skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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:
; ; ; ; ORCiD logo; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1592821
Grant/Contract Number:  
FG02-91ER20021
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:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

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. doi: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. doi: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 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.},
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
DOI: 10.1073/pnas.1913885117

Save / Share:

Works referenced in this record:

The Combined Effect of Drought Stress and Heat Shock on Gene Expression in Tobacco
journal, October 2002


The differential effects of herbivory by first and fourth instars of Trichoplusia ni (Lepidoptera: Noctuidae) on photosynthesis in Arabidopsis thaliana
journal, December 2005

  • Tang, Jennie Y.; Zielinski, Raymond E.; Zangerl, Arthur R.
  • Journal of Experimental Botany, Vol. 57, Issue 3
  • DOI: 10.1093/jxb/erj032

The wound hormone jasmonate
journal, September 2009


Modularity in Jasmonate Signaling for Multistress Resilience
journal, April 2018


GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling
journal, August 2013

  • Mousavi, Seyed A. R.; Chauvin, Adeline; Pascaud, François
  • Nature, Vol. 500, Issue 7463
  • DOI: 10.1038/nature12478

Molecular and genetic control of plant thermomorphogenesis
journal, January 2016


Community shifts under climate change: Mechanisms at multiple scales
journal, July 2013

  • Gornish, Elise S.; Tylianakis, Jason M.
  • American Journal of Botany, Vol. 100, Issue 7
  • DOI: 10.3732/ajb.1300046

High Temperature Induces Expression of Tobacco Transcription Factor NtMYC2a to Regulate Nicotine and JA Biosynthesis
journal, October 2016


Abiotic and biotic stress combinations
journal, April 2014

  • Suzuki, Nobuhiro; Rivero, Rosa M.; Shulaev, Vladimir
  • New Phytologist, Vol. 203, Issue 1
  • DOI: 10.1111/nph.12797

Plant Immunity to Insect Herbivores
journal, June 2008


Narrow safety margin in the phyllosphere during thermal extremes
journal, February 2019

  • Pincebourde, Sylvain; Casas, Jérôme
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 12
  • DOI: 10.1073/pnas.1815828116

Jasmonate signalling in Arabidopsis involves SGT1b–HSP70–HSP90 chaperone complexes
journal, April 2015


Stage-specific effects of temperature and dietary protein on growth and survival of Manduca sexta caterpillars
journal, March 2000


The invasin D protein from Yersinia pseudotuberculosis selectively binds the Fab region of host antibodies and affects colonization of the intestine
journal, March 2018

  • Sadana, Pooja; Geyer, Rebecca; Pezoldt, Joern
  • Journal of Biological Chemistry, Vol. 293, Issue 22
  • DOI: 10.1074/jbc.RA117.001068

COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine
journal, May 2008

  • Katsir, L.; Schilmiller, A. L.; Staswick, P. E.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 19
  • DOI: 10.1073/pnas.0802332105

Wounding-Induced Stomatal Closure Requires Jasmonate-Mediated Activation of GORK K+ Channels by a Ca2+ Sensor-Kinase CBL1-CIPK5 Complex
journal, January 2019


Adaptive evolution of threonine deaminase in plant defense against insect herbivores
journal, March 2011

  • Gonzales-Vigil, E.; Bianchetti, C. M.; Phillips, G. N.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 14
  • DOI: 10.1073/pnas.1016157108

Increase in crop losses to insect pests in a warming climate
journal, August 2018

  • Deutsch, Curtis A.; Tewksbury, Joshua J.; Tigchelaar, Michelle
  • Science, Vol. 361, Issue 6405
  • DOI: 10.1126/science.aat3466

Glutamate triggers long-distance, calcium-based plant defense signaling
journal, September 2018


Wound-induced Proteinase Inhibitor in Tomato Leaves: Some Effects of Light and Temperature on the Wound Response
journal, January 1973


Control of Carbon Assimilation and Partitioning by Jasmonate: An Accounting of Growth–Defense Tradeoffs
journal, January 2016


Jasmonate Negatively Regulates Stomatal Development in Arabidopsis Cotyledons
journal, March 2018

  • Han, Xiao; Hu, Yanru; Zhang, Gensong
  • Plant Physiology, Vol. 176, Issue 4
  • DOI: 10.1104/pp.17.00444

Indirect suppression of photosynthesis on individual leaves by arthropod herbivory
journal, July 2008

  • Nabity, Paul D.; Zavala, Jorge A.; DeLucia, Evan H.
  • Annals of Botany, Vol. 103, Issue 4
  • DOI: 10.1093/aob/mcn127

From The Cover: Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut
journal, December 2005

  • Chen, H.; Wilkerson, C. G.; Kuchar, J. A.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 52
  • DOI: 10.1073/pnas.0509026102

For security and stability: SGT1 in plant defense and development
journal, October 2011

  • Meldau, Stefan; Baldwin, Ian T.; Wu, Jianqiang
  • Plant Signaling & Behavior, Vol. 6, Issue 10
  • DOI: 10.4161/psb.6.10.17708

New Insights into Plant Responses to the Attack from Insect Herbivores
journal, December 2010


Why Does Herbivore Attack Reconfigure Primary Metabolism?
journal, March 2008


Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field
journal, November 2012


HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1
journal, January 2016

  • Wang, Renhou; Zhang, Yi; Kieffer, Martin
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10269

Impact of plant shoot architecture on leaf cooling: a coupled heat and mass transfer model
journal, August 2013

  • Bridge, L. J.; Franklin, K. A.; Homer, M. E.
  • Journal of The Royal Society Interface, Vol. 10, Issue 85
  • DOI: 10.1098/rsif.2013.0326

Jasmonate-Triggered Plant Immunity
journal, June 2014

  • Campos, Marcelo L.; Kang, Jin-Ho; Howe, Gregg A.
  • Journal of Chemical Ecology, Vol. 40, Issue 7
  • DOI: 10.1007/s10886-014-0468-3

High temperature exposure increases plant cooling capacity
journal, May 2012

  • Crawford, Amanda J.; McLachlan, Deirdre H.; Hetherington, Alistair M.
  • Current Biology, Vol. 22, Issue 10
  • DOI: 10.1016/j.cub.2012.03.044

Thermomorphogenesis
journal, April 2019


Jasmonate Passes Muster: A Receptor and Targets for the Defense Hormone
journal, June 2009


The Arabidopsis F-Box Protein CORONATINE INSENSITIVE1 Is Stabilized by SCF COI1 and Degraded via the 26S Proteasome Pathway
journal, February 2013


Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses
journal, December 2012

  • Raffa, K. F.; Powell, E. N.; Townsend, P. A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 6
  • DOI: 10.1073/pnas.1216666110

Biotic stress globally downregulates photosynthesis genes: Biotic stress downregulates photosynthesis
journal, September 2010


JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling
journal, July 2007

  • Thines, Bryan; Katsir, Leron; Melotto, Maeli
  • Nature, Vol. 448, Issue 7154
  • DOI: 10.1038/nature05960