bHLH17 Negatively Regulates Jasmonate-mediated Plant Defense Responses

doi:10.3724/SP.J.1259.2014.00643

Abstract

Abstract: The plant hormone jasmonate (JA) functions as a defense signal to regulate plant defense against insect attack and pathogen infection. It also acts as a developmental signal to regulate plant development and growth, including root growth, stamen development, trichome initiation, and leaf senescence. The JA receptor CORONATINE INSENSITIVE1 (COI1) perceives JA signals for interaction with JASMONATE-ZIM-DOMAIN (JAZ) proteins and subsequent ubiquitination of JAZs, thereby regulating the JA responses. The single mutants of the bHLH subgroup IIId factors (bHLH3, bHLH13, bHLH14 and bHLH17), which interact with JAZs, show no obvious phenotype in resistance to the fungus Botrytis cinerea and defense against the herbivore Spodoptera exigua. However, the quadruple mutant shows enhanced resistance to B. cinerea and defense against S. exigua. We investigated whether the overexpression of bHLH17 in Arabidopsis affected the resistance to B. cinerea and defense against S. exigua. Similar to the JA receptor mutant coi1-1, Arabidopsis bHLH17-overexpressing plants were more susceptible to B. cinerea and S. exigua than the wild type. As compared with the wild type, bHLH17 overexpression attenuated the JA-inducible expression of defense- or wounding-related genes, such as Thi2.1, VSP2, AOS, JAZ1, JAZ9 and JAZ10. Further transient expression analysis revealed that the N-terminus of bHLH17 was essential for its transcriptional repression function. Overexpression of bHLH17 negatively regulates plant defense against B. cinerea and S. exigua.

Cuili Wang, Haixia Tian, Jiaojiao Wang, Tiancong Qi, Huang Huang, Chunmei Ren, Daoxin Xie, Susheng Song. bHLH17 Negatively Regulates Jasmonate-mediated Plant Defense Responses[J]. Chinese Bulletin of Botany, 2014, 49(6): 643-652.

