Seed microbiome confers wheat resistance to soil-borne yellow mosaic virus through coordinated activation of ABA and SA signaling pathways

Aims: Soil-borne wheat yellow mosaic virus (WYMV), transmitted by the Polymyxa graminis, poses a severe threat to global wheat production. Although seed microbiome is the first colonizer of the rhizosphere and root tissues, its role in defense against soil-borne WYMV remains unexplored. Methods: Here, using 12 wheat varieties with contrasting resistance to WYMV, we integrated seed microbiome characterization, culturable seed endophyte inoculation assays, hydroponic validation experiments and defense gene expression profiling, to elucidate the contribution of the seed microbiome to soil-borne viral resistance. Results: We found that resistant varieties exhibited significantly reduced WYMV loads in both leaves (33.5% reduction) and roots (31.9% reduction), along with lower P. graminis colonization in roots (12.9% reduction) compared with susceptible varieties. Their seed endophytes displayed higher bacterial richness and enrichment of potential beneficial taxa, including Bradyrhizobium, Sphingomonas, and Epicoccum. Resistant varieties also harbored less complex microbial networks, with a higher proportion of negative interactions, and featured hub taxa linked to pathogen suppression and growth-promotion (e.g., Bacillus and Burkholderia). Crucially, inoculation with culturable endophytes from resistant seeds suppressed WYMV accumulation by 12.9%–20.7% and induced coordinated upregulation of abscisic acid (ABA; SnRK2, LIPASE, and TaPYL) and salicylic acid (SA; PR2, PR3, PR5, and SAG3) signaling pathways. In contrast, endophytes from susceptible seeds showed negligible effects. Conclusions: Our study uncovers the role of seed endophytic microbiome in conferring antiviral resistance through microbiome-mediated hormonal priming, providing a framework for leveraging native seed microbial communities in sustainable management of soil-borne viral disease.