Abstract
The role of 1-aminocyclopropane-1-carboxylate (ACC) synthase in rose flower petal senescence was investigated. A cDNA library from senescing petals of rose (Rosa × hybrid cv. Kardinal) prepared in λcDNA ZAP Express Vector was probed with a rose-specific 400-bp probe, and seven putative positive ACC synthase clones were isolated. Except for differences in length, the sequences of these clones were identical. A full-length clone, RKacc7, 1,750 bp long, coded for an open reading frame of 480 amino acids that contained the 11 conserved amino acid residues, the substrate and pyridoxal 5′-phosphate binding sites, all of which are characteristic of all ACC synthases. The transcripts prepared in vitro from the full-length clone when translated in rabbit reticulocyte lysates exhibited a 55-KDa polypeptide that comigrated with a polypeptide synthesized from a mRNA fraction isolated from senescing petals, and both were immunoselected by anti-ACC synthase antibodies. Reverse transcriptase-PCR-based studies showed that in planta RKacc7 is specifically expressed in rose petals, ovary and sepals. The expression of ACC synthase increased dramatically as the flower matured to senescence and also correlated positively with ethylene levels. The results of genomic Southern blots probed with RKacc7 are consistent with a pattern expected from a multigene family.
Similar content being viewed by others
References
Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology, 2nd edn. Academic Press, San Diego
Beltran-Destefano LGC, Caeneghem WV, Gielen J, Richard L, Montagu MV, 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
Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1-18
Botella JR, Arteca JM, Schlagnhaufer CD, Arteca RN, Phillips AT (1992) Identification and characterization of a full-length cDNA encoding for an auxin-induced 1-aminocyclopropane-1-caroxylate synthase from etiolated mungbean hypocotyl segment and expression of its mRNA in response to indole-3-acetic acid. Plant Mol Biol 20:425–436
Bui AQ, O’Neill SD (1998) Three 1-aminocyclopropane-1-carboxylate synthase genes regulated by primary and secondary pollination signals in orchid flowers. Plant Physiol 116:419–428
Callis J, Raasch JA, Vieerstra RD (1990) Ubiquitin extension proteins of Arabidopsis thaliana: structure, localization, and expression of their promoters in transgenic tobacco. J Biol Chem 265:12486–12493
Clark DG, Richards C, Hilioti Z, Lind-Iversen S, Brown K (1997) Effect of pollination on accumulation of ACC synthase and ACC oxidase transcripts, ethylene production and flower petal abscission in geranium (Pelargonium × hortorum L.H.Bailey). Plant Mol Biol 34:855–865
Fan JG, Ranu RS, Smith C, Ruan C, Fuller CW (1997) DNA sequencing with [α-33P]-labeled ddNTP terminators: a new approach to DNA sequencing with Thermo Sequenase DNA polymerase. Biotechniques 21:1132–1137
Henskens JAM, Rouwendal GJA,ten Have A, Woltering EJ (1994) Molecular cloning of two different ACC synthase PCR fragments in carnation flowers and organ-specific expression of the corresponding genes. Plant Mol Biol 26:453–458
Huang PL, Parks JE, Rottmann WH, Theologis A (1991) Two genes encoding 1-aminocyclopropane-1-carboxylate synthase in zucchini (Cucubita pepo) are clustered and similar but differentially regulated. Proc Natl Acad Sci USA 88:7021–7025
Hyodo H, Tanaka K, Watanae K (1983) Wound-induced ethylene production and 1-aminocyclopropane-1-caroxylic acid synthase in mesocarp tissue of winter squash fruit. Plant Cell Physiol 24:963–969
Liang X, Abel S, Keller JA, Shen NF, Theologis A (1992) The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proc Natl Acad Sci USA 89:11046–11050
Manning K (1991) Isolation of nucleic acids from plants by differential solvent precipitation. Anal Biochem 195:45–50
Müller R, Lind-Iversen S, Stummann BM, Serek M (2000a) Expression of genes for ethylene biosynthesis enzymes and an ethylene receptor in senescing flowers of miniature roses. J Hortic Sci Biotechnol 75:12–19
Müller R, Stummann BM, Serek M (2000b) Characterization of an ethylene receptor family with differential expression in rose (Rosa hybrida L.) flower. Plant Cell Rep 19:1232–1239
