Plant Hormone Jasmonate Prioritizes Defense Over Growth by Interfering with Gibberellin Signaling Cascade

Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade

Dong-Lei Yanga,1, Jian Yaob,c,1, Chuan-Sheng Meid,1,2, Xiao-Hong Tonga, Long-Jun Zenga, Qun Lia, Lang-Tao Xiaoe, Tai-ping Sunf, Jigang Lig, Xing-Wang Dengg, Chin Mei Leeb, Michael F. Thomashowb, Yinong Yangd,h,3, Zuhua Hea,3, and Sheng Yang Heb,c,3 aNational Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China; bDepartment of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824; cHoward Hughes Medical Institute, Chevy Chase, MD 20815; dDepartment of Plant Pathology, University of Arkansas, Fayetteville, AR 72701; eHunan Provincial Key Laboratory of Phytohormones, Hunan Agricultural University, Changsha 410128, China; fDepartment of Biology, Duke University, Durham, NC 27705; gDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520; and hDepartment of Plant Pathology and Huck Institutes of Life Sciences, Pennsylvania State University, University Park, PA 16802 AUTHOR SUMMARY

Organisms must effectively de- stream transcription factors, in- Block of jasmonate signaling Activation of jasmonate signaling fend against biotic and abiotic A (coi1 mutant or JAZ overexpression) B (Insect and pathogen attacks) cluding phytochrome interacting stresses to survive in nature. factors (PIFs), thereby activating However, this defense is costly, gibberellin responses (4). and, to efficiently allocate lim- Defense Growth Defense Growth Our study began with the ob- ited energy resources, organisms servation that, when the two often slow down growth during monocot dicot monocot dicot COI1 genes were silenced in rice (a model crop plant), the plants defense activation. The co- Gibberellin Jasmonate ordination of this tradeoff is not Gibberellin Jasmonate exhibited several hallmark phe- GID1 notypes of gibberellin hypersen- well understood, however. In COI1 plants, hormones called gibber- GID1 COI1 sitivity, including increased DELLA JAZ DELLA height, elongated internodes, ellin and jasmonate (JA) are JAZ JAZ faster germination, and hyper- essential for regulating growth JAZ PIF MYC sensitivity to exogenous gibber- and defense against stresses, re- MYC PIF ellin. Furthermore, we found spectively. Activation of JA de- Growth Defense that the gibberellin receptor fense signaling is associated with Growth Defense significant growth inhibition. In GID1 is required for the gibberellin hypersensitivity of this study, we elucidated a po- Fig. P1. A model illustrating how JA signaling modulates plant growth COI1 tentially widespread molecular -silenced rice plants. Simi- through antagonizing gibberellin signaling. (A)Incoi1 mutant or JAZ- larly, coi1 mutants in Arabi- mechanism by which flowering overexpressing plants, JA signaling is down-regulated. Accumulated dopsis, another common plants prioritize JA-mediated JAZ repressors titrate DELLA repressors away from PIF transcription experimental plant, exhibit sev- defense over growth. factors, allowing more PIFs to activate growth-promoting genes, eral phenotypes that resemble JA defense signaling requires thereby enhancing growth. (B) Activation of JA signaling in WT plants upon insect or pathogen attacks results in degradation of JAZ repressors gibberellin hypersensitivity, in- the coronatine insensitive 1 – and accumulation of DELLA repressors, collectively allowing more cluding elongated petioles (i.e., (COI1) JA ZIM domain DELLA repressors to inhibit PIF transcription factors, thereby slowing – stalks attaching leaf blades to (JAZ) MYC core signaling growth. Normal JA and gibberellin signaling components are depicted the stem) and hypocotyls (i.e., module. The COI1 protein is in red and green, respectively, whereas components with reduced stems of germinating seedlings) a substrate-recognition compo- level and/or activity are indicated in white. Upward arrows indicate and early flowering. Collectively, nent of an E3 ubiquitin ligase, increased level and/or activity, whereas downward arrows indicate reduced level and/or activity. Dashed lines indicate weakened effects. these results suggest that re- which adds a ubiquitin molecule moval of the JA receptor COI1 fi to speci c substrate proteins. enhances gibberellin signaling in Ubiquitin-tagged proteins are subsequently degraded by the proteasome, a major protein-

