JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis
Abstract
Plant immune responses mediated by the hormone jasmonoyl-L-isoleucine (JA-Ile) are metabolically costly and often linked to reduced growth. Although it is known that JA-Ile activates defense responses by triggering the degradation of JASMONATE ZIM DOMAIN (JAZ) transcriptional repressor proteins, expansion of the JAZ gene family in vascular plants has hampered efforts to understand how this hormone impacts growth and other physiological tasks over the course of ontogeny. Here, we combined mutations within the 13-member Arabidopsis JAZ gene family to investigate the effects of chronic JAZ deficiency on growth, defense, and reproductive output. A higher-order mutant (jaz decuple, jazD) defective in 10 JAZ genes (JAZ1–7, -9, -10, and -13) exhibited robust resistance to insect herbivores and fungal pathogens, which was accompanied by slow vegetative growth and poor reproductive performance. Metabolic phenotypes of jazD discerned from global transcript and protein profiling were indicative of elevated carbon partitioning to amino acid-, protein-, and endoplasmic reticulum body-based defenses controlled by the JA-Ile and ethylene branches of immunity. Resource allocation to a strong defense sink in jazD leaves was associated with increased respiration and hallmarks of carbon starvation but no overt changes in photosynthetic rate. Depletion of the remaining JAZ repressors in jazD further exaggeratedmore »
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States). DOE Plant Research laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1478446
- Alternate Identifier(s):
- OSTI ID: 1603655
- 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: 115 Journal Issue: 45; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; jasmonate; growth–defense trade-off; plant immunity; plant-insect interaction; carbon starvation
Citation Formats
Guo, Qiang, Yoshida, Yuki, Major, Ian T., Wang, Kun, Sugimoto, Koichi, Kapali, George, Havko, Nathan E., Benning, Christoph, and Howe, Gregg A. JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis. United States: N. p., 2018.
Web. doi:10.1073/pnas.1811828115.
Guo, Qiang, Yoshida, Yuki, Major, Ian T., Wang, Kun, Sugimoto, Koichi, Kapali, George, Havko, Nathan E., Benning, Christoph, & Howe, Gregg A. JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis. United States. https://doi.org/10.1073/pnas.1811828115
Guo, Qiang, Yoshida, Yuki, Major, Ian T., Wang, Kun, Sugimoto, Koichi, Kapali, George, Havko, Nathan E., Benning, Christoph, and Howe, Gregg A. Mon .
"JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis". United States. https://doi.org/10.1073/pnas.1811828115.
@article{osti_1478446,
title = {JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis},
author = {Guo, Qiang and Yoshida, Yuki and Major, Ian T. and Wang, Kun and Sugimoto, Koichi and Kapali, George and Havko, Nathan E. and Benning, Christoph and Howe, Gregg A.},
abstractNote = {Plant immune responses mediated by the hormone jasmonoyl-L-isoleucine (JA-Ile) are metabolically costly and often linked to reduced growth. Although it is known that JA-Ile activates defense responses by triggering the degradation of JASMONATE ZIM DOMAIN (JAZ) transcriptional repressor proteins, expansion of the JAZ gene family in vascular plants has hampered efforts to understand how this hormone impacts growth and other physiological tasks over the course of ontogeny. Here, we combined mutations within the 13-member Arabidopsis JAZ gene family to investigate the effects of chronic JAZ deficiency on growth, defense, and reproductive output. A higher-order mutant (jaz decuple, jazD) defective in 10 JAZ genes (JAZ1–7, -9, -10, and -13) exhibited robust resistance to insect herbivores and fungal pathogens, which was accompanied by slow vegetative growth and poor reproductive performance. Metabolic phenotypes of jazD discerned from global transcript and protein profiling were indicative of elevated carbon partitioning to amino acid-, protein-, and endoplasmic reticulum body-based defenses controlled by the JA-Ile and ethylene branches of immunity. Resource allocation to a strong defense sink in jazD leaves was associated with increased respiration and hallmarks of carbon starvation but no overt changes in photosynthetic rate. Depletion of the remaining JAZ repressors in jazD further exaggerated growth stunting, nearly abolished seed production and, under extreme conditions, caused spreading necrotic lesions and tissue death. Our results demonstrate that JAZ proteins promote growth and reproductive success at least in part by preventing catastrophic metabolic effects of an unrestrained immune response.},
doi = {10.1073/pnas.1811828115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 45,
volume = 115,
place = {United States},
year = {Mon Oct 22 00:00:00 EDT 2018},
month = {Mon Oct 22 00:00:00 EDT 2018}
}
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https://doi.org/10.1073/pnas.1811828115
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