Timing is everything: Transcriptomic response of tomato (Solanum lycopersicum) to single and sequential combined stressors of herbivory and flooding

Global change has increased the frequency and intensity of biotic and abiotic stressors of plants, including insect herbivory and flooding, with devastating consequences on crop productivity, and ultimately, food security. Although knowledge of plant responses to individual stressors is extensive, little is known about how plants respond to simultaneously occurring stress combinations. Also, it is poorly understood how the sequence of stress impacts plant responses and stress acclimation. The few available studies have uncovered unique and novel responses to single and combined stressors. Moreover, most combined stress studies were conducted on non-agricultural plants, creating a need for studies on crop plants. To fill these knowledge gaps, in this study, I investigated the dynamics of transcriptomic changes within tomato plants (Solanum lycopersicum L cv. ‘Cherokee Purple’) exposed to single, simultaneous, and sequential stress of herbivory by Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) and flooding. My results revealed that plants exposed to single stressors differentially expressed genes (DEGs) that correlated with response to phytohormones, signaling pathways, and ion transport. Herbivory alone caused upregulation of genes associated with jasmonic acid responses, jasmonic acid signaling pathways, and ion transport, whereas flooding alone caused upregulation of genes associated with ethylene responses and ethylene signaling pathways. When herbivory and flooding stressors were combined in a reciprocal sequential pattern (herbivory first followed by flooding vs. flooding first followed by herbivory), my results revealed a unique gene expression pattern, different from that brought about by single stressors alone. Combined stress in both sequences upregulated intracellular transport, and downregulated photosynthesis, exposing a general stress response strategy. The herbivory first response resulted in upregulation of sugar synthesis, modification and breakdown, and ion transport. In contrast, the flooding first response mirrored a general stress response strategy, with upregulation of intracellular transport and ion binding, and downregulation of photosynthesis. Taken together, my results reveal that gene expression is unique between different single stressors and the symmetrical switch of sequential stress combinations. The findings of this study provide insight into potential mechanisms of how plants respond and survive a combination of sequential biotic and abiotic plant stressors, and indicate that the sequence of stress matters. This lays an important foundation for future studies on management of stress combinations facing agricultural crops and development of crops that are resilient to multiple stressors.

Name thesis:degree_name

M.S.

Level thesis:degree_level

Thesis

Discipline thesis:degree_discipline

Entomology

Grantor

University of Illinois Urbana-Champaign

Year dc:date

2025

Author dc:creator

• Dady, Erinn Rea

Contributors dc:contributor

• Ngumbi, Esther N.
• Ngumbi, Esther N
• Hind, Sarah R
• Berenbaum, May R
• Suarez, Andrew

• Plant Stress
• Stress Combination
• Gene Expression
• Solanum Lycopersicum
• Spodoptera Exigua
• Insect Herbivory
• Flooding
• Biotic Stress
• Abiotic Stress

Statement dc:rights

• Copyright 2025 Erinn Rea Dady

Language dc:language

en, eng

Handle dc:identifier

https://hdl.handle.net/2142/130004

OAI record oai:identifier

https://www.ideals.illinois.edu/oai-pmh?verb=GetRecord&metadataPrefix=etdms&identifier=oai%3Awww.ideals.illinois.edu%3A2142%2F130004