Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Structure and expression of cDNAs encoding 1-aminocyclopropane-1-carboxylate oxidase homologs isolated from excised mung bean hypocotyls

  • 60 Accesses

  • 83 Citations

Abstract

By screening a mung bean (Vigna radiata L.) hypocotyl cDNA library using a combination of apple (pAE12) and tomato (pTOM13) 1-aminocyclopropane1-carboxylate (ACC)-oxidase cDNAs as probes, putative ACC-oxidase clones were isolated. Based on restriction-enzyme map and DNA-sequencing analyses, they can be divided into two homology classes, represented by pVR-ACO1 and pVR-ACO2. While pVR-ACO1 and pVR-ACO2 exhibit close homology in their coding regions, their 3′-noncoding regions are divergent. pVR-ACO1 is a 1312-bp full-length clone and contains a single open reading frame encoding 317 amino acids (MW = 35.8 kDa), while pVR-ACO2 is 1172 bp long and is a partial cDNA clone encoding 308 amino acids. These two deduced amino-acid sequences share 83% identity, and display considerable sequence conservation (73–86%) to other ACC oxidases from various plant species. Northern blot analyses of RNAs isolated from hypocotyl, leaf, and stem tissues using gene-specific probes indicate that the pVR-ACO1 transcript is present in all parts of the seedling and that the expression in hypocotyls is further increased following excision. The maximum induction of ACC-oxidase transcripts occurred at about 6 h after excision, while the maximum enzyme activity was observed at 24 h. When excised hypocotyls were treated with ethylene a further enhanced level of transcripts was observed. Aminooxyacetic acid, an inhibitor of ACC-synthase activity, and 2,5-norbornadiene, an inhibitor of ethylene action, suppressed the wound-induced accumulation of ACC-oxidase mRNA, while an addition of ethylene in these tissues restored the accumulation of ACC-oxidase mRNA. These results indicate that the wound-induced expression of ACC-oxidase transcripts is mediated through wound-induced ethylene. Furthermore, when intact mung-bean seedlings were treated with exogenous ethylene, a marked increase in the level of ACC-oxidase mRNA was observed. Together, these results indicate that ethylene plays a key role in activating the expression of the ACC-oxidase gene in both intact and excised mung-bean hypocotyls.

This is a preview of subscription content, log in to check access.

Abbreviations

ACC:

1-aminocyclopropane-1-carboxylate

AOA:

aminooxyacetic acid

MJ:

methyl jasmonate

NBD:

2,5-norbornadiene

PCR:

polymerase chain reaction

References

  1. Adams, D.O., Yang, S.F. (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc. Natl. Acad. Sci. USA76, 170–174

  2. Bailly, C., Corbineau, F., Come, D. (1992) The effects of abscisic acid and methyl jasmonate on 1-aminocyclopropane-1-carboxylic acid conversion to ethylene in hypocotyl segments of sunflower seedling, and their control by calcium and calmodulin. Plant Growth Regul.11, 349–355

  3. Balague, C., Watson, C.F., Turner, A.J., Rouge, P., Picton, S., Pech, J.-C., Grierson, D. (1993) Isolation of a ripening and wound-induced cDNA fromCucumis melo L. encoding a protein with homology to the ethylene-forming enzyme. Eur. J. Biochem.212, 27–34

  4. Bassi, P.K., Spencer, M.S. (1983) Does light inhibit ethylene production in leaves? Plant Physiol.73, 758–760

  5. Callahan, A.M., Morgens, P.H., Wright, P., Nichols, K.E. (1992) Comparison of Pch313 (pTOM13 homolog) RNA accumulation during fruit softening and wounding of two phenotypically different peach cultivars. Plant Physiol.100, 482–488

  6. Cameron, A.C., Fenton, C.A.L., Yu, Y., Adams, D.O., Yang, S.F. (1979) Increased production of ethylene by plant tissues treated with 1-aminocyclopropane-1-carboxylic acid. Hort Science14, 178–180

  7. Chou, C.M., Kao, C.H. (1992) Stimulation of 1-aminocyclopropane-1-carboxylic acid-dependent ethylene production in detached rice leaves by methyl jasmonate. Plant Sci.83, 137–141

