Jiayi Yao, Shaomin Wu, Shushu Gao, Zhidan Xiang, Qian Wang, Fei Ye, Qiansheng Liao, Zhouhang Gu, Zhiyou Du
RNA viruses usually reprogramme host cellular lipid metabolism to create favourable replication microenvironments, yet the broader biological significance of these lipid changes is largely unknown. To explore the potential roles of virus-induced lipids, we employed an economically important plant pathogen cucumber mosaic virus (CMV), which has a single-stranded, positive-sense, tripartite RNA genome replicating in host tonoplasts. Lipidomic analysis of purified tonoplasts revealed that CMV infection increased the relative accumulation of sphingolipids in tonoplasts. This is consistent with the increased expression levels of these enzymes involved in sphingolipid biosynthesis, particularly 3-ketosphinganine reductase (TSC10). Virus-induced silencing of Nb-TSC10 in Nicotiana benthamiana impaired CMV replication by triggering the unfolded protein response (UPR). Furthermore, we found that salicylic acid (SA) serves as a central regulator of UPR-mediated antiviral immunity. Notably, a specific sphingolipid, ceramide, was found to alleviate the UPR, suggesting an important role for sphingolipids during CMV infection: CMV subverts SA-induced immunity by rewiring sphingolipid biosynthesis to inhibit the UPR-mediated defence. This work advances mechanistic understanding of viral counterdefence strategies through sphingolipid-mediated modulation of UPR during plant-pathogen interactions.