RRC ID 81279
Author Guo Q, Yoshida Y, Major IT, Wang K, Sugimoto K, Kapali G, Havko NE, Benning C, Howe GA.
Title JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis.
Journal Proc Natl Acad Sci U S A
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 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.
Volume 115(45)
Pages E10768-E10777
Published 2018-11-6
DOI 10.1073/pnas.1811828115
PII 1811828115
PMID 30348775
PMC PMC6233084
MeSH Animals Arabidopsis / genetics* Arabidopsis / immunology Arabidopsis / microbiology Arabidopsis / parasitology Arabidopsis Proteins / genetics* Carbon / metabolism Cyclopentanes / metabolism* Disease Resistance / genetics Fungi / growth & development Fungi / pathogenicity Gene Expression Profiling Gene Expression Regulation, Developmental Gene Expression Regulation, Plant / immunology* Genetic Fitness / immunology* Insecta / pathogenicity Insecta / physiology Isoleucine / analogs & derivatives* Isoleucine / metabolism Metabolic Networks and Pathways / genetics Metabolic Networks and Pathways / immunology Multigene Family Mutation Plant Diseases / genetics* Plant Diseases / immunology Plant Diseases / microbiology Plant Diseases / parasitology Plant Immunity / genetics Protein Isoforms / deficiency Protein Isoforms / genetics Repressor Proteins / deficiency Repressor Proteins / genetics* Reproduction / genetics Reproduction / immunology Signal Transduction
Resource
Arabidopsis / Cultured plant cells, genes pst17092