  8. Creelman, R.A., Tierney, M.L., Mullet, J.E. (1992) Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc. Natl. Acad. Sci. USA89, 4938–4941

  9. Dong, J.G., Fernandez-Maculet, J.C., Yang, S.F. (1992a) Purification and characterization of 1-aminocyclopropane-1-carboxylate oxidase from apple fruit. Proc. Natl. Acad. Sci. USA89, 9789–9793

  10. Dong, J.G., Olson, D., Silverstone, A.L., Yang, S.F. (1992b) Sequence of a cDNA coding for 1-aminocyclopropane-1-carboxylate oxidase homolog from apple fruit. Plant Physiol.98, 1530–1531

  11. Drory, A., Mayak, S., Woodson, W.R. (1993) Expression of ethylene biosynthetic pathway mRNAs is spatially regulated within carnation flower petals. J. Plant Physiol.141, 663–667

  12. Dupille, E., Rombaldi, C., Lelievre, J.-M., Cleyet-Marel, J.-C., Pech, J.-C., Latche, A. (1993) Purification, properties and partial amino-acid sequence of 1-aminocyclopropane-1-carboxylic acid oxidase from apple fruits. Planta190, 65–70

  13. Farmer, E.E., Ryan, C.A. (1992) Octadecanoic precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell4, 129–134

  14. Fernandez-Maculet, J.C., Yang, S.F. (1992) Isolation and partial characterization of the ethylene-forming enzyme from apple fruit. Plant Physiol.99, 751–754

  15. Fuhrer, J. (1985) Production and release of ethylene from 1-aminocyclopropane-1-carboxylic acid inLemna minor L. in the dark and at different carbon dioxide compensation concentrations. J. Plant Physiol.117, 307–317

  16. Grodzinski, B., Boesel, I., Horton, R.F. (1982) Ethylene release from leaves ofXanthium strumarium L. andZea mays L. J. Exp. Bot.33, 344–354

  17. Guy, M., Kende, H. (1984) Conversion of 1-aminocyclopropane-1-carboxylic acid to ethylene by isolated vacuoles ofPisum sativum L. Planta160, 281–287

  18. Hamilton, A.J., Lycett, G.W., Grierson, D. (1990) Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature346, 284–287

  19. Hamilton, A.J., Bouzayen, M., Grierson, D. (1991) Identification of a tomato gene for the ethylene-forming enzyme by expression in yeast. Proc. Natl. Acad. Sci. USA88, 7434–7437

  20. Hildman, T., Ebneth, M., Pena-Cortes, H., Sanchez-Serrano, J.J., Willmitzer, L., Prat, S. (1992) General roles of abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell4, 1157–1170

  21. Hoffman, N.E., Yang, S.F. (1982) Enhancement of wound-induced ethylene synthesis by ethylene in preclimacteric cantaloupe. Plant Physiol.69, 317–322

  22. Holdsworth, M.J., Bird, C.R., Ray, J., Schuch, W, Grierson, D. (1987) Structure and expression of an ethylene-related mRNA from tomato. Nucleic Acid Res.15, 731–739

  23. Hyodo, H., Hashmito, C., Morozumi, S., Hu, W, Tanaka, K. (1993) Characterizarion and induction of the activity of 1-aminocyclopropane-1-carboxylate oxidase in the wounded mesocarp tissue ofCucurbita maxima. Plant Cell Physiol.34, 667–671

  24. Kende, H. (1993) Ethylene biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol.44, 283–307

  25. Kim, W.T., Silverstone, A., Yip, W.K., Dong, J.G., Yang, S.F. (1992) Induction of 1-aminocyclopropane-1-carboxylate synthase mRNA by auxin in mungbean hypocotyls and apple cultures shoots. Plant Physiol.98, 465–471

  26. Kuai, J., Dilley, D.R. (1992) Extraction, partial purification and characterization of 1-aminocyclopropane-1-carboxylic acid oxidase from apple (Malus domestica Borkh.) fruit. Postharvest Biol. Technol.1, 203–211

