Transcriptomic profiling provides molecular insights into tolerance mechanisms in wheat to wheat streak mosaic virus (WSMV)

Wheat curl mites (WCM) are arthropod pests that pose significant threats to wheat production by causing direct damage through feeding and transmitting viruses, such as wheat streak mosaic virus (WSMV), triticum mosaic virus (TriMV), and High Plains wheat mosaic virus (HPWMoV). Management of the WCM–WSMV disease complex has relied on strategies such as controlling volunteer wheat, delaying planting, and using wheat varieties resistant to the mite and the viruses. However, the emergence of virulent WCM populations and resistance-breaking isolates of WSMV underscores the urgent need to develop more diverse and durable sources of resistance. Over a two-year period of field screening, we found that a commercial wheat cultivar, Hatcher, with no known sources of resistance, consistently produced higher yields under high WSMV disease pressure, outperforming varieties that carry the WSMV and mite resistance genes. To investigate the mechanisms underlying the apparent tolerance in Hatcher, we compared its response to WCM and WSMV infection to a susceptible genotype, CO15D173R. Transcriptomic analysis revealed a nuanced interplay between plant defense and growth in Hatcher, with upregulation of genes related to jasmonic acid (JA), salicylic acid (SA), and abscisic acid (ABA) pathways, indicating a coordinated defense response. Notably, activation of lignin biosynthesis genes in Hatcher points to a potential role of cell wall strengthening in deterring WCM transmission of WSMV. Additionally, the regulation of genes involved in growth-related hormonal pathways, such as gibberellic acid (GA) and brassinosteroids (BR), highlights Hatcher’s ability to maintain growth under disease pressure. Our findings provide insight into the intricate network of phytohormones, growth-defense trade-offs, and cell wall modifications contributing to Hatcher’s potential tolerance to WCM and WSMV. This knowledge can inform the development of tolerant wheat varieties and enhance integrated pest management strategies, ultimately safeguarding wheat production.