Nichols R, Bufler G, Mor Y, Fujino W, Reid MS (1983) Changes in ethylene production and 1-aminocyclopropane-1-carboxylic acid content of pollinated carnation flowers. J Plant Growth Regul 2:1-8
Peck SC, Kende H (1998) A gene encoding 1-aminocyclopropane-1-carboxylate (ACC) synthase produces two transcripts: elucidation of a conserved response. Plant J 14:573–581
Ranu RS, Levin DH, Delauny J, Ernst V, London IM (1976) Regulation of protein synthesis in rabbit reticulocyte lysates; characterization of inhibition of protein synthesis by a translational inhibitor of initiation from home-deficient lysates and its relationship to the initiation factor which builds Met-tRNAf. Proc Natl Acad Sci USA 73:2720–2724
Ranu RS, Gowda S, Scholthof H, Wu FG, Shepherd RJ (1996) In vitro translation of the full-length RNA transcript of Figwort Mosaic Virus (Caulimovirus). Gene Express 5:143–153
Reid MS, Wu M (1992) Ethylene and flower senescence. Plant Growth Regul 11:37–43
Reid MS, Fujino DW, Hoffman NE, Whitehead CS (1984) 1-aminocyclopropane-1-carboxylic acid (ACC): the transmitted stimulus in pollinated flowers. J Plant Growth Regul 3:189–196
Rottmann WH, Peter GF, Oeller PW, Keller JA, Shen NF, Nagy BP, Taylor LP, Campbell AD, 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 22:937–961
Sato T, Theologis A (1989) Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate, the key enzyme for ethylene biosynthesis in plants. Proc Natl Acad Sci USA 86, 662–6625
Subramaniam K, Abbo S, Ueng PP (1996) Isolation of two differentially expressed wheat ACC synthase cDNAs and the characterization of one of their genes with root-predominant expression. Plant Mol Biol 31:1009–1020
Taylor BH, Manhart JR, Amasino RR (1993) Isolation and characterization of plant DNA. In: Glick BR, Thompson CR (eds) Methods in plant molecular biology and biotechnology. CRC Press, Boca Raton, pp 37–48
Ten Have A, Woltering EJ (1997) Ethylene biosynthetic genes are differentially expressed during carnation (Dianthus caryophyllus L.) flower senescence. Plant Mol Biol 34:89–97
Van Der Straeten D, Van Wiemeersch L, Goodman HM (1990) Cloning and sequence of two different cDNAs encoding 1-aminocyclopropane-1-carboxylate synthase in tomato. Proc Natl Acad Sci USA 87:4859–4863
Van Der Straeten D, Rodrigues-Pousada RA, Villarroel R, Hanley S, Van Montagu M (1992) Cloning, genetic mapping, and expression analysis of an Arabidopsis thaliana gene that encodes 1-aminocyclopropane-1-carboxylate synthase. Proc Natl Acad Sci USA 89:9969–9973
Wang T-W, Arteca RN (1995) Identification and characterization of cDNA encoding ethylene biosynthesis enzymes from Pelargonium × hortorum cv snow mass leaves. Plant Physiol 109:627–636
Wilkinson JQ, Landahan MB, Yen H-C, Giavannoni JJ, Klee HG (1995) An ethylene inducible compound of signal transduction encoded by Never-Ripe. Science 270:1807–1809
Woltering EJ, Van Doorn WG (1988) Role of ethylene in senescence of petals—morphological and taxonomical relationships. J Exp Bot 39:1605–1616
Woodson WR, Brandt AS, Itzhaki H, Maxson JM, Wang H, Park KY, Larsen PB (1993) Ethylene regulation and function of flower senescence-related genes In: Pech JC et al. (eds) Cellular and molecular aspects of plant hormone ethylene. Kluwer, Dordrecht, pp 291–297
Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189
Yip WK, Dong JG, Kenny JW, Thompson GA, Yang SF (1990) Characterization and sequencing of the active site of 1-aminocyclopropane-1-carboxylate synthase. Proc Natl Acad Sci USA 87:7930–7934
Zarembinski TI, 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
Zarembinski TI, Theologis A (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26:1579–1597
Acknowledgements
This work was supported by a research grant by the Tagawa Greenhouses of Brighton, Colorado. We thank David Belles for assistance in the ethylene measurements and Brian Cranmer for the use of the gas chromatography equipment (HP5890).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.S. Chung
Gene access number: AY378152
Rights and permissions
About this article
Cite this article
Wang, D., Fan, J. & Ranu, R.S. Cloning and expression of 1-aminocyclopropane-1-carboxylate synthase cDNA from rosa (Rosa x hybrida). Plant Cell Rep 22, 422–429 (2004). https://doi.org/10.1007/s00299-003-0721-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-003-0721-7