biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 60:715-723, 2016 | DOI: 10.1007/s10535-016-0652-0

Cloning, characterization, and subcellular localization of a novel JAZ repressor from Eleusine coracana

S. Sen1,*, S. K. Dutta1
1 Drug Development/Diagnostics and Biotechnology Division, CSIR - Indian Institute of Chemical Biology, Kolkata, India

Jasmonate ZIM domain (JAZ) proteins are key regulators of the jasmonic acid (JA) signaling pathway. Repressors of JAZ remain bound to the myelocytomatosis 2 (MYC2) or MYC3/MYC4 transcription factors in the absence of JA and negatively regulate transcription of the JA responsive genes. In the presence of JA, JAZ proteins interact with coronative insensitive 1 (COI1), the recognition molecule of E3 ubiquitin ligase SCFCOI1 (COI1 stabilized by Skp, cullin, F-box containing complex), get ubiquitinated, and subsequently degraded by the 26S proteasome. However, there is a dearth of knowledge about this gene family in monocot cereals, specifically its role in finger millet is unknown till date. Here we present the isolation and characterization of a novel JAZ family repressor gene from nonsequenced Eleusine coracana (EcJAZ) utilizing available genome information of Oryza, Sorghum, and Setaria. The EcJAZ sequence showed the presence of a conserved ZIM domain, the Jas motif, and N-terminal motif 7 like other Group1 TIFY sequence containing proteins. We observed coronatine (an analog of JA-Ile) dependent and time dependent degradation of recombinant EcJAZ that thereby fulfilled the basic characteristic of the JAZ proteins. We found a proteasome inhibitor N-(phenylmethoxy) carbonyl-L-leucyl-N-[(1R)-1-formyl-3-methylbutyl]-L-leucinamide) (MG132) mediated degradation inhibition of EcJAZ that supported its 26S proteasome mediated degradation. Our study shows the nuclear localization of GFP-EcJAZ by Agrobacterium mediated transient transformation of onion scale epidermal cells. In Eleusine leaves, transcription of EcJAZ increased 4.2-fold by salt stress and 5.5-fold by coronatine application; thus ascertained its inducibility by the abiotic stress as well as by bioactive JA-Ile. Taken together, all these results contribute to our understanding of the JA signaling pathway in Eleusine coracana.

Keywords: Agrobacterium transformation; coronatine; finger millet; jasmonic acid; salt stress
Subjects: jasmonate ZIM domain; coronatine; jasmonic acid; salt stress; phylogenetic tree; salicylic acid; water stress; finger millet; onion epidermis

Received: May 8, 2015; Revised: January 18, 2016; Accepted: March 14, 2016; Published: December 1, 2016  Show citation

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Sen, S., & Dutta, S.K. (2016). Cloning, characterization, and subcellular localization of a novel JAZ repressor from Eleusine coracana. Biologia plantarum, 60(4), 715-723. doi: 10.1007/s10535-016-0652-0
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    References

