Control of H2S synthesis by the monomer-oligomer transition of OsCBSX3 for modulating rice growth-immunity balance.

Hydrogen sulfide (H2S) is recognized as an important gaseous signaling molecule, similar to nitric oxide and carbon monoxide. However, the synthesis mechanism of H2S and its role in enhancing rice resistance to Xanthomonas oryzae pv. oryzicola (Xoc) and Xanthomonas oryzae pv. oryzae (Xoo) are less known. Our research identifies that H2S induces bursts of reactive oxygen species and upregulates defense-related genes in rice. However, excessive H2S concentrations inhibit rice growth. We further demonstrate that the cystathionine β-synthase, OsCBSX3, regulates rice growth and resistance to Xoc and Xoo by modulating H2S biosynthesis. OsCBSX3 exists in both oligomeric and monomeric forms in rice. Compared to the wild-type OsCBSX3, the oligomer-disrupting mutant exhibited a reduced capacity for H2S synthesis, diminished resistance to Xanthomonas oryzae, and an inability to localize to the chloroplast. Upon pathogen recognition, rice triggers PsbO-dependent oligomerization of OsCBSX3, leading to increased H2S production and enhanced defense responses. However, excessive concentrations of H2S reduce the oligomerized form of OsCBSX3, facilitating its dissociation from PsbO and its binding to OsTrxZ. OsTrxZ directly converts OsCBSX3 into monomers, thereby mitigating the excessive H2S synthesis and its negative effects on rice growth and development. OsTrxZ belongs to the thioredoxin family, and PsbO is an important subunit of photosystem II. Overexpression of PsbO enhances rice resistance to both Xoc and Xoo, whereas overexpression of OsTrxZ exerts the opposite effect. These findings suggest that PsbO and OsTrxZ antagonistically modulate the conversion between oligomeric and monomeric forms of OsCBSX3, thereby balancing rice resistance and developmental processes.