Integrated GWAS and multi-omics reveal rapid JA signaling activation orchestrated by OsJAR2 to drive Southern Rice Black-Streaked Dwarf Virus resistance in rice

Background Southern rice black-streaked dwarf virus (SRBSDV), transmitted by the white-backed planthopper (WBPH), causes severe yield losses (up to 70%) in rice across Asia. However, elite resistant germplasms and molecular defense mechanisms remain elusive, hindering breeding efforts. Effective management strategies are limited, necessitating systematic dissection of SRBSDV resistance networks. Results Screening 195 rice accessions identified the indica variety R91 as highly resistant (0% disease incidence), exhibiting dual resistance to SRBSDV and rice black-streaked dwarf virus (RBSDV). South Asian accessions displayed superior resistance compared to East Asian counterparts. Multi-omics analysis revealed rapid defense activation in R91, including a 1.88-fold increase in jasmonic acid (JA) at 5 days post-inoculation (dpi) and upregulation of > 2,000 defense genes, while susceptible lines showed JA depletion (70%) and suppressed responses. Time-ordered co-expression networks pinpointed OsJAR2 (JA-Ile synthase, LOC_Os01g12160 ) as a central hub, with 3.2-fold higher expression in R91 during early infection. GWAS identified a novel SRBSDV resistance QTL ( qSRBSDV1-1 ) co-localizing with OsJAR2 , and haplotype analysis validated OsJAR2 as the candidate causal resistance gene, providing genetic evidence for its role in SRBSDV defense. Conclusions Our study identifies R91 as a dual-resistant germplasm to SRBSDV and RBSDV, with OsJAR2-mediated JA signaling playing a pivotal role in conferring resistance. The rapid activation of JA biosynthesis and synchronized defense gene regulation establish a molecular blueprint for resistance breeding. Importantly, OsJAR2 represents a novel candidate functional resistance gene, and its H3 haplotype may serve as a robust genetic marker for accelerating the development of elite SRBSDV-resistant varieties through marker-assisted selection. By integrating germplasm characterization, mechanistic insights, and breeding applications, this work provides a foundation for sustainable rice protection against viral threats.