Skip to main content
Log in

Isolation of an Ethylene-induced Putative Nucleotide Laccase in Miniature Roses (Rosa hybrida L.)

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Using differential display we isolated five ethylene-responsive cDNAs from Rosa hybrida L. and identified for the first time an ethylene-induced cDNA homologous to a laccase gene. Three cDNAs were isolated from petioles and two cDNAs from pedicels. Expression levels of all cDNAs in pedicels were higher than in petioles. The laccase homolog cDNA was termed the RhLAC (Rosa hybrida Laccase) gene. The RhLAC gene encodes for a putative protein of 573 amino acids containing three conserved domains characteristic of the multicopper oxidase family. Southern blot hybridization analyses indicated that there are multiple copies of the RhLAC gene in the Rosa species. Comparison of the relative expression of isolated RhLAC in various organs showed that it was highly induced in the leaf abscission zone of petioles and the bud abscission zone of floral bud pedicels, whereas it was low in both leaf blades and petioles. These results suggest that RhLAC may play an important role in senescence and abscission in roses.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Belfield EJ, Ruperti B, Roberts JA, McQueen-Mason S (2005) Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra. J Exp Bot 56:817–823

    Article  PubMed  CAS  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  PubMed  CAS  Google Scholar 

  • Bleecker AB, Patterson SE (1997) Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9:1169–1179

    Article  PubMed  CAS  Google Scholar 

  • Brown KM (1997) Ethylene and abscission. Physiol Plant 100:567–576

    Article  CAS  Google Scholar 

  • Buanong M, Mibus H, Sisler E, Serek M (2005) Efficacy of new inhibitors of ethylene perception in improvement of display quality of miniature potted roses (Rosa hybrida L). Plant Growth Regul 47:29–38

    Article  CAS  Google Scholar 

  • Cai X, Davis EJ, Ballif J, Liang M, Bushman E, Haroldsen V, Torabinejad J, Wu Y (2006) Mutant identification and characterization of the laccase gene family in Arabidopsis. J Exp Bot 57:2563–2569

    Article  PubMed  CAS  Google Scholar 

  • Caparros-Ruiz D, Fornale S, Civardi L, Puigdomenech P, Rigau J (2006) Isolation and characterisation of a family of laccases in maize. Plant Sci 171:217–225

    Article  CAS  Google Scholar 

  • Chen SL, Wang SS, Huttermann A, Altman A (2002) Xylem abscisic acid accelerates leaf abscission by modulating polyamine and ethylene synthesis in water-stressed intact poplar. Trees 16:16–22

    Article  CAS  Google Scholar 

  • Debener T, Mattiesch L (1999) Construction of a genetic linkage map for roses using RAPD and AFLP markers. Theor Appl Genet 99:891–899

    Article  CAS  Google Scholar 

  • Debouck C (1995) Differential display or differential dismay? Curr Opin Biotechnol 6:597–599

    Article  CAS  Google Scholar 

  • del Campillo E, Bennett AB (1996) Pedicel breakstrength and cellulase gene expression during tomato flower abscission. Plant Physiol 111:813–820

    Article  PubMed  CAS  Google Scholar 

  • Devon RS, Porteous DJ, Brookes AJ (1995) Splinkerettes—improved vectorettes for greater efficiency in PCR walking. Nucleic Acids Res 23:1644–1645

    Article  PubMed  CAS  Google Scholar 

  • Ecker J, Davis RW (1987) Plant defense genes are regulated by ethylene. Proc Natl Acad Sci USA 84:5202–5206

    Article  PubMed  CAS  Google Scholar 

  • Francia D, Demaria D, Calderini O, Ferraris L, Valentino D, Arcioni S, Tamietti G, Cardinale F (2007) Wounding induces resistance to pathogens with different lifestyles in tomato: role of ethylene in cross-protection. Plant Cell Environ 30:1357–1365

    Article  PubMed  CAS  Google Scholar 

  • Fujii H, Shimada T, Sugiyama A, Nishikawa F, Endo T, Nakano M, Ikoma Y, Shimizu T, Omura M (2007) Profiling ethylene-responsive genes in mature mandarin fruit using a citrus 22 K oligoarray. Plant Sci 173:340–348

    Article  CAS  Google Scholar 

  • Gonzalez-Carranza Z, Lozoya-Gloria E, Roberts J (1998) Recent developments in abscission: shedding light on the shedding process. Trends Plant Sci 3:10–14

    Article  Google Scholar 

  • Hassan F, Schmidt G, Ankush J, Dorogi Z (2004) Use of silver thiosulphate (STS) and 1-methylcyclopropene (1-MCP) to improve the shelf life of miniature potted rose cv. Amore. Acta Agronom Hung 52:343–350

    Article  CAS  Google Scholar 

  • Higgins DG (1994) CLUSTAL V: multiple alignments of DNA and protein sequences. Methods Mol Biol 25:307–318

