Abstract
Ethylene-regulated gene expression in leaves of Arabidopsis thaliana was investigated with an expressed sequence tag-based microarray containing about 6000 unique genes. Comparing expression profiles of the ethylene-insensitive mutant etr1-1, the ethylene-constitutive mutant ctr1-1, ethylene-treated wild-type and untreated wild-type plants identified ca. 7% of the investigated genes as ethylene-regulated. Exogenous ethylene treatment and ctr1-1 had similar changes in gene expression, but differences were noted. Ethylene-regulated genes involved in its own biosynthesis and signal transduction pathway were identified. A large number of transcription factors and some putative signaling components were highly regulated by ethylene. Chloroplast structural protein and photosynthetic genes were generally down-regulated. Ethylene appeared to regulate other primary metabolic genes. Plant defense and PR protein genes were differentially regulated, with some genes within this class highly up-regulated. Other ethylene-regulated genes identified were known sugar-, auxin-, wounding- and jasmonic acid-related genes, suggesting the existence of coordinated interactions between ethylene and other hormonal and defense signaling pathways. Although hundreds of potentially important transcriptome changes were identified, the functions of many ethylene-regulated genes remain unknown.
Similar content being viewed by others
References
Abeles, F.B., Morgan, P.W. and Saltveit, M.E. 1992. Ethylene in Plant Biology. Academic Press, New York.
Alexander, L. and Grierson, D. 2002. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J. Exp. Bot. 53: 2039-2055.
Arabidopsis Genome Initiative. 2000. http://www.arabidopsis. org/info/agi.html
Arondel, V., Vergnolle, C., Cantrel C. and Kader, J.C. 2000. Lipid transfer proteins are encoded by a small multigene family in Arabidopsis thaliana. Plant Sci. 157: 1-12.
Assmann, S.M. 2002. Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell 14: S355-S373.
Bandurski, R.S., Cohen, J.D., Slovin, J.P. and Reinecke, D.M. 1995. Hormone biosynthesis and metabolism. In: P.J. Davies (Ed.) Plant Hormones, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 39-65.
Berger, S., Bell, E., Sadka, A. and Mullet, J.E. 1995. Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol. Biol. 27: 933-942.
Bleecker, A.B., Estelle, M.A., Somerville, C. and Kende, H. 1988. Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241: 1086-1089.
Bolwell, G.P. and Wojtaszek, P. 1997. Mechanisms for the generation of reactive oxygen species in plant defense-a broad perspective. Physiol. Mol. Plant Path. 51: 347-366.
Bucher, M., Brunner, S., Zimmermann, P., Zardi, G.I., Amrhein, N., Willmitzer, L. and Riesmeier, J.W. 2002. The expression of an extensin-like protein correlates with cellular tip growth in tomato. Plant Physiol. 128: 911-923.
Büttner, M. and Singh, K.B. 1997. Arabidopsis thaliana ethyleneresponsive element binding protein (AtEBP), an ethyleneinducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc. Natl. Acad. Sci. USA 27: 5961-5966.
Chang, C., Kwok, S.F., Bleecker, A.B. and Meyerowitz, E.M. 1993. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262: 539-544.
Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W. and Ecker, J.R. 1997. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENEINSENSITIVE3 and related proteins. Cell 89: 1133-1144.
Chen, Q.G. and Bleecker, A.B. 1995. Analysis of ethylene signaltransduction kinetics associated with seedling-growth response and chintinase induction in wild-type and mutant Arabidopsis. Plant Physiol. 108: 597-607.
Chen, W., Provart, N.J., Glazebrook, J., Katagiri, F., Chang, HS., Eulgem, T., Mauch, F., Luan, S., Zou, G., Whitham, S.A., Budworth, P.R., Tao, Y., Xie, Z., Chen, X., Lam, S., Kreps, J.A., Harper, J.F., Si-Ammour, A., Mauch-Mani, B., Heinlein, M., Kobayashi, K., Hohn, T., Dangl, J.L., Wang, X. and Zhu, T. 2002. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14: 559-574.
Cheong, Y.H., Chang, H.S., Gupta, R., Wang, X., Zhu, T. and Luan, S. 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129: 1-17.
Ecker, J.R. 1995. The ethylene signal transduction pathway in plants. Science 268: 667-675.
Eisen, M.B., Spellman, P.T., Brown, P.O. and Bostein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95: 14863-14868.
Ellis, C. and Turner, J.G. 2001. The arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13: 1025-1033.
