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

Authors: ZHU, LIECENG - Fayetteville State University; MALDANI, MOHAMED - Fayetteville State University; Subramanyam, Subhashree; Chen, Ming Shun; SHI, RUI - North Carolina State University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/17/2026
Publication Date: 5/5/2026
Citation: Zhu, L., Maldani, M., Subramanyam, S., Chen, M., Shi, R. 2026. Transcriptomic changes associated with heat-induced susceptibility in wheat plants to Hessian fly (Diptera: Cecidomyiidae). Frontiers in Plant Science. https://doi.org/10.3389/fpls.2026.1794823.
DOI: https://doi.org/10.3389/fpls.2026.1794823

Interpretive Summary: Wheat is an important agricultural crop in the US and worldwide. Insect pests constantly threaten wheat crop productivity and global food security. Hessian fly is a major destructive insect pest of wheat causing significant loss of yield and negatively impacts US wheat growers and producers. Natural resistance in some wheat lines is the most cost-effective and sound strategy to control this pest. However, this strategy is threatened by heat stress that leads to the breakdown of native insect resistance in wheat. In this foundational study, we have identified molecular components involved in wheat resistance that are rendered ineffective to insect attack in heat-stressed wheat plants, leading to susceptibility and yield loss. This information is extremely important to allow breeders and scientists to design effective and sound approaches for more durable resistance to insect pests under fluctuating temperatures.

Technical Abstract: Wheat (Triticum aestivum L.) resistance to Hessian fly (HF, Mayetiola destructor) conferred by HF resistance (R) genes, is often vulnerable to heat stress. This study investigates the molecular basis of heat-induced susceptibility in wheat to HF. We compared the resistant cultivar ‘Molly’, which carries H13, 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 mounted stronger and broader defenses than Newton under normal temperature, whereas heat-stressed Molly displayed massive transcriptional reprogramming resulting in induced susceptibility. Comparative analysis identified 74 genes, including 63 upregulated and 11 downregulated genes, consistently regulated across all susceptible states, including heat-stressed Molly and Newton at both high and normal temperatures, but not in the resistant Molly under normal temperature. Most of these genes are defense related. Functional analysis of these genes revealed: (1) high auxin activity combined with low salicylic acid (SA) and 12-oxo-phytodienoic acid (OPDA) activity play central roles in susceptibility of wheat plants to HF under normal and heat-stressed conditions, (2) susceptibility is associated with misregulation and miscoordination of defense-related pathways, and (3) many defense-related genes induced in susceptible plants seemed to act as susceptibility-associated isoforms rather than effective resistance factors. The identification of susceptibility-associated genes provides molecular targets for breeding wheat cultivars with more durable resistance under rising temperatures.