degradation nanomachine in eukaryotic cells. Recent studies Author contributions: D.-L.Y., J.Y., C.-S.M., Y.Y., Z.H., and S.Y.H. designed research; D.-L.Y., show that COI1 is a principal component of a receptor for JA, J.Y., C.-S.M., X.-H.T., L.-J.Z., L.-T.X., Y.Y., and Z.H. performed research; C.-S.M., Q.L., T.-p.S., J.L., and that the JAZ-family transcriptional repressor proteins are X.-W.D., C.M.L., M.F.T., Y.Y., Z.H., and S.Y.H. contributed new reagents/analytic tools; D.-L.Y., J.Y., C.-S.M., Y.Y., Z.H., and S.Y.H. analyzed data; and D.-L.Y., J.Y., C.-S.M., Y.Y., the substrate proteins of the COI-associated E3 ubiquitin ligase Z.H., and S.Y.H. wrote the paper. (Fig. P1). At rest, JAZ proteins repress the transcription of JA- The authors declare no conﬂict of interest. responsive genes through direct interaction with defense-asso- This article is a PNAS Direct Submission. ciated transcription factors, such as MYC2 (1, 2). Bioactive JA Data deposition: The data reported in this paper have been deposited in the Gene Ex- promotes physical interaction between the COI1 protein and pression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession nos. GSE29577 JAZ proteins, which results in the degradation of JAZs, thereby and GSM732294–GSM732299). initiating JA responses. In an analogous signaling cascade, active 1D.-L.Y., J.Y., and C.-S.M. contributed equally to this work. gibberellin binds to the GID1 receptor, which, in turn, interacts 2Present address: Institute for Sustainable and Renewable Resources, Institute for Ad- with the DELLA family transcriptional repressors (3, 4). The vanced Learning and Research, Danville, VA 24540. DELLA repressors are recognized and ubiquitinated by the 3To whom correspondence may be addressed. E-mail: [email protected], [email protected], or SLY1-associated E3 ubiquitin ligase, leading to degradation of [email protected]. DELLA proteins through the proteasome. Degradation of DELLA See full research article on page E1192 of www.pnas.org. repressors relieves the DELLA-imposed repression of down- Cite this Author Summary as: PNAS 10.1073/pnas.1201616109.

7152–7153 | PNAS | May 8, 2012 | vol. 109 | no. 19 www.pnas.org/cgi/doi/10.1073/pnas.1201616109 Downloaded by guest on September 26, 2021 both monocot (i.e., rice) and dicot (i.e., Arabidopsis) plants. teraction with RGA in yeast and plant cells. Furthermore, PNAS PLUS How does removal of the JA receptor COI1 potentiate gib- overexpression of PIF3 alone was sufficient to partially counter berellin signaling? Because the stability of DELLA repressors is JA-induced inhibition of hypocotyl growth, whereas the pif the key to gibberellin signaling (4) (Fig. P1), we investigated the quadruple mutant (pifq) was no longer able to respond to JA- level of the DELLA repressors (SLR1 in rice and RGA in mediated inhibition of hypocotyl growth. Thus, JAZ repressors Arabidopsis coi1 )in mutants and/or in response to JA treatment. interfere with one of the most important steps in gibberellin fi We found that, in rice, the SLR1 level was signi cantly lower signaling: the DELLA–PIF interaction. in the absence of COI1. Conversely, JA treatment increased Overall, our study has revealed a potentially widely conserved DELLA protein levels and slowed gibberellin-induced DELLA mechanism, i.e., one maintained across a range of species (from degradation. These results suggest that activation of JA signaling rice to Arabidopsis), by which flowering plants adjust growth stabilizes DELLA repressors. rates, presumably to accommodate increased energy demand A recent report shows that several JAZ repressors physically during defense against insect and pathogen attacks. Under- interact with DELLA proteins in Arabidopsis (5). Hou et al. standing this mechanism may lead to innovative methods to studied how gibberellin antagonizes JA signaling, providing fl evidence that gibberellin could inhibit JA signaling through lessen the growth/defense con ict in crop plants so yields and DELLA-mediated interference with the JAZ–MYC2 interaction defense against stresses can be augmented at the same time (5). We also observed multiple JAZ–DELLA interactions based in agriculture. on a number of plant- or yeast-based assays. Most strikingly, in our study, we found that the ability of JAZ overexpression (a 1. Pauwels L, Goossens A (2011) The JAZ proteins: A crucial interface in the jasmonate coi1 signaling cascade. Plant Cell 23:3089–3100. procedure that mimics mutations) to confer gibberellin hy- 2. Browse J (2009) Jasmonate passes muster: A receptor and targets for the defense persensitivity-like phenotypes was correlated with the ability of hormone. Annu Rev Plant Biol 60:183–205. specific JAZ proteins to physically interact with DELLA pro- 3. Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA teins. Because DELLA proteins physically interact and repress growth regulatory mechanism: How an “inhibitor of an inhibitor” enables flexible growth-promoting transcription factors, such as the PIF-family response to fluctuating environments. Plant Cell 21:1328–1339. Arabidopsis 4. Sun TP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA proteins in (4), we investigated the possibility that signaling module in plants. Curr Biol 21:R338–R345. JAZ repressors may impede the DELLA–PIF interaction. In- 5. Hou X, Lee LYC, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via deed, we found that JAZ9 could effectively inhibit PIF3 in- competitive binding to JAZs. Dev Cell 19:884–894. PLANT BIOLOGY

Yang et al. PNAS | May 8, 2012 | vol. 109 | no. 19 | 7153 Downloaded by guest on September 26, 2021