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

Abstract

Hydrogen sulfide (H₂S) is recognized as an important gaseous signaling molecule, similar to nitric oxide and carbon monoxide. However, less is known about the biosynthetic mechanism of H₂S in plants and its role in plant-pathogen interactions. Here, we show that H₂S induces the bursts of reactive oxygen species and upregulates the expression of defense-related genes in rice. However, excessive H₂S concentrations inhibit rice growth. We found that the cystathionine β-synthase OsCBSX3 regulates rice growth and resistance to bacteria pathogens, Xanthomonas oryzae pv. oryzicola (Xoc) and X. oryzae pv. oryzae (Xoo), by modulating H₂S biosynthesis. OsCBSX3 exists in both oligomeric and monomeric forms in rice. Compared with wild-type OsCBSX3, an oligomerization-disrupted mutant exhibits the reduced capacity for H₂S synthesis, diminished resistance to X. oryzae, and inability to localize to the chloroplast. Upon pathogen infection, 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, an important subunit of photosystem II, and its binding to OsTrxZ, a member of the thioredoxin family. We further demonstrated that OsTrxZ can directly convert OsCBSX3 into monomers, thereby mitigating the excessive H₂S synthesis and its negative effects on rice growth and development. Overexpression of PsbO enhances rice resistance to both Xoc and Xoo, whereas overexpression of OsTrxZ exerts the opposite effect. Taken together, these findings suggest that PsbO and OsTrxZ antagonistically modulate the interconversion between oligomeric and monomeric forms of OsCBSX3, thereby balancing rice resistance and developmental processes.