Transcriptomic changes associated with heat-induced susceptibility in wheat plants to Hessian fly (Diptera: Cecidomyiidae)

Wheat (<i>Triticum aestivum</i> L.) resistance to Hessian fly (HF, <i>Mayetiola destructor</i>) conferred by HF resistance (<i>R</i>) genes, is often vulnerable to heat stress. This study aims to investigate the molecular basis of heat-induced susceptibility in wheat to HF. We compared the resistant cultivar 'Molly', which carries <i>H13</i>, with its susceptible near-isogenic line 'Newton' to determine how elevated temperature alters phenotypic and molecular responses to HF infestation. Our phenotyping results showed that a single 24 h heat treatment at 30 °C was sufficient to compromise Molly's resistance, resulting in more than 70% of plants becoming susceptible. Transcriptomic profiling revealed that resistant Molly exhibited stronger and broader defenses than Newton under normal temperature, whereas heat-stressed Molly displayed extensive transcriptional reprogramming resembling the naturally susceptible Newton wheat. Comparative analysis of transcriptomic profiles identified 74 genes that are consistently regulated across all susceptible states at 24 h after initial HF infestation, including heat-stressed Molly and Newton under both high and normal temperatures, but not in the resistant Molly under normal temperature. Functional annotation of these susceptibility-related genes in combination with previous findings suggest that susceptibility is likely associated with increased auxin-related activity, reduced salicylic acid (SA) and OPDA-associated defense signaling, and altered coordination of defense pathways that favor feeding-site establishment and redirecting host resource to developing HF larvae. The identification of susceptibility-associated candidate genes provides molecular targets for breeding wheat cultivars with more durable resistance under rising temperatures.