    1. Bai, Y., Meng, Y., Huang, D., Qi, Y., Chen, M.: Origin and evolutionary analysis of the plant specific TIFY transcription factor family. - Genomics 98: 128-136, 2011. Go to original source...
    2. Barbeau, W.E., Hilu, K.W.: Protein, calcium, iron, and amino acid content of selected wild and domesticated cultivars of finger millet. - Plant Foods Human Nutr. 43: 97-104, 1993. Go to original source...
    3. Bender, C.L., Alarcon-Chaidez, F., Gross, D.C.: Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. - Microbiol. mol. Biol. Rev. 63: 266-292, 1999. Go to original source...
    4. Browse, J.: Jasmonate passes muster: a receptor and targets for the defense hormone. - Annu. Rev. Plant Biol. 60: 183-205, 2009. Go to original source...
    5. Cheng, Z., Sun, L., Qi, T., Zhang, B., Peng, W., Liu, Y., Xie, D.: The bHLH transcription factor MYC3 interacts with the jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis. - Mol. Plants 4: 279-288, 2011. Go to original source...
    6. Chini, A., Fonseca, S., Fernández, G., Adie, B., Chico, J.M., Lorenzo, O., García-Casado, G., López-Vidriero, I., Lozano, F.M., Ponce, M.R., Micol, J.L., Solano, R.: The JAZ family of repressors is the missing link in jasmonate signalling. - Nature 448: 666-671, 2007. Go to original source...
    7. Chung, H.S., Koo A. J. K., Gao, X., Jayanti, S., Thines, B., Jones, A.D., Howe, G.A.: Regulation and function of Arabidopsis JASMONATE ZIM domain genes in response to wounding and herbivory. - Plant Physiol. 146: 952-964, 2008. Go to original source...
    8. Chung, H.S., Niu, Y.J., Browse, J., Howe, G.A.: Top hits in contemporary JAZ: an update on jasmonate signaling. - Phytochemistry 70: 1547-1559, 2009. Go to original source...
    9. Conconi, A., Smerdon, M.J., Howe, G.A., Ryan, C.A.: The octadecanoid signaling pathway in plants mediates a resoponse to ultraviolet radiation. - Nature 383: 826-829, 1996. Go to original source...
    10. Crooks, G.E., Hon, G., Chandonia, J.M., Brenner, S.E.: WebLogo: a sequence logo generator. - Genome Res. 14: 1188-1190, 2004. Go to original source...
    11. De Castro, E., Sigrist, C.J.A., Gattiker, A., Bulliard, V., Petra, S., Langendijk-Genevaux, P.S., Gasteiger, E., Bairoch, A., Hulo, N.: ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. - Nucl. Acids Res. 34: W362-W365, 2006. Go to original source...
    12. Devi, P.B., Vijayabharathi, R., Sathyabama, S., Malleshi, N.G., Priyadarshini, V.B.: Health benefits of finger millet (Eleusine coracana L.) polyphenols and dietary fiber: a review. - J. Food Sci. Technol. 51: 1021-1040, 2014. Go to original source...
    13. Farmer, E. E., Johnson, R. R., Ryan, C. A.: Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. - Plant Physiol. 98: 995-1002, 1992. Go to original source...
    14. Fernández-Calvo, P., Chini, A., Fernández-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., Solano, R.: 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, 2011. Go to original source...
    15. Feys, B.J.F., Benedetti, C.E., Penfold, C.N., 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 6: 751-759, 1994. Go to original source...
    16. Fonseca, S., Chini, A., Hamberg, M., Adie, B., Porzel, A., Kramell, R., Miersch, O., Wasternack, C., Solano, R.: (+)-7-Iso-jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. - Nat. Chem. Biol. 5: 344-350, 2009. Go to original source...
    17. Gao, X., Brodhagen, M., Isakeit, T., Brown, S.H., Gobel, C., Betran, J., Feussner, I., Keller, N.P., Kolomiets, M.V.: Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. - Mol. Plant Microbe Interact. 22: 222-231, 2009. Go to original source...
    18. Gish, W., States, D.J.: Identification of protein coding regions by database similarity search. - Nat. Genet. 3: 266-272, 1993. Go to original source...
