In:
Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, Vol. 109, No. 19 ( 2012-05-08)
Abstract:
Overall, our study has revealed a potentially widely conserved mechanism, i.e., one maintained across a range of species (from rice to Arabidopsis ), by which flowering plants adjust growth rates, presumably to accommodate increased energy demand during defense against insect and pathogen attacks. Understanding this mechanism may lead to innovative methods to lessen the growth/defense conflict in crop plants so yields and defense against stresses can be augmented at the same time in agriculture. A recent report shows that several JAZ repressors physically interact with DELLA proteins in Arabidopsis ( 5 ). Hou et al. studied how gibberellin antagonizes JA signaling, providing evidence that gibberellin could inhibit JA signaling through DELLA-mediated interference with the JAZ–MYC2 interaction ( 5 ). We also observed multiple JAZ–DELLA interactions based on a number of plant- or yeast-based assays. Most strikingly, in our study, we found that the ability of JAZ overexpression (a procedure that mimics coi1 mutations) to confer gibberellin hypersensitivity-like phenotypes was correlated with the ability of specific JAZ proteins to physically interact with DELLA proteins. Because DELLA proteins physically interact and repress growth-promoting transcription factors, such as the PIF-family proteins in Arabidopsis ( 4 ), we investigated the possibility that JAZ repressors may impede the DELLA–PIF interaction. Indeed, we found that JAZ9 could effectively inhibit PIF3 interaction with RGA in yeast and plant cells. Furthermore, overexpression of PIF3 alone was sufficient to partially counter JA-induced inhibition of hypocotyl growth, whereas the pif quadruple mutant ( pifq ) was no longer able to respond to JA-mediated inhibition of hypocotyl growth. Thus, JAZ repressors interfere with one of the most important steps in gibberellin signaling: the DELLA–PIF interaction. How does removal of the JA receptor COI1 potentiate gibberellin signaling? Because the stability of DELLA repressors is the key to gibberellin signaling ( 4 ) ( Fig. P1 ), we investigated the level of the DELLA repressors (SLR1 in rice and RGA in Arabidopsis ) in coi1 mutants and/or in response to JA treatment. We found that, in rice, the SLR1 level was significantly lower in the absence of COI1. Conversely, JA treatment increased DELLA protein levels and slowed gibberellin-induced DELLA degradation. These results suggest that activation of JA signaling stabilizes DELLA repressors. Our study began with the observation that, when the two COI1 genes were silenced in rice (a model crop plant), the plants exhibited several hallmark phenotypes of gibberellin hypersensitivity, including increased height, elongated internodes, faster germination, and hypersensitivity to exogenous gibberellin. Furthermore, we found that the gibberellin receptor GID1 is required for the gibberellin hypersensitivity of COI1 -silenced rice plants. Similarly, coi1 mutants in Arabidopsis , another common experimental plant, exhibit several phenotypes that resemble gibberellin hypersensitivity, including elongated petioles (i.e., stalks attaching leaf blades to the stem) and hypocotyls (i.e., stems of germinating seedlings) and early flowering. Collectively, these results suggest that removal of the JA receptor COI1 enhances gibberellin signaling in both monocot (i.e., rice) and dicot (i.e., Arabidopsis ) plants. JA defense signaling requires the coronatine insensitive 1 (COI1)–JA ZIM domain (JAZ)–MYC core signaling module. The COI1 protein is a substrate-recognition component of an E3 ubiquitin ligase, which adds a ubiquitin molecule to specific substrate proteins. Ubiquitin-tagged proteins are subsequently degraded by the proteasome, a major protein-degradation nanomachine in eukaryotic cells. Recent studies show that COI1 is a principal component of a receptor for JA, and that the JAZ-family transcriptional repressor proteins are the substrate proteins of the COI-associated E3 ubiquitin ligase ( Fig. P1 ). At rest, JAZ proteins repress the transcription of JA-responsive genes through direct interaction with defense-associated transcription factors, such as MYC2 ( 1 , 2 ). Bioactive JA promotes physical interaction between the COI1 protein and JAZ proteins, which results in the degradation of JAZs, thereby initiating JA responses. In an analogous signaling cascade, active gibberellin binds to the GID1 receptor, which, in turn, interacts with the DELLA family transcriptional repressors ( 3 , 4 ). The DELLA repressors are recognized and ubiquitinated by the SLY1-associated E3 ubiquitin ligase, leading to degradation of DELLA proteins through the proteasome. Degradation of DELLA repressors relieves the DELLA-imposed repression of downstream transcription factors, including phytochrome interacting factors (PIFs), thereby activating gibberellin responses ( 4 ). Organisms must effectively defend against biotic and abiotic stresses to survive in nature. However, this defense is costly, and, to efficiently allocate limited energy resources, organisms often slow down growth during defense activation. The coordination of this tradeoff is not well understood, however. In plants, hormones called gibberellin and jasmonate (JA) are essential for regulating growth and defense against stresses, respectively. Activation of JA defense signaling is associated with significant growth inhibition. In this study, we elucidated a potentially widespread molecular mechanism by which flowering plants prioritize JA-mediated defense over growth.
Type of Medium:
Online Resource
ISSN:
0027-8424
,
1091-6490
DOI:
10.1073/pnas.1201616109
Language:
English
Publisher:
Proceedings of the National Academy of Sciences
Publication Date:
2012
detail.hit.zdb_id:
209104-5
detail.hit.zdb_id:
1461794-8
SSG:
11
SSG:
12
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