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Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.)

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Abstract

Indole-3-acetic acid (IAA) markedly increased ethylene production by inducing the expression of three 1-aminocyclopropane-1-carboxylate (ACC) synthase cDNAs (pVR-ACS1, pVR-ACS6 and pVR-ACS7) in mung bean hypocotyls. Results from nuclear run-on transcription assay and RNA gel blot studies revealed that all three genes were transcriptionally active displaying unique patterns of induction by IAA and various hormones in etiolated hypocotyls. Particularly, 24-epibrassinolide (BR), an active brassinosteroid, specifically enhanced the expression of VR-ACS7 by a distinct temporal induction mechanism compared to that of IAA. In addition, BR synergistically increased the IAA-induced VR-ACS6 and VR-ACS7 transcript levels, while it effectively abolished both the IAA- and kinetin-induced accumulation of VR-ACS1 mRNA. In light-grown plants, VR-ACS1 was induced by IAA in roots, and VR-ACS6 in epicotyls. IAA- and BR-treatments were not able to increase the VR-ACS7 transcript in the light-grown tissues. These results indicate that the expression of ACC synthase multigene family is regulated by complex hormonal and developmental networks in a gene- and tissue-specific manner in mung bean plants. The VR-ACS7 gene was isolated, and chimeric fusion between the 2.4 kb 5′-upstream region and the β-glucuronidase (GUS) reporter gene was constructed and introduced into Nicotiana tabacum. Analysis of transgenic tobacco plants revealed the VR-ACS7 promoter-driven GUS activity at a highly localized region of the hypocotyl-root junction of control seedlings, while a marked induction of GUS activity was detected only in the hypocotyl region of the IAA-treated transgenic seedlings where rapid cell elongation occurs. Although there was a modest synergistic effect of BR on the IAA-induced GUS activity, BR alone failed to increase the GUS activity, suggesting that induction of VR-ACS7 occurs via separate signaling pathways in response to IAA and BR. A scheme of the multiple regulatory pathways for the expression of ACC synthase multigene family by auxin and BR is presented.

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References

  • Abel, S. and Theologis, A. 1996. Early genes and auxin action. Plant Physiol. 111: 9–17.

    Google Scholar 

  • Abel, S., Nguyen, M.D., Chow, W. and Theologis, A. 1995. ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. J. Biol. Chem. 270: 19093–19099.

    Google Scholar 

  • Abeles, F.B., Morgan, P.W. and Saltveit, M.E. 1992. Ethylene in Plant Biology. Academic Press, San Diego, CA.

    Google Scholar 

  • Arteca, J.M. and Arteca R.N. 1999. A multi-responsive gene en-coding 1-aminocyclopropane-1-carboxylate synthase (ACS6) in mature Arabidopsis leaves. Plant Mol. Biol. 39: 209–219.

    Google Scholar 

  • Arteca, R.N., Tsai, D.-S., Schlagnhaufer, C. and Mandava, N.B. 1983. The effect of brassinosteroid on auxin-induced ethylene production by etiolated mung bean segments. Physiol. Plant 59: 539–544.

    Google Scholar 

  • Botella, J.R., Arteca, J.M., Schlagnhaufer, C.D., Arteca, R.N. and Phillips, A.T. 1992. Identification and characterization of a full-length cDNA encoding for an auxin-induced 1-aminocyclopropane-1-carboxylate synthase from etiolated mung bean hypocotyl segments and expression of its mRNA in response to indole-3-acetic acid. Plant Mol. Biol. 20: 425–436.

    Google Scholar 

  • Botella, J.R., Schlagnhaufer, C.D., Arteca, R.N. and Phillips, A.T. 1992. Identification and characterization of three putative genes for 1-aminocyclopropane-1-carboxylate synthase from etiolated mung bean hypocotyl segments. Plant Mol. Biol. 18: 793–797.

    Google Scholar 

  • Botella, J.R., Schlagnhaufer, C.D., Arteca, J.M., Arteca, R.N. and Phillips, A.T. 1993. Identification of two new members of the 1-aminocyclopropane-1-carboxylate synthase-encoding multigene family in mung bean. Gene 123: 249–253.

    Google Scholar 

  • Brown, J.W.S. 1986. A catalogue of splice junctions and putative branch point sequences from plant introns. Nucl. Acids Res. 14: 9549–9559.

    Google Scholar 

  • Bui, A.Q. and O'Neill, S.D. 1998. Three 1-aminocyclopropane-1-carboxylate synthase genes regulated by primary and secondary pollination signals in orchid flowers. Plant Physiol. 116: 419–428.

    Google Scholar 

  • Clouse, S.D. 1997. Molecular genetic analysis of brassinosteroid action. Physiol. Plant 100: 702–709.

    Google Scholar 

  • Clouse, S.D., Zurek, D.M., McMorris, T.C. and Baker M.E. 1992. Effect of brassinolide on gene expression in elongating soybean epicotyls. Plant Physiol. 100: 1377–1383.