    19. Gynheung, A.: Binary Ti vectors for plant transformation and promoter analysis. - Methods Enzymol. 153: 292-305, 1987. Go to original source...
    20. Howe, G. A., Lightner, J., Browse, J., Ryan, C. A.: An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. - Plant Cell 8: 2067-2077, 1996. Go to original source...
    21. Kang, D.J., Seo, Y.J., Lee, J.D., Ishii, R., Kim, U., Shin, D.H., Park, S.K., Jang, S.W., Lee, I.J.: Jasmonic acid differentially affects growth, ion uptake and abscisic acid concentration in salt tolerant and salt sensitive rice cultivars. - J. Agr. Crop Sci. 191: 273-282, 2005. Go to original source...
    22. Katsir, L., Schilmiller, A.L., Staswick, P.E., He, S.Y., Howe, G.A.: COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. - Proc. nat. Acad. Sci. USA 105: 7100-7105, 2008. Go to original source...
    23. Kazan, K., Manners, J.M.: JAZ repressors and the orchestration of phytohormone crosstalk. - Cell 17: 22-31, 2012. Go to original source...
    24. Kepinsky, S.: The anatomy of auxin perception. - BioEssays 29: 953-956, 2007. Go to original source...
    25. Lee, H.Y., Seo, J.S., Cho, J.H, Jung, H., Kim, J.K., Lee, J.S., Rhee, S., Choi, Y.D.: Oryza sativa COI1 homologues restore jasmonate signal transduction in Arabidopsis COI1-1 mutants. - PLoS ONE 8: e52802, 2013. Go to original source...
    26. Letunic, I., Bork, P.: Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. - Nucl. Acids Res. 39: W475-W478, 2011. Go to original source...
    27. Mewes, H.M., Frishman, D., Güldener, U., Mannhaupt, G., Mayer, K., Mokrejs, M., Morgenstern, B., Münsterkötter, M., Rudd, S., Weil, B.: MIPS: a database for genomes and protein sequences. - Nucl. Acids Res. 30: 31-34, 2002. Go to original source...
    28. Paterson, A.H., Bowers, J.E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., et al.: The Sorghum bicolor genome and the diversification of grasses. - Nature 457: 551-556, 2009. Go to original source...
    29. Pauwels, L., Morrel, K., De Witte, E., Lammertyn, F., Van Montagu, M., Boerjan, W., Inze, D., Gossens, A.: Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. - Proc. nat. Acad. Sci. USA 105: 1380-1385, 2008. Go to original source...
    30. Pauwels, L., Barbero, G.F., Geerinck, J., Tilleman, S., Grunewald, W., Pérez, A.C., Chico, J.M., Bossche, R.V., Sewell, J., Gil, E., García-Casado, G., Witters, E., Inzé, D., Long, J.A., Jaeger, G.D., Solano, R., Goossens, A.: NINJA connects the co-repressor TOPLESS to jasmonate signalling. - Nature 464: 788-792, 2010. Go to original source...
    31. Pedrazani, H., Racagni, G., Alemano, S., Miersch, O., Ramirez, I., Pena-Cortes, H., Taleisnik, E., Machado-Domenech, E., Abdala, G.: Salt tolerant tomato plants show increased levels of jasmonic acid. - Plant Growth Regul. 41: 149-158, 2003. Go to original source...
    32. Perez, A.G., Sanz, C., Olias, R., Olias, J.M.: Effect of methyl jasmonate on in vitro strawberry ripening. - J. Agr. Food Chem. 45: 3733-737, 1997. Go to original source...
    33. Qi, J., Zhou, G., Yang, L., Erb, M., Lu, Y., Sun, X., Cheng, J., Lou, Y.: The chloroplast-localized phospholipases D a4 and a5 regulate herbivore-induced direct and indirect defenses in rice. - Plant Physiol. 157: 1987-1999, 2011. Go to original source...
    34. Rattei, T., Tischler, P., Götz, S., Jehl, M.A., Hoser, J., Arnold, R., Conesa, A., Mewes, H.W.: SIMAP - a comprehensive database of pre-calculated protein sequence similarities, domains, annotations and clusters. - Nucl. Acids Res. 38 (Database Issue): D223-D226, 2010. Go to original source...
    35. Reymond, P., Weber, H., Damond, M., Farmer, E.E.: Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. - Plant Cell Online 12: 707-720, 2000. Go to original source...
    36. 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., 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. 65: 907-921, 2011. Go to original source...
