Abstract
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.
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Abbreviations
- ABA:
-
abscisic acid
- COI1:
-
coronatine insensitive 1
- GFP:
-
green fluorescence protein
- Ile:
-
isoleaucine
- JA:
-
jasmonic acid
- JAZ:
-
jasmonate ZIM domain
- MeJa:
-
methyl jasmonate
- MG132:
-
N-(phenylmethoxy) carbonyl-L-Leucyl-N-[(1R)-1-formyl-3-methylbutyl]-L-leucinamide
- MYC:
-
myelocytomatosis
- RE:
-
restriction endonuclease
- SCFCOI1 :
-
COI1 stabilized by Skp, Cullin, F-box containing complex
- TIFY:
-
conserved TIFY sequence containing protein
- ZIM:
-
zinc finger protein expressed in inflorescence meristem
References
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.
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.
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.
Browse, J.: Jasmonate passes muster: a receptor and targets for the defense hormone. — Annu. Rev. Plant Biol. 60: 183–205, 2009.
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.
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.
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.
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.
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.
Crooks, G.E., Hon, G., Chandonia, J.M., Brenner, S.E.: WebLogo: a sequence logo generator. — Genome Res. 14: 1188–1190, 2004.
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.
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.
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.
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.
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.
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.
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.
Gish, W., States, D.J.: Identification of protein coding regions by database similarity search. — Nat. Genet. 3: 266–272, 1993.
Gynheung, A.: Binary Ti vectors for plant transformation and promoter analysis. — Methods Enzymol. 153: 292–305, 1987.
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.
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.
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.
Kazan, K., Manners, J.M.: JAZ repressors and the orchestration of phytohormone crosstalk. — Cell 17: 22–31, 2012.
Kepinsky, S.: The anatomy of auxin perception. — BioEssays 29: 953–956, 2007.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Vanholme, B., Grunewald, W., Bateman, A., Kohchi, T., Gheysen, G.: The TIFY family previously known as ZIM. — Trends Plant Sci. 12: 239–244, 2007.
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.
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.
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.
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.
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.
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.
Zhu, J.: Salt and drought stress signal transduction in plants. — Annu. Rev. Plant Biol. 53: 247–273, 2002.
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Acknowledgement: This study was supported by the WOS-A scheme of the Department of Science and Technology, the Government of India (Grant No. SR/WOS-A/LS-431/2011(G)). The authors are thankful to the Director, CSIR-IICB, for kindly allowing us to carry out this work. The authors are also thankful to Dr. S. Chattopadhyay for kindly providing pCAMBIA1303.
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Sen, S., Dutta, S.K. Cloning, characterization, and subcellular localization of a novel JAZ repressor from Eleusine coracana . Biol Plant 60, 715–723 (2016). https://doi.org/10.1007/s10535-016-0652-0
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DOI: https://doi.org/10.1007/s10535-016-0652-0