Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato
| Autor: | Alan M. McClain, Michael R. Das, Gregg A. Howe, George Kapali, Nathan E. Havko, Thomas D. Sharkey |
|---|---|
| Rok vydání: | 2020 |
| Předmět: |
0106 biological sciences
Hot Temperature Insecta Climate Change media_common.quotation_subject stomata Plant Biology Cyclopentanes Insect Biology 01 natural sciences plant–insect interaction 03 medical and health sciences Solanum lycopersicum Plant Growth Regulators Heat shock protein Botany Animals HSP90 Heat-Shock Proteins Herbivory Oxylipins Jasmonate heat shock protein 90 Plant Proteins 030304 developmental biology media_common 2. Zero hunger 0303 health sciences Herbivore Multidisciplinary Abiotic stress fungi food and beverages Feeding Behavior Biological Sciences Biotic stress biology.organism_classification jasmonate Plant Leaves 13. Climate action Plant hormone Solanum 010606 plant biology & botany |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America |
| ISSN: | 1091-6490 0027-8424 |
| Popis: | Significance Crop damage by insect pests is predicted to increase as rising surface temperatures accelerate insect metabolism, population size, and range expansion. The plant defense hormone jasmonate promotes resistance to diverse herbivores, but how this wound signal impacts the plant’s ability to cope with a combination of herbivory and elevated temperature remains unknown. Here, we show that heat shock proteins contribute to enhanced jasmonate responses in tomato plants subjected to simulated heat waves. Herbivore-induced jasmonate signaling at elevated temperature, however, blocked stomatal opening and leaf hyponasty, leading to leaf overheating, reduced photosynthesis, and growth inhibition. Our results show how signal conflict between biotic and abiotic stress may exaggerate crop losses under warming conditions that accelerate herbivory, potentially jeopardizing food security. As global climate change brings elevated average temperatures and more frequent and extreme weather events, pressure from biotic stresses will become increasingly compounded by harsh abiotic stress conditions. The plant hormone jasmonate (JA) promotes resilience to many environmental stresses, including attack by arthropod herbivores whose feeding activity is often stimulated by rising temperatures. How wound-induced JA signaling affects plant adaptive responses to elevated temperature (ET), however, remains largely unknown. In this study, we used the commercially important crop plant Solanum lycopersicum (cultivated tomato) to investigate the interaction between simulated heat waves and wound-inducible JA responses. We provide evidence that the heat shock protein HSP90 enhances wound responses at ET by increasing the accumulation of the JA receptor, COI1. Wound-induced JA responses directly interfered with short-term adaptation to ET by blocking leaf hyponasty and evaporative cooling. Specifically, leaf damage inflicted by insect herbivory or mechanical wounding at ET resulted in COI1-dependent stomatal closure, leading to increased leaf temperature, lower photosynthetic carbon assimilation rate, and growth inhibition. Pharmacological inhibition of HSP90 reversed these effects to recapitulate the phenotype of a JA-insensitive mutant lacking the COI1 receptor. As climate change is predicted to compound biotic stress with larger and more voracious arthropod pest populations, our results suggest that antagonistic responses resulting from a combination of insect herbivory and moderate heat stress may exacerbate crop losses. |
| Databáze: | OpenAIRE |
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