JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis

Abstract

SignificanceThe plant hormone jasmonate promotes resistance to plant-eating organisms, ranging from pathogenic microbes to mammals. Jasmonate reprograms metabolism to fuel the production of diverse defense compounds and simultaneously inhibits plant growth. Understanding how growth is influenced across a range of defense levels remains unclear, but has important implications for optimizing crop productivity. Using a genetic approach to “tune” the jasmonate response, we assessed the physiological consequences of discrete levels of defense throughout the plant life cycle. Overactivation of jasmonate response led to carbon starvation, near loss of seed production and, under extreme conditions, lethality. Our findings explain the emergence of diverse strategies to keep jasmonate responses at bay and provide new insights into metabolic processes that underlie growth–defense trade-offs.

Evolutionary Origin of JAZ Proteins and Jasmonate Signaling

“…Consistent with the notion that AtJAZs perform partially overlapping tasks, analysis of multi-order jaz mutants (i.e., defective in several JAZ genes) revealed that plant sensitivity to JA-Ile gradually increases as more JAZs are removed (Campos et al, 2016;Guo et al, 2018b). Graduated JAZ deficiency in Arabidopsis also increases resistance to biotic stress and concomitantly decreases growth and reproductive output (Guo et al, 2018b). These findings indicate that although AtJAZs are potent repressors of diverse defense responses, they also behave as positive regulators of growth and reproductive fitness.…”

“…Progress toward this goal, however, has been hampered by genetic redundancy within the JAZ gene family, which in Arabidopsis consists of 13 members (Howe et al, 2018). Consistent with the notion that AtJAZs perform partially overlapping tasks, analysis of multi-order jaz mutants (i.e., defective in several JAZ genes) revealed that plant sensitivity to JA-Ile gradually increases as more JAZs are removed (Campos et al, 2016;Guo et al, 2018b). Graduated JAZ deficiency in Arabidopsis also increases resistance to biotic stress and concomitantly decreases growth and reproductive output (Guo et al, 2018b).…”

OsPEX5 regulates rice spikelet development through modulating jasmonic acid biosynthesis

“…The msd1 mutant displayed a large panicle phenotype due to greater size and number of inflorescence branches, suggesting that JA regulates pedicellate spikelet fertility in sorghum (Jiao et al ., ). Arabidopsis mutants defective in JA biosynthesis and signalling pathway, such as dad1 , opr3 , myc2/3/4/5 , and coi1 , displayed a male sterility phenotype caused by delayed anther dehiscence, inactive pollen and short filament elongation (Feys et al ., ; Stintzi & Browse, ; Ishiguro et al ., ; Browse, ; Qi et al ., ) and jazD (defective in 10 JAZ genes) exhibited slow vegetative growth and low fertility, but powerful resistance to necrotrophic pathogens and insect herbivores (Guo et al ., ). In Marchantia polymorpha , Mpjaz showed dwarf phenotypes, narrow branches, and aberrant antheridiophores (Monte et al ., ).…”

Integrated Multi-omic Framework of the Plant Response to Jasmonic Acid

“…In addition, MYCs simultaneously target various negative regulators enabling MYCs to efficiently dampen the JA response pattern. Key negative regulators of JA signaling are the JAZ repressors, a gene family of 13 members in Arabidopsi s (Guo et al, 2018, Chung et al, 2010, Cuellar Perez et al, 2014) which can interact with the adaptor protein NINJA to confer TOPLESS-mediated gene repression (Pauwels et al, 2010). Strikingly, all JAZs and also NINJA are directly bound by MYC2 and MYC3 (Supplementary Fig.…”

“…Uncoupling these subnetworks would be an effective way to determine how they interact to drive very robust activation of the JA pathway. The combination of our multi-omic framework approach coupled with powerful genetic approaches such as the generation of the jaz decuple mutant (Guo et al, 2018) should significantly contribute to a better understanding of JA response pathways…”