Sulfur Transport and Metabolism in Legume Root Nodules

Abstract

Sulfur is an essential nutrient in plants as a constituent element of some amino acids, metal cofactors, coenzymes, and secondary metabolites. Not surprisingly, sulfur deficiency decreases plant growth, photosynthesis, and seed yield in both legumes and non-legumes. In nodulated legumes, sulfur supply is positively linked to symbiotic nitrogen fixation (SNF) and sulfur starvation causes three additional major effects: decrease of nodulation, inhibition of SNF, and slowing down of nodule metabolism. These effects are due, at least in part, to the impairment of nitrogenase biosynthesis and activity, the accumulation of nitrogen-rich amino acids, and the decline in leghemoglobin, ferredoxin, ATP, and glucose in nodules. During the last decade, some major advances have been made about the uptake and metabolism of sulfur in nodules. These include the identification of the sulfate transporter SST1 in the symbiosomal membrane, the finding that glutathione produced in the bacteroids and host cells is essential for nodule activity, and the demonstration that sulfur assimilation in the whole plant is reprogrammed during symbiosis. However, many crucial questions still remain and some examples follow. In the first place, it is of paramount importance to elucidate the mechanism by which sulfur deficiency limits SNF. It is unknown why homoglutahione replaces glutathione as a major water-soluble antioxidant, redox buffer, and sulfur reservoir, among other relevant functions, only in certain legumes and also in different tissues of the same legume species. Much more work is required to identify oxidative post-translational modifications entailing cysteine and methionine residues and to determine how these modifications affect protein function and metabolism in nodules. Likewise, most interactions of antioxidant metabolites and enzymes bearing redox-active sulfur with transcription factors need to be defined. Solving these questions will pave the way to decipher sulfur-dependent mechanisms that regulate SNF, thereby gaining a deep insight into how nodulated legumes adapt to the fluctuating availability of nutrients in the soil.

Keywords: (homo)glutathione; bacteroids; cysteine; legume nodules; sulfur metabolism; symbiosis.

FIGURE 1

Sulfur deficiency negatively affects the performance of nodulated legumes. The scheme depicts four major general effects in interaction, as well as some specific biochemical features that may, at least in part, account for such effects. Information was gathered from studies by Anderson and Spencer (1950), DeBoer and Duke (1982), Zhao et al. (1999), Scherer (2008), and Varin et al. (2010).

FIGURE 2

Schematics of sulfur metabolism in legume nodules. In the cytosol, some common reactions affecting the thiol group of Cys residues of proteins (P) are indicated. These include sulfenylation (P-SOH), sulfinylation (P-SO₂H), sulfonylation (P-SO₃H), persulfidation (P-S-SH), S-nitrosylation (P-SNO), glutathionylation (P-S-S-G, where G is a glutathione molecule linked to a protein Cys residue through its thiol group), and formation of mixed disulfides (P-S-S-P’, where P and P’ may be identical or different proteins). Note that sulfenylation, glutathionylation, and formation of mixed disulfide are reversible, whereas sulfinylation may be irreversible and sulfonylation is irreversible. For simplicity, we omit reactions such as Cys synthesis that may also occur in the mitochondria. Abbreviations are as indicated in Table 1. Cyst, cystathionine; (h)GSSG, (homo)glutathione disulfide; HCys, homocysteine; MetSO, methionine sulfoxide; OAcSer, O-acetylserine.