography, Gas
  • Iron / metabolism*
  • Lipid Peroxidation
  • Malondialdehyde / metabolism
  • Mass Spectrometry
  • Metabolome / genetics
  • Metabolome / physiology
  • Nitrogen / metabolism*
  • Nitrogen Fixation / genetics
  • Nitrogen Fixation / physiology
  • Nitrogenase / metabolism
  • Plant Leaves / chemistry
  • Plant Leaves / enzymology
  • Plant Leaves / metabolism*
  • Plant Roots / chemistry
  • Plant Roots / enzymology
  • Plant Roots / metabolism
  • Root Nodules, Plant / chemistry
  • Root Nodules, Plant / enzymology
  • Root Nodules, Plant / metabolism*
  • Soybeans / chemistry
  • Soybeans / metabolism*
  • Sugars / metabolism
  • Symbiosis

Substances

  • Amino Acids
  • Ammonium Compounds
  • Sugars
  • Malondialdehyde
  • Iron
  • Nitrogenase
  • Nitrogen