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

Authors:
 [1];  [1];  [1];  [1]; ORCiD logo [1]; ORCiD logo [1]
  1. Michigan State Univ., East Lansing, MI (United States)
Publication Date:
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 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

Citation Formats

Havko, Nathan E., Das, Michael R., McClain, Alan M., Kapali, George, Sharkey, Thomas D., and Howe, Gregg A. Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato. United States: N. p., 2020. Web. doi:10.1073/pnas.1913885117.
Havko, Nathan E., Das, Michael R., McClain, Alan M., Kapali, George, Sharkey, Thomas D., & Howe, Gregg A. Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato. United States. https://doi.org/10.1073/pnas.1913885117
Havko, Nathan E., Das, Michael R., McClain, Alan M., Kapali, George, Sharkey, Thomas D., and Howe, Gregg A. Tue . "Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato". United States. https://doi.org/10.1073/pnas.1913885117.
@article{osti_1592821,
title = {Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato},
author = {Havko, Nathan E. and Das, Michael R. and McClain, Alan M. and Kapali, George and Sharkey, Thomas D. and Howe, Gregg A.},
abstractNote = {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 plantSolanum 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.},
doi = {10.1073/pnas.1913885117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 4,
volume = 117,
place = {United States},
year = {2020},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1913885117

Citation Metrics:
Cited by: 35 works
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Figures / Tables:

Fig. 1 Fig. 1: Elevated temperature enhances JA responses and insect feeding. (A) Inh-II levels in leaves of wounded (W) and undamaged control (C) plants. Wild-type and jasmonate-insensitive1 (jai1-1) tomato plants grown for 17 d under the CT regime (28 °C 16 h light/18 °C 8 h dark) were transferred to eithermore » CT or ET (38 °C 16 h light/28 °C 8 h dark). Five days after transfer to CT or ET treatment chambers, leaves were mechanically wounded. Inh-II levels in the damaged leaves were measured 24 h after wounding. Data points represent the mean ± SE of four biological replicates. Lowercase letters denote significant differences (Tukey’s honestly significant difference [HSD] test P < 0.05). (B and C) Time course of wound-induced transcript accumulation of two JA-responsive genes, ARG2 (B) and TD2 (C). WT plants were grown as described in A and transferred to CT or ET treatment chambers for 2 d prior to wounding. Leaf tissue was harvested for RNA extraction at the indicated times after wounding. ARG2 and TD2 mRNA levels were determined by qPCR, with normalization to an ACTIN housekeeping gene. Data points represent the mean ± SE of four biological replicates. (D) Effect of ET on JA-mediated root growth inhibition. WT seeds were germinated at ambient temperature (22 °C) on filter paper prior to treatment with 1 mM MeJA or mock control (mock), followed by immediate transfer to CT or ET conditions for 2 d. Data points represent the mean ± SE of >30 seedlings. Lowercase letters denote significant differences (Tukey’s HSD test P < 0.05). (E and F) Insect feeding assays on WT and jai1-1 plants under CT or ET conditions. Seventeen-day-old WT and jai1-1 plants grown under CT conditions were transferred to CT or ET treatment chambers for 5 d prior to challenge with two M. sexta larva per leaf. Feeding proceeded at either CT or ET. The amount of leaf area consumed per larva (E) and larval weight gain (F) were measured at the indicated times after challenge. Data points represent the mean ± SE of three biological replicates.« less

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Works referencing / citing this record:

Stimulation of Insect Herbivory by Elevated Temperature Outweighs Protection by the Jasmonate Pathway
journal, February 2020


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.