  27. Liu, Y, Hoffman, N.E., Yang, S.F. (1985) Promotion by ethylene of the capability to convert 1-aminocyclopropane-1-carboxylic acid to ethylene in preclimacteric tomato and cantaloupe fruits. Plant Physiol.77, 407–411

  28. Lizzardi, P.M. (1983) Methods for the preparation of messenger RNA. Methods Enzymol.96, 24–38

  29. Maniatis, T., Fritsch, E.F., Sambrook, J. (1983) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratories, Cold Spring Harbor, NY

  30. McGarvy, D.J., Christoffersen, R.E. (1992) Characterization and kinetic parameters of ethylene forming enzyme from avocado fruit. J. Biol. Chem.267, 5964–5967

  31. McGarvey, D.J., Yu, H., Christoffersen, R.E. (1990) Nucleotide sequence of a ripening-related cDNA from avocado fruit. Plant Mol. Biol.15, 165–167

  32. Nadeau, J.A., Zhang, X.S., Nair, H., O'Neill, S.D. (1993) Temporal and spatial regulation of 1-aminocyclopropane-1-carboxylate oxidase in the pollination-induced senescence of orchid flowers. Plant Physiol.103, 31–39

  33. Peck, S.C., Olson, D.C., Kende, H. (1993) A cDNA sequence encoding 1-aminocyclopropane-1-carboxylate oxidase from pea. Plant Physiol.101, 689–690

  34. Riov, J., Yang, S.F. (1982) Effects of exogenous ethylene on ethylene production in citrus leaf tissue. Plant Physiol.70, 136–141

  35. Ross, G.S., Knighton, M.L., Lay-Yee, M. (1992) An ethylene-related cDNA from ripening apples. Plant Mol. Biol.19, 213–238

  36. Saltveit, M.E., Dilley, D.R. (1978) Rapidly induced wound ethylene from excised segments of etiolatedPisum sativum L., cv. Alaska. Plant Physiol.61, 447–450

  37. Sisler, E.C., Yang, S.F. (1984) Anti-ethylene effects of cis-2-butene and cyclic olefins. Phytochemistry12, 2765–2768

  38. Spanu, P., Reinhardt, D., Boller, T. (1991) Analysis and cloning of the ethylene-forming enzyme from tomato by functional expression of its mRNA inXenopus laevis oocytes. EMBO J.10, 2007–2013

  39. Theologis, A. (1992) One rotten apple spoils the whole bushel: The role of ethylene in fruit ripening. Cell70, 181–184

  40. Vangronsveld, J., Clijsters, H., Van Poucke, M. (1988) Phytochrome-controlled ethylene biosynthesis of intact etiolated bean seedlings. Planta174, 19–24

  41. Ververidis, P., John, P. (1991) Complete recovery in vitro of ethylene-forming enzyme avtivity. Phytochemistry30, 725–727

  42. Wang, H., Woodson, W.R. (1991) A flower senescence-related mRNA from carnation shares sequence similarity with fruit ripening-related mRNAs involved in ethylene biosynthesis. Plant Physiol.96, 1000–1001

  43. Woodson, W.R., Park, K.Y., Drory, A., Larsen, P.B., Wang, H. (1992) Expression of ethylene biosynthetic pathway transcripts in senescing carnation flowers. Plant Physiol.99, 526–532

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

  45. Yu, Y.-B., Adams, D.O., Yang, S.F. (1979) 1-aminocyclopropane-1-carboxylate synthase, a key enzyme in ethylene biosynthesis. Arch. Biochem. Biophys.198, 280–286

Download references

Author information

Additional information

This work was supported by Grant MCB-9303801 from the National Science Foundation. The GenBank accession numbers for the sequences of pVR-ACO1 and pVR-ACO2 are U06046 and U06047, respectively.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kim, W.T., Yang, S.F. Structure and expression of cDNAs encoding 1-aminocyclopropane-1-carboxylate oxidase homologs isolated from excised mung bean hypocotyls. Planta 194, 223–229 (1994). https://doi.org/10.1007/BF01101681

Download citation

Key words

  • 1-Aminocyclopropane-1-carboxylate oxidase
  • Ethylene
  • Gene expression
  • Hypocotyl excision
  • Vigna
  • Wounding