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Cloning and characterization of a MeJA-responsive jasmonate ZIM-domain gene (SmJAZ1) from Salvia miltiorrhiza Bunge

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Abstract

Methyl jasmonate (MeJA) has an important role in modulating the accumulation of secondary metabolites in Salvia miltiorrhiza Bunge. However, little research has been reported on genes involved in the JA signaling pathway in this species. Jasmonate ZIM-domain (JAZ) transcriptional repressors are the key regulators of the hormonal response. We cloned a novel JAZ gene, SmJAZ1, from S. miltiorrhiza by screening its transcriptome database. Its full-length sequence is 2024 bp long, including a 1308-bp promoter, and comprises two introns and three exons that encode a polypeptide of 180 amino acid residues. The predicted SmJAZ1 contains the ZIM domain and Jas domain, which are highly conserved regions in the JAZ family. Most JAZ genes can be induced by treatment with MeJA or wounding, a phenomenon that is characteristic of JAZs. Similar to other JAZ genes, our real-time quantitative PCR analysis showed that SmJAZ1 expression increased rapidly, by 2.1-fold, within 1 h after MeJA treatment. It was also strongly induced, to 6.0-fold, within 0.5 h after wounding. Therefore, we believe that this gene is a member of the JAZ family. Although it was detected in four tissues examined here, expression was significantly elevated in the stems and leaves. This gene also responded to treatments with other phytohormones and plant growth regulators (ABA, gibberellin, naphthalene acetic acid, and salicylic acid) and to low-temperature stress. The results obtained provide general characteristics for SmJAZ1 and contribute to our understanding of the jasmonate signaling pathway in S. miltiorrhiza.

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Abbreviations

COI1 :

Coronatine Insensitive 1

GA3 :

gibberellins

JA:

jasmonic acid

JAZ:

jasmonate ZIM-domain

MeJA:

methyl jasmonate

ORF:

open reading frame

PAC:

paclobutrazol

SA:

salicylic acid

TF:

transcription factor

References

  1. Rao, M.V., Lee, H., Creelman, R.A., Mullet, J.E., and Davis, K.R., Jasmonic acid signaling modulates ozone-induced hypersensitive cell death, Plant Cell, 2000, vol. 12, pp. 1633–1646.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  2. Browse, J. and Howe, G.A., New weapons and a rapid response against insect attack, Plant Physiol., 2008, vol. 146, pp. 832–838.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  3. Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Pichersky, E., and Howe, G.A., The tomato homolog of CORONATINE-INSENSITIVE1 required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development, Plant Cell Online, 2004, vol. 16, pp. 126–143.

    Article  CAS  Google Scholar 

  4. Shoji, T., Ogawa, T., and Hashimoto, T., Jasmonate-induced nicotine formation in tobacco is mediated by tobacco COI1 and JAZ genes, Plant Cell Physiol., 2008, vol. 49, pp. 1003–1012.

    Article  PubMed  CAS  Google Scholar 

  5. Feys, B., Benedetti, C.E., Penfold, C.N., and Turner, J.G., Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen, Plant Cell, 1994, vol. 6, pp. 751–759.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  6. Chini, A., Fonseca, S., Fernández, G., Adie, B., Chico, J.M., Lorenzo, O., Garcia-Casado, G., López-Vidriero, I., Lozano, F.M., Ponce, M.R., Micol, J.L., and Solano, R., The JAZ family of repressors is the missing link in jasmonate signalling, Nature, 2007, vol. 448, pp. 666–671.

    Article  PubMed  CAS  Google Scholar 

  7. Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A., and Browse, J., JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling, Nature, 2007, vol. 448, pp. 661–665.

    Article  PubMed  CAS  Google Scholar 

  8. Kazan, K. and Manners, J.M., JAZ repressors and the orchestration of phytohormone crosstalk, Trends Plant Sci., 2011, vol. 17, pp. 21–31.

    Google Scholar 

  9. Yang, D.L., Yao, J., Mei, C.S., Tong, X.H., Zeng, L.J., Li, Q., Xiao, L.T., Sun, T.P., Li, J., Deng, X.W., Lee, C.M., Thomashow, M.F., Yang, Y., He, Z., and He, S.Y., Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade, Proc. Natl. Acad. Sci. USA, 2012, vol. 109, pp. 1192–1200.

    Article  Google Scholar 

  10. Dombrecht, B., Xue, G.P., Sprague, S.J., Kirkegaard, J.A., Ross, J.J., Reid, J.B., Fitt, G.P., Sewelam, N., Schenk, P.M., Manners, J.M., and Kazan, K., MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis, Plant Cell Online, 2007, vol. 19, pp. 2225–2245.

    Article  CAS  Google Scholar 

  11. Qi, T., Song, S., Ren, Q., Wu, D., Huang, H., Chen, Y., Fan, M., Peng, W., Ren, C., and Xie, D., 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 Online, 2011, vol. 23, pp. 1795–1814.

    Article  CAS  Google Scholar 

  12. De Boer, K., Tilleman, S., Pauwels, L., van den Bossche, R., de Sutter, V., Vanderhaeghen, R., Hilson, P., Hamill, J.D., and Goossens, A., APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis, Plant J., 2011, vol. 66, pp. 1053–1065.