    Google Scholar 

  • Creelman, R.A. and Mullet, J.E. 1997. Oligosaccharins, brassinolides, and jasmonates: Nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9: 1211–1223.

    Google Scholar 

  • Destefano-Beltran, L.J.C., Van Caeneghem, W., Gielen, J., Richard, L., Van Montagu, M. and Van Der Straeten, D. 1995. Characterization of three members of the ACC synthase gene family in Solanum tuberosum L. Mol. Gen. Genet. 246: 496–508.

    Google Scholar 

  • Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G. and Fraley, R.T. 1985. A simple and general method for transferring genes into plants. Science 227: 1229–1231.

    Google Scholar 

  • Jin, E.S., Lee, J.-H., Park, J.A. and Kim, W.T. 1999. Temporal and spatial regulation of the expression of 1-aminocyclopropane-1-carboxylate oxidase by ethylene in mung bean (Vigna radiata). Physiol. Plant. 105: 132–140.

    Google Scholar 

  • Jones, M.L. and Woodson, W.R. 1999. Differential expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in carnation. Plant Physiol. 119: 755–764.

    Google Scholar 

  • Kende, H. 1993. Ethylene biosynthesis. Annu. Rev.Plant Physiol. Plant Mol. Biol. 44: 283–307.

    Google Scholar 

  • Kende, H. and Zeevaart, J.A.D. 1997. The five 'classical' plant hormones. Plant Cell 9: 1197–1210.

    Google Scholar 

  • Kim, W.T., Campbell, A., Moriguchi, T., Yi, H.C. and Yang, S.F. 1997. Auxin induces three genes encoding 1-aminocyclopropane-1-carboxylate synthase in mung bean hypocotyls. J. Plant Physiol. 150: 77–84.

    Google Scholar 

  • Kim, W.T., Silverstone, A., Yip, W.K., Dong, J.G. and Yang, S.F. 1992. Induction of 1-aminocyclopropane-1-carboxylate synthase mRNA by auxin in mung bean hypocotyls and cultured apple shoots. Plant Physiol. 98: 465–471.

    Google Scholar 

  • Liang, X.L., Abel, S., Keller, J.A., Shen, N.F. and Theologis, A. 1992. The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 89: 11046–1105.

    Google Scholar 

  • Martin, T., Wohner, R.-V., Hummel, S., Willmitzer, L. and From-mer, W.B. 1992. The GUS reporter system as a tool to study plant gene expression. In: S.R. Gallagher (Ed.), GUS Protocol: Using the GUS Gene as a Reporter of Gene Expression, Academic Press, San Diego, CA.

    Google Scholar 

  • Oetiker, J.H., Olson, D.C., Shiu, O.Y. and Yang, S.F. 1997. Dif-ferential induction of seven 1-aminocyclopropane-1-carboxylate synthase genes by elicitor in suspension cultures of tomato (Lycopersicon esculentum). Plant Mol. Biol. 34: 275–286.

    Google Scholar 

  • Olson, D.C., Oetiker, J.H. and Yang, S.F. 1995. Analysis of LE-ACS3, a 1-aminocyclopropane-1-carboxylic acid synthase gene.454 expressed during flooding in the roots of tomato plants. J. Biol. Chem. 270: 14056–14061.

    Google Scholar 

  • Olson, D.C., White, J.A., Edelman, L., Harkins, R.N. and Kende, H. 1991. Differential expression of two genes for 1-aminocyclopropane-1-carboxylate synthase in tomato fruits. Proc. Natl. Acad. Sci. USA 88: 5340–5344.

    Google Scholar 

  • Rottmann, W.H., Peter, G.F., Oeller, P.W., Keller, J.A., Shen, N.F., Nagy, B.P., Taylor, L.P., Campbell, A.D. and Theologis, A. 1991. 1-Aminocyclopropane-1-carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. J. Mol. Biol. 222: 937–961.

    Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Schlagnhaufer, C.D., Arteca, R.N. and Pell, E.J. 1997. Sequen-tial expression of two 1-aminocyclopropane-1-carboxylate syn-thase genes in response to biotic and abiotic stresses in potato (Solanum tuberosum L.) leaves. Plant Mol. Biol. 35: 683–688.

    Google Scholar 

  • Schlagnhaufer, C., Arteca, R.N. and Yopp, J.H. 1984. Evidence that brassinosteroid stimulates auxin-induced ethylene synthesis in mung bean hypocotyls between S-adenosylmethionine and 1-aminocyclopropane-1-carboxylic acid. Physiol. Plant. 61: 555–558.

    Google Scholar 

  • Shen, W.J. and Forde, B.G. 1989. Efficient transformation of Agrobacterium spp. by high voltage electroporation. Nucl. Acids Res. 17: 8385.

