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.
Highlights
Nitrogen (N) is an essential plant nutrient and the most limiting factor for plant productivity and agricultural production worldwide
We provide evidence for the crucial role of active transport of high levels of S through the symbiosome membrane (SM) and its significant accumulation in the bacteroids, which is essential for nitrogenase biosynthesis
We found that the abundance of 34S was significantly (P ≤ 0.001) reduced, reaching only about 6 at% (i.e., ~2% higher than natural abundance) in the bacteroids of the mutant nodules (Figure 2e), confirming the importance of sulfate transport for Symbiotic nitrogen fixation (SNF)
Summary
Nitrogen (N) is an essential plant nutrient and the most limiting factor for plant productivity and agricultural production worldwide. KEYWORDS legume nodules, nanoSIMS, nitrogen fixation, stable isotope labelling, sulfur deficiency, symbiotic sulfate transporter (SST1)
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