    Article  PubMed  Google Scholar 

  13. Seo, J.S., Joo, J., Kim, M.J., Kim, Y.K., Nahm, B.H., Song, S.I., Cheong, J.J., Lee, J.S., Kim, J.K., and Choi, Y.D., OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice, Plant J., 2011, vol. 65, pp. 907–921.

    Article  PubMed  CAS  Google Scholar 

  14. Ismail, A., Riemann, M., and Nick, P., The jasmonate pathway mediates salt tolerance in grapevines, J. Exp. Bot., 2012, vol. 63, pp. 2127–2139.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  15. Han, J.Y., Fan, J.Y., Horie, Y., Miura, S., Cui, D.H., Ishii, H., Hibi, T., Tsuneki, H., and Kimura, I., Ameliorating effects of compounds derived from Salvia miltiorrhiza root extract on microcirculatory disturbance and target organ injury by ischemia and reperfusion, Pharmacol. Therapeut., 2008, vol. 117, pp. 280–295.

    Article  CAS  Google Scholar 

  16. Zhao, J.L., Zhou, L.G., and Wu, J.Y., Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures, Appl. Microbiol. Biotechnol., 2010, vol. 87, pp. 137–144.

    Article  PubMed  CAS  Google Scholar 

  17. Yang, D., Ma, P., Liang, X., Liang, Z., Liu, Y., and Liu, F., PEG and ABA trigger methyl jasmonate accumulation to induce the MEP pathway and increase tanshinone production in Salvia miltiorrhiza hairy roots, Physiol. Plant., 2012, vol. 146, pp. 173–183.

    Article  PubMed  CAS  Google Scholar 

  18. Xiao, Y., Gao, S., Di, P., Chen, J., Chen, W., and Zhang, L., Methyl jasmonate dramatically enhances the accumulation of phenolic acids in Salvia miltiorrhiza hairy root cultures, Physiol. Plant., 2009, vol. 137, pp. 1–9.

    Article  PubMed  CAS  Google Scholar 

  19. Doyle, J.J. and Doyle, J.L., A rapid DNA isolation procedure from small quantities of fresh leaf tissue, Phytochem. Bull., 1987, vol. 19, pp. 11–15.

    Google Scholar 

  20. Hua, W., Zhang, Y., Song, J., Zhao, L., and Wang, Z., De novo transcriptome sequencing in Salvia miltiorrhiza to identify genes involved in the biosynthesis of active ingredients, Genomics, 2011, vol. 98, pp. 272–279.

    Article  CAS  Google Scholar 

  21. Song, J. and Wang, Z., Molecular cloning, expression and characterization of a phenylalanine ammonialyase gene (SmPAL1) from Salvia miltiorrhiza, Mol. Biol. Rep., 2008, vol. 36, pp. 939–952.

    Article  PubMed  Google Scholar 

  22. Figueroa, P. and Browse, J., The Arabidopsis JAZ2 promoter contains a G-Box and thymidine-rich module that are necessary and sufficient for jasmonate-dependent activation by MYC transcription factors and repression by JAZ proteins, Plant Cell Physiol., 2012, vol. 53, pp. 330–343.

    Article  PubMed  CAS  Google Scholar 

  23. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and Lohmann, J.U., A gene expression map of Arabidopsis thaliana development, Nat. Genet., 2005, vol. 37, pp. 501–506.

    Article  PubMed  CAS  Google Scholar 

  24. Chung, H.S., Koo, A.J., Gao, X., Jayanty, S., Thines, B., Jones, A.D., and Howe, G.A., Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory, Plant Physiol., 2008, vol. 146, pp. 952–964.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  25. Zhang, H.B., Bokowiec, M.T., Rushton, P.J., Han, S.C., and Timko, M.P., Tobacco transcription factors NtMYC2a and NtMYC2b form nuclear complexes with the NtJAZ1 repressor and regulate multiple jasmonate-inducible steps in nicotine biosynthesis, Mol. Plant, 2011, vol. 5, pp. 73–84.

    Article  PubMed  CAS  Google Scholar 

  26. Bai, Y., Meng, Y., Huang, D., Qi, Y., and Chen, M., Origin and evolutionary analysis of the plant-specific TIFY transcription factor family, Genomics, 2011, vol. 98, pp. 128–136.

    Article  PubMed  CAS  Google Scholar 

  27. Hou, X., Lee, L.Y.C., Xia, K., Yan, Y., and Yu, H., DELLAs modulate jasmonate signaling via competitive binding to JAZs, Dev. Cell, 2010, vol. 19, pp. 884–894.

    Article  PubMed  CAS  Google Scholar 

  28. Leon-Reyes, A., van der Does, D., de Lange, E.S., Delker, C., Wasternack, C., van Wees, S.C., Ritsema, T., and Pieterse, C.M., Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway, Planta, 2010, vol. 232, pp. 1423–1432.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. Grunewald, W., Vanholme, B., Pauwels, L., Plovie, E., Inzé, D., Gheysen, G., and Goossens, A., Expression of the Arabidopsis jasmonate signalling repressor JAZ1/TIFY10A is stimulated by auxin, EMBO Rep., 2009, vol. 10, pp. 923–928.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Correspondence to Z. Z. Wang.

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Ge, Q., Xiao, Y.P. & Wang, Z.Z. Cloning and characterization of a MeJA-responsive jasmonate ZIM-domain gene (SmJAZ1) from Salvia miltiorrhiza Bunge. Russ J Plant Physiol 61, 862–872 (2014). https://doi.org/10.1134/S1021443714060065

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