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.

Significance: Plants receive volatile compounds emitted by neighboring plants that are infested by herbivores, and consequently the receiver plants begin to defend against forthcoming herbivory. To date, how plants receive volatiles and, consequently, how they fortify their defenses, is largely unknown. We found that tomato plants absorbed the airborne green leaf alcohol ( Z )-3-hexenol emitted by neighboring conspecific plants under attack by herbivores and subsequently converted the alcohol to a glycoside. The glycoside suppressed growth and survival rates of cutworms. The accumulation of glycoside in the receiver plants explained the defense acquired via “smelling” their neighbors. This study showed that the processing of a volatile compound is a mechanism of volatile reception in tomato plants.

Almost all terrestrial plants produce green leaf volatiles (GLVs), consisting of six-carbon (C6) aldehydes, alcohols and their esters, after mechanical wounding. C6 aldehydes deter enemies, but C6 alcohols and esters are rather inert. In this study, we address why the ability to produce various GLVs in wounded plant tissues has been conserved in the plant kingdom. The major product in completely disrupted Arabidopsis leaf tissues was (Z)-3-hexenal, while (Z)-3-hexenol and (Z)-3-hexenyl acetate were the main products formed in the intact parts of partially wounded leaves. ¹³C-labeled C6 aldehydes placed on the disrupted part of a wounded leaf diffused into neighboring intact tissues and were reduced to C6 alcohols. The reduction of the aldehydes to alcohols was catalyzed by an NADPH-dependent reductase. When NADPH was supplemented to disrupted tissues, C6 aldehydes were reduced to C6 alcohols, indicating that C6 aldehydes accumulated because of insufficient NADPH. When the leaves were exposed to higher doses of C6 aldehydes, however, a substantial fraction of C6 aldehydes persisted in the leaves and damaged them, indicating potential toxicity of C6 aldehydes to the leaf cells. Thus, the production of C6 aldehydes and their differential metabolisms in wounded leaves has dual benefits. In disrupted tissues, C6 aldehydes and their α,β-unsaturated aldehyde derivatives accumulate to deter invaders. In intact cells, the aldehydes are reduced to minimize self-toxicity and allow healthy cells to survive. The metabolism of GLVs is thus efficiently designed to meet ecophysiological requirements of the microenvironments within a wounded leaf.

As reactive oxygen species (ROS) play critical roles in plants to determine cell fate in various physiological situations, there is keen interest in the biochemical processes of ROS signal transmission. Reactive carbonyl species (RCS), the α,β-unsaturated aldehydes and ketones produced from lipid peroxides, due to their chemical property to covalently modify protein, can mediate ROS signals to proteins. Comprehensive carbonyl analysis in plants has revealed that more than a dozen different RCS, e.g., acrolein, 4-hydroxy-(E)-2-nonenal and malondialdehyde, are produced from various membranes, and some of them increase and modify proteins in response to oxidative stimuli. At early stages of response, specific subsets of proteins are selectively modified with RCS. The involvement of RCS in ROS signaling can be judged on three criteria: (1) A stimulus to increase the ROS level in plants leads to the enhancement of RCS levels. (2) Suppression of the increase of RCS by scavenging enzymes or chemicals diminishes the ROS-induced response. (3) Addition of RCS to plants evokes responses similar to those induced by ROS. On these criteria, the RCS action as damaging/signaling agents has been demonstrated for root injury, programmed cell death, senescence of siliques, stomata response to abscisic acid, and root response to auxin. RCS thus act as damage/signal mediators downstream of ROS in a variety of physiological situations. A current picture and perspectives of RCS research are presented in this article.

Significance: Jasmonate (JA) is a plant hormone involved in regulating defense response, growth, and development. A mechanistic understanding of JA signaling has great importance in agriculture, especially for enhancing plant resilience against biotic stresses and optimizing defense and growth in crop fields. This study reports the crystal structure of a key protein complex (MYC3–CMID ^JAZ10 ) involved in the desensitization of JA signaling. Desensitization of JA signaling after an effective JA response is necessary to re-establish signal homeostasis and prevent JA signaling from running out of control, which could lead to severe growth and fitness penalties. The MYC3–CMID ^JAZ10 desensitization complex structure reported here closes a major gap in our understanding of one of the most important hormone signaling pathways in plants.