Sulfate is transported at significant rates through the symbiosome membrane and is crucial for nitrogenase biosynthesis

Plant Cell Environ. 2019 Apr;42(4):1180-1189. doi: 10.1111/pce.13481. Epub 2019 Jan 28.

Abstract

Legume-rhizobia symbioses play a major role in food production for an ever growing human population. In this symbiosis, dinitrogen is reduced ("fixed") to ammonia by the rhizobial nitrogenase enzyme complex and is secreted to the plant host cells, whereas dicarboxylic acids derived from photosynthetically produced sucrose are transported into the symbiosomes and serve as respiratory substrates for the bacteroids. The symbiosome membrane contains high levels of SST1 protein, a sulfate transporter. Sulfate is an essential nutrient for all living organisms, but its importance for symbiotic nitrogen fixation and nodule metabolism has long been underestimated. Using chemical imaging, we demonstrate that the bacteroids take up 20-fold more sulfate than the nodule host cells. Furthermore, we show that nitrogenase biosynthesis relies on high levels of imported sulfate, making sulfur as essential as carbon for the regulation and functioning of symbiotic nitrogen fixation. Our findings thus establish the importance of sulfate and its active transport for the plant-microbe interaction that is most relevant for agriculture and soil fertility.

Keywords: legume nodules; nanoSIMS; nitrogen fixation; stable isotope labelling; sulfur deficiency; symbiotic sulfate transporter (SST1).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Gas Chromatography-Mass Spectrometry
  • Lotus / metabolism
  • Membrane Transport Proteins / metabolism*
  • Microscopy, Electron, Transmission
  • Nitrogenase / biosynthesis*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Rhizobiaceae / metabolism
  • Root Nodules, Plant / metabolism
  • Root Nodules, Plant / ultrastructure
  • Sulfates / metabolism*
  • Symbiosis

Substances

  • Membrane Transport Proteins
  • Sulfates
  • Nitrogenase