Evertsz, E., Starink, P., Gupta, R. and Watson, D. 2000. Technology and application of gene expression microarrays. In: M. Schena (Ed.) Microarray Biochip Technology, Eaton Publishing, Natick, pp. 149-166.
Gibson, S.I., Laby, R.J. and Kim, D. 2001. The sugar-insensitive1 (sis1) mutant of Arabidopsis is allelic to ctr1. Biochem. Biophys. Res. Commun. 280: 196-203.
Gómez-Lim, M.A., Valedes-López, V., Cruz-Hernández, A. and Saucedo-Arias, L.J. 1993. Isolation and characterization of a gene involved in ethylene biosynthesis from Arabidopsis thaliana. Gene 134: 217-221.
Grbic, V. and Bleecker, A.B. 1993. Role of ethylene in the control of leaf senescence in Arabidopsis thaliana. Plant Physiol. (suppl) 102: 131.
Horvath, D.P., Schaffer, R., West, M. and Wisman, E. 2003. Arabidopsis microarrays identify conserved and differentially expressed genes involved in shoot growth and development from distantly related plant species. Plant J. 34: 125-134.
Hua, J. and Meyerowitz, E. 1998. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94: 261-271.
Hua, J., Sakai, H., Nourizadeh, S., Chen, Q.G., Bleecker, A.B., Ecker, J.R. and Meyerowitz, E.M. 1998. EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10: 1321-1332.
Hunter, T. 1995. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80: 225-236.
Johnson, P.R. and Ecker, J.R. 1998. The ethylene gas signal transduction pathway: a molecular perspective. Annu. Rev. Genet. 32: 227-254.
Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A. and Ecker, J.R. 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72: 427-441.
Kieffer, F., Lherminier, J., Simon-Plas, F., Nicole, M., Paynot, M., Elmayan, T. and Blein, J.P. 2000. The fungal elicitor cryptogein induces cell wall modifications on tobacco cell suspension. J. Exp. Bot. 51: 1799-1811.
Knoester, M., van Loon, L.C., van den Heuvel, J., Hennig, J., Bol, J.F. and Linthorst, H.J.M. 1998. Ethylene-insensitive tobacco lacks non-host resistance against soilborne fungi. Proc. Natl. Acad. Sci. USA 95: 1933-1937.
Lam, E., Pontier, D. and del Pozo, O. 1999. Die and let live: programmed cell death in plants. Curr. Opin. Plant Biol. 2: 502-507.
Lease, K.A., Wen, J., Li, J., Doke, J.T., Liscum, E. and Walker, J.C.2001. A mutant Arabidopsis heterotrimeric G-protein beta subunit affects leaf, flower, and fruit development. Plant Cell 13: 2631-2641.
Liu, Z.B., Ulmasov, T., Shi, X., Hagen, G. and Guilfoyle, T.J. 1994. Soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell 6: 645-657.
Ma, L., Li, J., Qu, L., Hager, J., Chen, Z., Zhao, H. and Deng, X.W. 2001. Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13: 2589-2607.
Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K.A., Dangl, J.L. and Dietrich, R.A. 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genet. 26: 403-410.
Membré, N., Bernier, F., Staiger, D. and Berna, A. 2000. Arabidopsis thaliana germin-like proteins: common and specific features point to a variety of functions. Planta 211: 345-354.
Mittler, R. and Zilinskas, B.A. 1992. Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J. Biol. Chem. 267: 21802-21807.
Nairn, C.J., Lewandowski, D.J. and Burns, J.K. 1998. Genetics and expression of two pectinesterase genes in Valencia orange. Physiol. Plant. 102: 226-235.
O'Donnell, P.J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H.M.O. and Bowles, D.J. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science 274: 1914-1917.
Ohme-Takagi, M. and Shinshi, H. 1995. Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7: 173-182.
Ouyang, J., Shao, X. and Li, J. 2000. Indole-3-glycerol phosphate, a branchpoint of indole-3-acetic acid biosynthesis from the tryptophan biosynthetic pathway in Arabidopsis thaliana. Plant J. 24: 327-333.
Potter, S., Uknes, S., Lawton, K., Winter, A.M., Chandler, D., DiMaio, J., Novitzky, R., Ward, E. and Ryals, J. 1993. Regulation of a hevein-like gene in Arabidopsis. Mol. Plant-Microbe Interact. 6: 680-685.
Raz, V. and Fluhr, R. 1993. Ethylene signal is transduced via protein phosphorylation events in plants. Plant Cell 5: 523-530.