    Google Scholar 

  • Shiu, O.Y., Oetiker, J.H., Yip, W.K. and Yang, S.F. 1998. The promoter of LE-ACS7, an early flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of the tomato, is tagged by a Sol3 transposon. Proc. Natl. Acad. Sci. USA 95: 10334–10339.

    Google Scholar 

  • Spanu, P., Boller, T. and Kende, H. 1993. Differential accumulation of transcripts of 1-aminocyclopropane-1-carboxylate synthase genes in tomato plants infected with Phytophthora infestans and in elicitor-treated tomato cell suspensions. J. Plant Physiol. 141: 557–562.

    Google Scholar 

  • Theologis, A. 1992. One rotten apple spoils the whole bushel: the role of ethylene in fruit ripening. Cell 70: 181–184.

    Google Scholar 

  • Tuomainen, J., Betz, C., Kangasjarvi, J., Ernst, D., Yin, Z.-H., Langebartels, C. and Sandermann, H. Jr. 1997. Ozone induction of ethylene emission in tomato plants: regulation by differential accumulation of transcripts for biosynthetic enzymes. Plant J. 12: 1151–1162.

    Google Scholar 

  • Vahala, J., Schlagnhaufer, C.D. and Pell, E.J. 1998. Induction of an ACC synthase cDNA by ozone in light-grown Arabidopsis thaliana leaves. Physiol. Plant 103: 45–50.

    Google Scholar 

  • Van der Straeten, D., Van Wiemeersch, L., Goodman, H.M. and Van Montagu, M. 1990. Cloning and sequence of two different cDNAs encoding 1-aminocyclopropane-1-carboxylate synthase in tomato. Proc. Natl. Acad. Sci. USA 87: 4859–4863.

    Google Scholar 

  • Walling, L., Drews, G.N. and Goldberg, R.B. 1986. Transcriptional and post-transcriptional regulation of soybean seed protein mRNA levels. Proc. Natl. Acad. Sci. USA 83: 2123–2127.

    Google Scholar 

  • Woeste, K.E., Ye, C. and Kieber, J.J. 1999. Two Arabidopsis mutants that overproduce ethylene are affected in the post-transcriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase. Plant Physiol. 119: 521–529.

    Google Scholar 

  • Xu, W., Campbell, P., Vargheese, A.K. and Braam, J. 1996. The Arabidopsis XET-related gene family: environmental and hormonal regulation of expression. Plant J. 9: 879–889.

    Google Scholar 

  • Xu, W., Purugganan, M.M., Polisensky, D.H., Antosiewicz, D.M., Fry, S.C. and Braam, J. 1995. Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7: 1555–1567.

    Google Scholar 

  • Yang, S.F. and Hoffman, N.E. 1984. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35: 155–189.

    Google Scholar 

  • Yip, W.-K., Moore, T. and Yang, S.F. 1992. Differential accu-mulation of transcripts for four tomato 1-aminocyclopropane-1-carboxylate synthase homologs under various conditions. Proc. Natl. Acad. Sci. USA 89: 2475–2479.

    Google Scholar 

  • Yoon, I.S., Mori, H., Kim, J.H., Kang, B.G. and Imaseki, H. 1997. VR-ACS6 is an auxin-inducible 1-aminocyclopropane-1-carboxylate synthase gene in mung bean (Vigna radiata). Plant Cell Physiol. 38: 217–224.

    Google Scholar 

  • Yopp, J.H., Colclasure, G.C. and Mandava, N. 1979. Effects of brassin complex on auxin and gibberellin mediated events in the morphogenesis of the etiolated bean hypocotyl. Physiol. Plant. 46: 247–254.

    Google Scholar 

  • Zarembinski, T.I. and Theologis, A. 1993. Anaerobiosis and plant growth hormones induce two genes encoding 1-aminocyclopropane-1-carboxylate synthase in rice (Oryza sativa L.). Mol. Biol. Cell 4: 363–373.

    Google Scholar 

  • Zurek, D.M. and Clouse, S.D. 1994. Molecular cloning and char-acterization of a brassinosteroid-regulated gene from elongating soybean (Glycine max L.) epicotyls. Plant Physiol. 104: 161–170.

    Google Scholar 

  • Zurek, D.M., Rayle, D.L., McMorris, T.C. and Clouse, S.D. 1994. Investigation of gene expression, growth kinetics, and wall extensibility during brassinosteroid-regulated stem elongation. Plant Physiol. 104: 505–513.

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, College of Science, Yonsei University, Seoul, 120-749, Korea

    Ho Chul Yi, Sunjoo Joo, Kyung Hee Nam, Bin G. Kang & Woo Taek Kim

  2. Department of Biological Science, Ewha Womans University, Seoul, 120-750, Korea

    June Seung Lee

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  1. Ho Chul Yi
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Yi, H.C., Joo, S., Nam, K.H. et al. Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.). Plant Mol Biol 41, 443–454 (1999). https://doi.org/10.1023/A:1006372612574

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