    37. Sheard, L.B., Tan, X., Mao, H., Withers, J., Ben-Nissan, G., Hinds, T.R., Kobayashi, Y., Hsu, F.F., Sharon, M., Browse, J., He, S.Y., Rizo, J., Howe, G., Zheng, N.: Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ coreceptor. - Nature 468: 400-405, 2010. Go to original source...
    38. Staswick, P. E., Su, W., Howell, S. H.: Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. - Proc. nat. Acad. Sci. USA 89: 6837-6840, 1992. Go to original source...
    39. Staswick, P.E., Tiryaki, I.: The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. - Plant Cell 16: 2117-2127, 2004. Go to original source...
    40. Stintzi, A., Browse, J.: The Arabidopsis male-sterile mutant, OPR3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. - Proc. nat. Acad. Sci. USA 97: 10625-10630, 2000. Go to original source...
    41. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S.: MAGA6: molecular evolutionary genetics analysis version 6.0. - Mol. Biol. Evolut. 30: 2725-2729, 2013. Go to original source...
    42. Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A., Browse, J.: JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. - Nature 448: 661-665, 2007. Go to original source...
    43. Thompson, J.D., Higgins, D.G., Gibson, T.J.: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. - Nucl. Acids Res. 22: 4673-4680, 1994. Go to original source...
    44. Vadivoo, A.S., Joseph, R., Garesan, N.M.: Genetic variability and calcium contents in finger millet (Eleusine coracana L. Gaertn) in relation to grain colour. - Plant Foods Human Nutr. 52: 353-364, 1998. Go to original source...
    45. Vanholme, B., Grunewald, W., Bateman, A., Kohchi, T., Gheysen, G.: The TIFY family previously known as ZIM. - Trends Plant Sci. 12: 239-244, 2007. Go to original source...
    46. Withers, J., Yao, J., Mecey, C., Howe, G.A., Melotto, M., He, S.Y.: Transcriptionfactor-dependent nuclear localization of a transcriptional repressor in jasmonate hormone signaling. - Proc. nat. Acad. Sci. USA 109: 20148-20153, 2012. Go to original source...
    47. Xiao, S., Dai, L., Liu, F., Wang, Z., Peng, W., Xie, D.: COS1: an Arabidopsis coronatine insensitive1 suppressor essential for regulation of jasmonate-mediated plant defense and senescence. - Plant Cell Online 16: 1132-1142, 2004. Go to original source...
    48. Xie, D.X., Feys, B.F., James, S., Nieto-Rostro, M., Turner, J.G.: COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. - Science 280: 1091-1094, 1998. Go to original source...
    49. Xu, K., Huang, X., Wu, M., Wang, Y., Chang, Y., Liu, K., Zhang, J., Zhang, Y., Zhang, F., Yi, L., Li, T., Wang, R., Tan, G., Li, C.: A rapid, highly efficient and economical method Agrobacterium-mediated In planta transient transformation in living onion epidermis. - PLoS ONE 9: e83556, 2014. Go to original source...
    50. Yan, Y., Christensen, S., Isakeit, T., Engelberth, J., Meeley, R., Hayward, A., Emery, R.J., Kolomiets, MV.: Disruption of OPR7 and OPR8 reveals the versatile functions of jasmonic acid in maize development and defense. - Plant Cell 24: 1420-1436, 2012. Go to original source...
    51. Zhang, G., Liu, X., Quan, Z., Cheng, S., Xu, X., Pan, S., Xie, M., Zeng, P., P., Yue, Z., Wang, W., Tao, Y., Bian, C., Han, C., Xia, Q., Peng, X., Cao, R., Yang, X., Zhan, D., Hu, J., Zhang, Y., Li, H., Li, H., Li, N., Wang, J., Wang, C., Wang, R., Guo, T., Cai, Y., Liu, C., Xiang, H., Shi, Q., Huang, P., Chen, Q., Li, Y., Wang, J., Zhao, Z., Wang, J.: Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. - Nat. Biotech. 30: 549-554, 2012. Go to original source...
    52. Zhu, J.: Salt and drought stress signal transduction in plants. - Annu. Rev. Plant Biol. 53: 247-273, 2002. Go to original source...

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