Reddy, A.S. and Poovaiah, B.W. 1990. Molecular cloning and sequencing of a cDNA for an auxin-repressed mRNA: correlation between fruit growth and repression of the auxin-regulated gene. Plant Mol. Biol. 14: 127-136.
Reinke, V., Smith, H.E., Nance, J., Doren, A., Begley, R., Jones, S.J.M., Davis, E.B., Scherer, S., Ward, S. and Kim, S.K. 2000. A global profile of germline gene expression in C. elegans. Mol. Cell 6: 605-616.
Roberts, J.A., Elliott, K.A. and González-Carranza, Z.H. 2002. Abscission, dehiscence, and other cell separation processes. Annu. Rev. Plant Biol. 53: 131-158.
Rojo, E., León, J. and Sánchez-Serrano, J.J. 1999. Cross-talk between wound signaling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J. 20: 135-142.
Scheideler, M., Schlaich, N.L., Fellenberg, K., Beissbarth, T., Hauser, N.C., Vingron, M., Slusarenko, A.J. and Hoheisel, J.D. 2002. Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J. Biol. Chem. 277: 10555-10561.
Schena, M., Shalon, D. and Brown, P.O. 1995. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270: 467-470.
Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C. and Manners, J.M. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97: 11655-11660.
Sehnke, P.C., DeLille, J.M. and Ferl, R.J. 2002. Consummating signal transduction: the role of 14-3-3 proteins in the completion of signal-induced transitions in protein activity. Plant Cell 14: S339-S354.
Smart, C.M. 1994. Gene expression during leaf senescence. New Phytol. 126: 419-448.
Stotz, H.U., Pittendrigh, B.R., Kroymann, J., Weniger, K., Fritsche, J., Bauke, A. and Mitchell-Olds, T. 2000. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol. 124: 1007-1018.
Tanimoto, M., Roberts, K. and Dolan, L. 1995. Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J. 8: 943-948.
Tieman, D.M., Ciardi, J.A., Taylor, M.G. and Klee, H.J. 2001. Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J. 26: 47-58.
Turner, J.G., Ellis, C. and Devoto, A. 2002. The jasmonate signal pathway. Plant Cell 14: S153-S164.
Wang, K.L.C., Li, H. and Ecker, J.R. 2002. Ethylene biosynthesis and signaling networks. Plant Cell 14: S131-S151.
Wilkinson, J.Q., Lanahan, M.B., Clark, D.G., Bleecker, A.B., Chang, C., Meyerowitz, E.M. and Klee, H.J. 1997. A dominant mutant receptor from Arabidopsis confers ethylene insensitivity in heterologous plants. Nature Biotech. 15: 444-447.
Xu, Y. Chang, P.F.L., Liu, D., Narasimhan, M.L., Raghothama, K.G., Hasegawa, P.M. and Bressan, R.A. 1994. Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6: 1077-1085.
Yang, S.F. and Hoffman, N.E. 1984. Ethylene biosynthesis and its regulation in higher-plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 35: 155-189.
Yip, W.-K., Moore, T. and Yang, S.F. 1992. Differential accumulation of transcripts for four tomato 1-aminocyclopropane-1-carboxylate synthase homologs under various conditions. Proc. Nat. Acad. Sci. USA 89: 2475-2479.
Zhang, L., Zhang, Y., Zhou, Y., An, S., Zhou, Y. and Cheng, J. 2002. Response of gene expression in Saccharomyces cerevisiae to amphotericin B and nystatin measured by microarrays. J. Antimicrob. Chemother. 49: 905-915.
Zhong, G.Y., Goren, R., Riov, J., Sisler, E.C. and Holland, D. 2001. Characterization of an ethylene-induced esterase gene isolated from Citrus sinensis by competitive hybridization. Physiol. Plant. 113: 267-274.
Zhu, T. and Wang, X. 2000. Large scale profiling of the arabidopsis genome. Plant Physiol. 124: 1472-1476.
Author information
Authors and Affiliations
Corresponding author
Additional information
An erratum to this article is available at http://dx.doi.org/10.1007/s11103-006-8444-0.
Rights and permissions
About this article
Cite this article
Van Zhong, G., Burns, J.K. Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol Biol 53, 117–131 (2003). https://doi.org/10.1023/B:PLAN.0000009270.81977.ef
Issue Date:
DOI: https://doi.org/10.1023/B:PLAN.0000009270.81977.ef