    PubMed  CAS  Google Scholar 

  • Jackson MB, Osborne DJ (1972) Abscisic acid, auxin and ethylene in explants abscission. J Exp Bot 23:849–862

    Article  CAS  Google Scholar 

  • Kraft M, Kuglitsch R, Kwiatkowski J, Frank M, Grossmann K (2007) Indole-3-acetic acid and auxin herbicides up-regulate 9-cis-epoxycarotenoid dioxygenase gene expression and abscisic acid accumulation in cleavers (Galium aparine): interaction with ethylene. J Exp Bot 58:1497–1503

    Article  PubMed  CAS  Google Scholar 

  • Kuroda S, Hirose Y, Shiraishi M, Davies E, Abe S (2004) Co-expression of an ethylene receptor gene, ERS1, and ethylene signaling regulator gene, CTR1, in Delphinium during abscission of florets. Plant Physiol Biochem 42:745–751

    Article  PubMed  CAS  Google Scholar 

  • Liang P (2002) A decade of differential display. BioTechniques 33:338–346

    PubMed  CAS  Google Scholar 

  • Liang P, Pardee AB (1992) Differential display of eukaryotic mRNA by means of the polymerase chain reaction. Science 257:967–971

    Article  PubMed  CAS  Google Scholar 

  • Liang M, Davis E, Gardner D, Cai X, Wu Y (2006a) Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 224:1185–1196

    Article  PubMed  CAS  Google Scholar 

  • Liang M, Haroldsen V, Cai X, Wu Y (2006b) Expression of a putative laccase gene, ZmLAC1, in maize primary roots under stress. Plant Cell Environ 29:746–753

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Baird WV (2003) Differential expression of genes regulated in response to drought or salinity stress in sunflower. Crop Sci 43:678–687

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Ma N, Tan H, Liu X, Xue J, Li Y, Gao J (2006) Transcriptional regulation of ethylene receptor and CTR genes involved in ethylene-induced flower opening in cut rose (Rosa hybrida) cv. Samantha. J Exp Bot 57:2763–2773

    Article  CAS  Google Scholar 

  • Makino N, Ogura Y (1971) Oxidation-reduction titrations of copper ions in Rhus-laccase: properties of two types of copper ions in the molecule. J Biochem 69:91–100

    PubMed  CAS  Google Scholar 

  • Mayak S, Halevy AH (1972) Interrelationships of ethylene and abscisic acid in the control of rose petal senescence. Plant Physiol 50:341–346

    Article  PubMed  CAS  Google Scholar 

  • Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565

    Article  PubMed  CAS  Google Scholar 

  • McCaig BC, Meagher RB, Dean JFD (2005) Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana. Planta 221:619–636

    Article  PubMed  CAS  Google Scholar 

  • Mibus H, Tatlioglu T (2004) Molecular characterization and isolation of the F/f gene for femaleness in cucumber (Cucumis sativus L.). Theor Appl Genet 109:1669–1676

    Article  PubMed  CAS  Google Scholar 

  • Müller R, Andersen AS, Serek M (1998) Differences in display life of miniature potted roses (Rosa hybrida L.). Sci Hortic (Amsterdam) 76:59–71

    Article  Google Scholar 

  • Müller R, Stummann BM, Serek M (2000) Characterization of an ethylene receptor family with differential expression in rose (Rosa hybrida L.) flowers. Plant Cell Rep 19:1232–1239

    Article  Google Scholar 

  • Müller R, Stummann BM, Andersen AS (2001a) Comparison of postharvest properties of closely related miniature rose cultivars (Rosa hybrida L.). Sci Hortic (Amsterdam) 91:325–337

    Article  Google Scholar 

  • Müller R, Andersen AS, Serek M, Stummann M (2001b) Effects and interactions of ethylene and abscisic acid in detached and intact miniature rose flowers. Acta Hort 553:173–174

    Google Scholar 

  • O’Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917

    Article  PubMed  CAS  Google Scholar 

  • Patterson SE, Bleecker AB (2004) Ethylene-dependent and -independent processes associated with floral organ abscission in Arabidopsis. Plant Physiol 134:194–203

    Article  PubMed  CAS  Google Scholar 

  • Pourcel L, Routaboul JM, Kerhosa L, Caboche M, Lepiniec L, Debeaujon I (2005) Transparent testa10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17:2966–2980

    Article  PubMed  CAS  Google Scholar 

  • Ramina A, Bonghi C, Giovannoni JJ, Ruperti B, Tonutti P (1999) Differential display and isolation of cDNAs corresponding to mRNAs whose abundance is influenced by ethylene during peach fruitlet abscission. In: Kanellis AK, Chang C, Klee H, Bleecker AB, Pech JC, Grierson D (eds) Biology and biotechnology of the plant hormone ethylene II. Kluwer Academic Publishers, Dordrecht, pp 249–254

