Different shades of JAZ during plant growth and defense.

Abstract

Ever since their discovery as key regulators of the jasmonate (JA) signaling pathway, repressor proteins of the JASMONATE ZIM-domain (JAZ) family are rising stars in research on hormonal regulation of plant growth and defense. In plant cells, JAZ repressor proteins interact with an E3 ubiquitin ligase complex (SCFCOI1) that together functions as a JA receptor. In uninduced cells, JAZs block the activity of transcriptional regulators of JA responses by physically binding to them. Upon perception of bioactive JAs, JAZ proteins are rapidly degraded via the ubiquitin/26S proteasome-dependent proteolytic pathway. This releases the JAZ-bound transcription factors, resulting in the activation of downstream JA responses. JAs play a dominant role in regulating defense responses against herbivorous insects and necrotrophic pathogens, and in adaptive responses to beneficial soil-borne microbes. In addition, JAs have a signal function in a myriad of other processes, including abiotic stress reactions and plant growth responses to environmental cues. The JA pathway functions in the context of a complex network of hormone-regulated signaling pathways that, depending on the environmental or developmental condition, can act antagonistically or synergistically on each other to finely balance resource allocation between growth and defense and minimize fitness tradeoffs. In the process of balancing plant growth and defense, gibberellins (GAs) emerged as dominant antagonists of the JA signaling output. GAs regulate different aspects of plant growth via DELLA repressor proteins that block the activity of transcriptional regulators of GA responses by physically binding to them. Analogous to the role of JAZs in the JA pathway, DELLAs are degraded upon perception of GAs, resulting in the activation of downstream growth responses. Interestingly, DELLAs also interact with JAZs, thereby mutually limiting the cellular binding capacity to their cognate transcription factors. Consequently, GA-mediated degradation of DELLAs enhances the cellular binding capacity of JAZs to their cognate transcription factors, thus reducing the potential JA signaling output. This GA-mediated antagonistic effect on the JA pathway becomes apparent during the shade-avoidance response of plants that grow in dense vegetation stands. Shade-intolerant plant species respond to competition for light by increasing apical dominance and accelerating stem and petiole elongation. These growth and developmental responses occur in response to a drop in the red:far-red (R:FR) light ratio that is sensed by the phytochrome photoreceptors, predominantly phyB, and are GA-dependent through GA-mediated degradation of DELLA proteins. This allows them to outgrow neighboring plants, but at the cost of a reduced defensive capacity against necrotrophic pathogens and insect herbivores. In this issue of New Phytologist, Leone and co-workers zoomed in on the specific role of the Arabidopsis thaliana (Arabidopsis) JAZ10 protein in this process and shed light on the involvement of DELLAs in GA-JA crosstalk during the shade avoidance response. Besides growth-related hormones, also effector proteins of pathogens and plant growth-promoting mycorrhizal fungi have recently been shown to target JAZ repressor proteins, thereby changing the defense-related signaling circuitry for their own benefit. Hence, JAZ repressor proteins are emerging as central targets in the rewiring of the hormone-regulated signaling circuitry that regulates growth and defense.