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References

Bohlmann, H., Vignutelli, A., Hilpert, B., Miersch, O., Wasternack, C., and Apel, K. (1998). Wounding and chemicals induce expression of the Arabidopsis thaliana gene Thi2.1, encoding a fungal defense thionin, via the octadecanoid pathway. FEBS Lett 437: 281-286.
Chen, Q., Sun, J., Zhai, Q., Zhou, W., Qi, L., Xu, L., Wang, B., Chen, R., Jiang, H., Qi, J., Li, X., Palme, K., and Li, C. (2011). The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23: 3335-3352.
Cheng, Z., Sun, L., Qi, T., Zhang, B., Peng, W., Liu, Y., and Xie, D. (2011). The bHLH Transcription Factor MYC3 Interacts with the Jasmonate ZIM-Domain Proteins to Mediate Jasmonate Response in Arabidopsis. Mol. Plant 4: 279-288.
Chini, A., Fonseca, S., Fernandez, G., Adie, B., Chico, J.M., Lorenzo, O., Garcia-Casado, G., Lopez-Vidriero, I., Lozano, F.M., Ponce, M.R., Micol, J.L., and Solano, R. (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671.
Chung, H.S., Koo, A.J., Gao, X., Jayanty, S., Thines, B., Jones, A.D., and Howe, G.A. (2008). Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol. 146: 952-964.
Fedina, I., Nedeva, D., Georgieva, K., and Velitchkova, M. (2009). Methyl Jasmonate Counteract UV-B Stress in Barley Seedlings. Journal of Agronomy and Crop Science 195: 204-212.
Fernandez-Calvo, P., Chini, A., Fernandez-Barbero, G., Chico, J.M., Gimenez-Ibanez, S., Geerinck, J., Eeckhout, D., Schweizer, F., Godoy, M., Franco-Zorrilla, J.M., Pauwels, L., Witters, E., Puga, M.I., Paz-Ares, J., Goossens, A., Reymond, P., De Jaeger, G., and Solano, R. (2011). The Arabidopsis bHLH Transcription Factors MYC3 and MYC4 Are Targets of JAZ Repressors and Act Additively with MYC2 in the Activation of Jasmonate Responses. Plant Cell 23: 701-715.
Feys, B.J.F., Benedetti, C.E., Penfold, C.N., and Turner, J.G. (1994). Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male-sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751-759.
Fonseca, S., Chini, A., Hamberg, M., Adie, B., Porzel, A., Kramell, R., Miersch, O., Wasternack, C., and Solano, R. (2009). (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5: 344-350.
Guo, S., Xu, Y., Liu, H., Mao, Z., Zhang, C., Ma, Y., Zhang, Q., Meng, Z., and Chong, K. (2013). The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat Commun 4: 1566.
Hong, G.J., Xue, X.Y., Mao, Y.B., Wang, L.J., and Chen, X.Y. (2012). Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24: 2635-2648.
Liu, Y., Ahn, J.E., Datta, S., Salzman, R.A., Moon, J., Huyghues-Despointes, B., Pittendrigh, B., Murdock, L.L., Koiwa, H., and Zhu-Salzman, K. (2005). Arabidopsis vegetative storage protein is an anti-insect acid phosphatase. Plant Physiol 139: 1545-1556.
Lorenzo, O., Chico, J.M., Sanchez-Serrano, J.J., and Solano, R. (2004). JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938-1950.
Mason, H.S., and Mullet, J.E. (1990). Expression of two soybean vegetative storage protein genes during development and in response to water deficit, wounding, and jasmonic acid. Plant Cell 2: 569-579.
McConn, M., and Browse, J. (1996). The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8: 403-416.
McConn, M., Creelman, R.A., Bell, E., Mullet, J.E., and Browse, J. (1997). Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 94: 5473-5477.
Nakata, M., Mitsuda, N., Herde, M., Koo, A.J., Moreno, J.E., Suzuki, K., Howe, G.A., and Ohme-Takagi, M. (2013). A bHLH-Type Transcription Factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, Acts as a Repressor to Negatively Regulate Jasmonate Signaling in Arabidopsis. Plant Cell 25: 1641-1656.
Niu, Y., Figueroa, P., and Browse, J. (2011). Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot 62: 2143-2154.
Park, J.H., Halitschke, R., Kim, H.B., Baldwin, I.T., Feldmann, K.A., and Feyereisen, R. (2002). A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J. 31: 1-12.
Qi, T., Song, S., Ren, Q., Wu, D., Huang, H., Chen, Y., Fan, M., Peng, W., Ren, C., and Xie, D. (2011). The Jasmonate-ZIM-Domain Proteins Interact with the WD-Repeat/bHLH/MYB Complexes to Regulate Jasmonate-Mediated Anthocyanin Accumulation and Trichome Initiation in Arabidopsis thaliana. Plant Cell 23: 1795-1814.
Rao, M.V., Lee, H., Creelman, R.A., Mullet, J.E., and Davis, K.R. (2000). Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12: 1633-1646.
Santner, A., and Estelle, M. (2007). The JAZ proteins link jasmonate perception with transcriptional changes. Plant Cell 19: 3839-3842.
Schommer, C., Palatnik, J.F., Aggarwal, P., Chetelat, A., Cubas, P., Farmer, E.E., Nath, U., and Weigel, D. (2008). Control of jasmonate biosynthesis and senescence by miR319 targets. PloS Biol. 6: e230.
Schweizer, F., Fernandez-Calvo, P., Zander, M., Diez-Diaz, M., Fonseca, S., Glauser, G., Lewsey, M.G., Ecker, J.R., Solano, R., and Reymond, P. (2013). Arabidopsis Basic Helix-Loop-Helix Transcription Factors MYC2, MYC3, and MYC4 Regulate Glucosinolate Biosynthesis, Insect Performance, and Feeding Behavior. Plant Cell.
Shan, X., Wang, J., Chua, L., Jiang, D., Peng, W., and Xie, D. (2011). A role of Arabidopsis Rubisco activase in jasmonate-induced leaf senescence. Plant Physiol. 155: 751-764.
Song, S., Qi, T., Fan, M., Zhang, X., Gao, H., Huang, H., Wu, D., Guo, H., and Xie, D. (2013). The bHLH Subgroup IIId Factors Negatively Regulate Jasmonate-Mediated Plant Defense and Development. PLoS Genet 9: e1003653.
Song, S., Qi, T., Huang, H., Ren, Q., Wu, D., Chang, C., Peng, W., Liu, Y., Peng, J., and Xie, D. (2011). The Jasmonate-ZIM Domain Proteins Interact with the R2R3-MYB Transcription Factors MYB21 and MYB24 to Affect Jasmonate-Regulated Stamen Development in Arabidopsis. Plant Cell 23: 1000-1013.
Thomma, B.P., Eggermont, K., Penninckx, I.A., Mauch-Mani, B., Vogelsang, R., Cammue, B.P., and Broekaert, W.F. (1998). Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci U S A 95: 15107-15111.
Toledo-Ortiz, G., Huq, E., and Quail, P.H. (2003). The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15: 1749-1770.
Wasternack, C., and Hause, B. (2013). Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot.
Xie, D.X., Feys, B.F., James, S., Nieto-Rostro, M., and Turner, J.G. (1998). COI1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280: 1091-1094.
Yan, J., Zhang, C., Gu, M., Bai, Z., Zhang, W., Qi, T., Cheng, Z., Peng, W., Luo, H., Nan, F., Wang, Z., and Xie, D. (2009). The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21: 2220-2236.
Yan, Y.X., Stolz, S., Chetelat, A., Reymond, P., Pagni, M., Dubugnon, L., and Farmer, E.E. (2007). A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19: 2470-2483.
Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572.
Yoshida, Y., Sano, R., Wada, T., Takabayashi, J., and Okada, K. (2009). Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development 136: 1039-1048.
Zhai, Q., Yan, L., Tan, D., Chen, R., Sun, J., Gao, L., Dong, M.Q., Wang, Y., and Li, C. (2013). Phosphorylation-Coupled Proteolysis of the Transcription Factor MYC2 Is Important for Jasmonate-Signaled Plant Immunity. PLoS Genet 9: e1003422.
Zhang, H.B., Bokowiec, M.T., Rushton, P.J., Han, S.C., and Timko, M.P. (2012). Tobacco transcription factors NtMYC2a and NtMYC2b form nuclear complexes with the NtJAZ1 repressor and regulate multiple jasmonate-inducible steps in nicotine biosynthesis. Mol Plant 5: 73-84.
Zhu, Z., An, F., Feng, Y., Li, P., Xue, L., A, M., Jiang, Z., Kim, J.M., To, T.K., Li, W., Zhang, X., Yu, Q., Dong, Z., Chen, W.Q., Seki, M., Zhou, J.M., and Guo, H. (2011). Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108: 12539-12544.