    Google Scholar 

  • Reid MS (1995) Ethylene in plant growth, development, and senescence. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology 1995. Kluwer, Dordrecht, pp 486–508

    Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Sane AP, Tripathi SK, Nath P (2007) Petal abscission in rose (Rosa bourboniana var Gruss an Teplitz) is associated with the enhanced expression of an alpha expansin gene, RbEXPA1. Plant Sci 172:481–487

    Article  CAS  Google Scholar 

  • Saltveit MEJ (1978) Simple apparatus for diluting and dispensing trace concentrations of ethylene in air. HortSci 13:249–251

    CAS  Google Scholar 

  • Serek M, Reid MS (1994) A volatile ethylene inhibitor improves the postharvest life of potted roses. J Am Soc Hort Sci 119:572–577

    CAS  Google Scholar 

  • Serek M, Sisler EC, Reid MS (1996) Ethylene and the postharvest performance of miniature roses. ISHS Acta Hortic 424:81–86

    Google Scholar 

  • Sexton R, Lewis LN, Trewavas AJ, Kelly P (1985) Ethylene and abscission. In: Roberts JA, Tucker GA (eds) Ethylene and plant development. Butterworths, London, pp 173–196

    Google Scholar 

  • Sisler EC, Yang SF (1984) Ethylene, the gaseous plant hormone. BioScience 34:234–238

    Article  CAS  Google Scholar 

  • Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96:2563–2606

    Article  PubMed  CAS  Google Scholar 

  • Sriskandarajah S, Mibus H, Serek M (2007) Transgenic Campanula carpatica plants with reduced ethylene sensitivity. Plant Cell Rep 26:805–813

    Article  PubMed  CAS  Google Scholar 

  • Stotz HU, Pittendrigh B, Kroymann J, Weniger K, Fritsche J, Bauke A, Mitchell-Olds T (2000) Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cottonworm but not diamondback moth. Plant Physiol 124:1007–1017

    Article  PubMed  CAS  Google Scholar 

  • Sun Y, Zhou X, Ma H (2007) Genome-wide analysis of Kelch repeat containing F-box family. J Integr Plant Biol 49:940–952

    Article  CAS  Google Scholar 

  • Suttle JC, Hultstrand JF (1993) Involvement of abscisic acid in ethylene-induced cotyledon abscission in cotton seedlings. Plant Physiol 101:641–646

    PubMed  CAS  Google Scholar 

  • Tucker ML, Sexton R, del Campillo E, Lewis L (1988) Bean abscission cellulase, characterization of a cDNA clone and regulation of gene expression by ethylene and auxin. Plant Physiol 88:1257–1262

    PubMed  CAS  Google Scholar 

  • Uheda E, Nakamura S (2000) Abscission of Azolla branches induced by ethylene and sodium azide. Plant Cell Physiol 41:1365–1372

    Article  PubMed  CAS  Google Scholar 

  • Van Dijck P, Mascorro-Gallardo JO, De Bus M, Royackers K, Iturriaga G, Thevelein JM (2002) Truncation of Arabidopsis thaliana and Selaginella lepidophylla trehalose-6-phosphate synthase unlocks high catalytic activity and supports high trehalose levels on expression in yeast. Biochem J 366:63–71

    PubMed  Google Scholar 

  • Van Doorn WG (2002) Effect of ethylene on flower abscission: a survey. Ann Bot 89:689–693

    Article  PubMed  CAS  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):s131–s151

    PubMed  CAS  Google Scholar 

  • Wei JZ, Tirajoh A, Effendy J, Plant AL (2000) Characterization of salt-induced changes in gene expression in tomato (Lycopersicon esculentum) roots and the role played by abscisic acid. Plant Sci 159:135–148

    Article  PubMed  CAS  Google Scholar 

  • Xu Q, Wen X, Deng X (2004) A simple protocol for isolating genomic DNA from chestnut rose (Rosa roxburghii Tratt) for RFLP and PCR analyses. Plant Mol Biol Rep 22:301a–301g

    Article  Google Scholar 

  • Yamazaki M, Saito K (2002) Differential display analysis of gene expression in plants. Cell Mol Life Sci 59:1246–1255

    Article  PubMed  CAS  Google Scholar 

  • Zhong GY, Burns JK (2003) Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol Biol 53:117–131

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by a PhD grant (to NA) from the Ministry of Science, Research and Technology of Iran. The authors would like to thank Prof. Bjarne M. Stummann for critical reading of the manuscript and valuable comments, and Prof. Errol Hewett (Massey University, Palmerston North, New Zealand) for linguistic editing of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Margrethe Serek.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahmadi, N., Mibus, H. & Serek, M. Isolation of an Ethylene-induced Putative Nucleotide Laccase in Miniature Roses (Rosa hybrida L.). J Plant Growth Regul 27, 320–330 (2008). https://doi.org/10.1007/s00344-008-9059-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-008-9059-2

Keywords

Navigation