Title: Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato

Abstract

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 pestmore » populations, our results suggest that antagonistic responses resulting from a combination of insect herbivory and moderate heat stress may exacerbate crop losses.« less

Authors:

Havko, Nathan E.; Das, Michael R.; McClain, Alan M.; Kapali, George; Sharkey, Thomas D. ;

• Search DOE PAGES for author "Sharkey, Thomas D."
• Search DOE PAGES for ORCID "0000-0002-4423-3223"
• Search orcid.org for ORCID "0000-0002-4423-3223"

Howe, Gregg A.

• Search DOE PAGES for author "Howe, Gregg A."
• Search DOE PAGES for ORCID "0000-0002-9218-979X"
• Search orcid.org for ORCID "0000-0002-9218-979X"

Publication Date:

2020-01-21

Research Org.:

Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory

Sponsoring Org.:

USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:

1592821

Alternate Identifier(s):

OSTI ID: 1625053; OSTI ID: 1735833

Grant/Contract Number:  

FG02-91ER20021; T32-GM110523

Resource Type:

Published Article

Journal Name:

Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:

Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 117 Journal Issue: 4; Journal ID: ISSN 0027-8424

Publisher:

National Academy of Sciences

Country of Publication:

United States

Language:

English

Subject:

54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; science & technology - other topics; climate change; jasmonate; plant–insect interaction; stomata; heat shock protein 90