Flooding and herbivory: The effect of concurrent stress factors on plant volatile emissions and gene expression in two heirloom tomato varieties

Authors: NGUMBI, ESTHER - University Of Illinois; DADY, ERINN - University Of Illinois; Calla, Bernarda

Submitted to: BMC Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/7/2022
Publication Date: 12/1/2022
Citation: Ngumbi, E., Dady, E., Calla, B. 2022. Flooding and herbivory: The effect of concurrent stress factors on plant volatile emissions and gene expression in two heirloom tomato varieties. BMC Plant Biology. 22. Article 536. https://doi.org/10.1186/s12870-022-03911-3.
DOI: https://doi.org/10.1186/s12870-022-03911-3

Interpretive Summary: Flooding and herbivory may cause significant crop yield losses if present, requiring sometimes costly managing and mitigation practices. Although the effects of flooding and herbivory in crop plants have been largely studied, the effects of the combination of those two factors, which may occur simultaneously or sequentially in the field, are less understood. In this work, we carried out experiments to compare the volatile chemical profiles and the molecular underpinning of the response of two heirloom tomato varieties to flooding and herbivory alone or in combination. We found that flooding in combination to herbivory significantly increased the emission of terpene volatiles in the two tomato varieties studied, whereas herbivory alone had no significant effects. Gene expression analyses showed that flooding affected plant defense responses, hormone metabolism and photosynthesis whereas the herbivory treatment only had significant effects in gene expression when combined with flooding. Major pathways activated with flooding and herbivory included phenylpropanoid and the terpenoid biosynthesis. Understanding how different tomato varieties respond to the simultaneous exposure of flooding and herbivory is important for the selection and development of newer varieties and for the formulation of efficient mitigation methods.

Technical Abstract: Background: In nature and in cultivated fields, plants encounter multiple stress factors. Nonetheless, our understanding of how plants actively respond to combinatorial stress remains limited. Among the least studied stress combination is that of flooding and herbivory, despite the growing importance of these stressors in the context of climate change. We investigated plant chemistry and gene expression changes in two heirloom tomato varieties: Cherokee purple (CP) and Striped German (SG) in response to flooding, herbivory by Spodoptera exigua, and their combination. Results: Volatile organic compounds (VOCs) identified in tomato plants subjected to flooding and/or herbivory included several mono- and sesquiterpenes. Flooding was the main factor altering VOCs emission rates, and impacted plant biomass accumulation, while different varieties had quantitative differences in their VOC emissions. At the gene expression levels, there were 335 differentially expressed genes between the two tomato plant varieties, these included genes encoding for phenylalanine ammonia-lyase (PAL), cinnamoyl-CoA-reductase-like, and phytoene synthase (Psy1). Flooding and variety effects together influenced ABA signaling genes with the SG variety showing higher levels of ABA production and ABA-dependent signaling upon flooding. Flooding downregulated genes associated with cytokinin catabolism and general defense response and upregulated genes associated with ethylene biosynthesis, anthocyanin biosynthesis, and gibberellin biosynthesis. Combining flooding and herbivory induced the upregulation of genes including chalcone synthase (CHS), PAL, and genes encoding BAHD acyltransferase and UDP-glucose iridoid glucosyltransferase-like genes in one of the tomato varieties (CP) and a disproportionate number of heat-shock proteins in SG. Only the SG variety had measurable changes in gene expression due to herbivory alone, upregulating zeatin, and O-glucosyltransferase and thioredoxin among others. Conclusion: Our results suggest that both varieties differ in their production of secondary metabolites including phenylpropanoids and terpenoids and their regulation and activation of ABA signaling upon stress associated with flooding. Herbivory and flooding together had interacting effects that were evident at the level of VOC production, gene expression and biomass markers. Results from our study highlight the complex nature of plant responses to combinatorial stresses and point at specific genes and pathways that might be affected flooding and herbivory combined.