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Evidence for Positive Regulation by Gibberellins and Ethylene of ACC Oxidase Expression and Activity During Transition From Dormancy to Germination in Fagus sylvatica L. Seeds

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Abstract

1-aminocyclopropane-1-carboxylic acid (ACC) oxidase is a key enzyme in the ethylene biosynthesis pathway. In the present report the changes in ACC content, ACC oxidase activity and ethylene production have been examined in Fagus sylvatica L. dormant seeds after stratification and different treatments that maintain or release dormancy. Additionally, a cDNA encoding an ACC oxidase (ACO) from Fagus sylvatica has been isolated and characterized. This clone, named FsACO1, exhibits high homology to ACC oxidases from several plant species and the corresponding enzyme, expressed in Escherichia coli as a fusion protein, is active in converting ACC into ethylene. The transcript levels of FsACO1 are correlated with the ACC content, the ethylene production and the ACC oxidase activity measured in vitro as well as with the germination percentages observed in the seeds under the different treatments used in this study. There is a drastic increase in all these parameters when seeds are treated with GA3 or ethephon (which releases ethylene in solution), hormones previously proven to be efficient in the breaking of dormancy of beech seeds. The stimulatory effect of ethephon is reverted by paclobutrazol, a well known GA biosynthesis inhibitor. These results indicate that ethylene biosynthesis is positively regulated by both gibberellins and ethylene and suggest a cross-talk regulation by these two hormones of the processes involved in the transition from seed dormancy to germination.

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References

  1. FB Abeles (1973) Ethylene in plant biology Academic Press New York

    Google Scholar 

  2. FB Abeles PW Morgan ME Salveit (1992) Ethylene in plant biology EditionNumber2nd ed Academic Press San Diego

    Google Scholar 

  3. P Achard WH Vriezen D Straeten Particlevan der NP Harberd (2003) ArticleTitleEthylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor factor Plant Cell 15 2816–2825 Occurrence Handle10.1105/tpc.015685 Occurrence Handle1:CAS:528:DC%2BD2cXhtVSitQ%3D%3D Occurrence Handle14615596

    Article  CAS  PubMed  Google Scholar 

  4. EK Akamine T Goo (1978) ArticleTitleRespiration and ethylene production in mammee apple (Mammea americana L) J Am Soc Hortic Sci 103 308–310 Occurrence Handle1:CAS:528:DyaE1cXltVersLw%3D

    CAS  Google Scholar 

  5. L Alexander D Grierson (2002) ArticleTitleEthylene biosynthesis and action in tomato: a model for climateric fruit ripening J Exp Bot 53 2039–2055 Occurrence Handle10.1093/jxb/erf072 Occurrence Handle1:CAS:528:DC%2BD38XnsVGks7s%3D Occurrence Handle12324528

    Article  CAS  PubMed  Google Scholar 

  6. A Avni BA Bailey AK Mattoo JD Anderson (1994) ArticleTitleInduction of ethylene biosynthesis in Nicotiana tabacum by a Trichoderma viride xylanase is correlated to the accumulation of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase and ACC oxidase transcripts Plant Physiol 106 1049–1055 Occurrence Handle10.1104/pp.106.3.1049 Occurrence Handle1:CAS:528:DyaK2MXitlentr4%3D Occurrence Handle7824643

    Article  CAS  PubMed  Google Scholar 

  7. CS Barry B Blume M Bouzayen W Cooper AJ Hamilton D Grierson (1996) ArticleTitleDifferential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato Plant J 9 525–535 Occurrence Handle10.1046/j.1365-313X.1996.09040525.x Occurrence Handle1:CAS:528:DyaK28XivFWntLg%3D Occurrence Handle8624515

    Article  CAS  PubMed  Google Scholar 

  8. N Beaudoin C Serizet F Gosti J Giraudat (2000) ArticleTitleInteractions between abscisic acid and ethylene signaling cascades Plant Cell 12 1103–1115 Occurrence Handle10.1105/tpc.12.7.1103 Occurrence Handle1:CAS:528:DC%2BD3cXlslygtLo%3D Occurrence Handle10899977

    Article  CAS  PubMed  Google Scholar 

  9. AB Bleecker H Kende (2000) ArticleTitleEthylene: a gaseous signal molecule in plants Annu Rev Cell Dev Biol 16 1–18 Occurrence Handle10.1146/annurev.cellbio.16.1.1 Occurrence Handle1:CAS:528:DC%2BD3MXpvFOj Occurrence Handle11031228

    Article  CAS  PubMed  Google Scholar 

  10. T Boller RC Herner H Kende (1979) ArticleTitleAssay for an enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylic acid Planta 145 293–303 Occurrence Handle1:CAS:528:DyaE1MXktFKjt7g%3D

    CAS  Google Scholar 

  11. MM Bradford (1976) ArticleTitleA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 248–254 Occurrence Handle10.1006/abio.1976.9999 Occurrence Handle1:CAS:528:DyaE28XksVehtrY%3D Occurrence Handle942051

    Article  CAS  PubMed  Google Scholar 

  12. SM Brady P McCourt (2003) ArticleTitleHormone cross-talk in seed dormancy J Plant Growth Regul 22 25–31 Occurrence Handle10.1007/s00344-003-0018-7 Occurrence Handle1:CAS:528:DC%2BD3sXosF2ktbs%3D

    Article  CAS  Google Scholar 

  13. NM Brunhuber JL Mort RE Christoffersen NO Reich (2000) ArticleTitleSteady-state kinetic mechanism of recombinant avocado ACC oxidase: initial velocity and inhibitor studies Biochemistry 39 10738–10739

    Google Scholar 

  14. AP Calvo JA Jiménez C Nicolás G Nicolás D Rodriguez (2003) Isolation and characterization of genes related with the breaking of beechnuts dormancy and putatively involved in ethylene signal perception and transduction G Nicolás KJ Bradford D Come H Pritchard (Eds) The biology of seeds: recent research advances 2003 CAB International Wallingford 141–149

    Google Scholar 

  15. AP Calvo C Nicolás G Nicolás D Rodríguez (2004) ArticleTitleEvidence of a cross-talk regulation of a GA 20-oxidase (FsGA20ox1) by gibberellins and ethylene during the breaking of dormancy in Fagus sylvatica L. seeds Physiol Plant 120 623–630 Occurrence Handle10.1111/j.0031-9317.2004.0270.x Occurrence Handle1:CAS:528:DC%2BD2cXjtFWmu7g%3D Occurrence Handle15032824

    Article  CAS  PubMed  Google Scholar 

  16. D Martins ParticleDe C Mariania (1999) ArticleTitleSilencing gene expression of the ethylene-forming enzyme results in a reversible inhibition of ovule development in transgenic tobacco plants Plant Cell 11 1061–1072 Occurrence Handle10.1105/tpc.11.6.1061 Occurrence Handle10368177

    Article  PubMed  Google Scholar 

  17. A Drory S Mayak WR Woodson (1993) ArticleTitleExpression of ethylene biosynthetic pathway mRNA is spatially regulated within carnation flower petals J Plant Physiol 141 663–667 Occurrence Handle1:CAS:528:DyaK3sXltFemsrw%3D

    CAS  Google Scholar 

  18. R Fluhr A Mattoo (1996) ArticleTitleEthylene-biosynthesis and perception Crit Rev Plant Sci 15 479–523 Occurrence Handle1:CAS:528:DyaK28XmsFSqs78%3D

    CAS  Google Scholar 

  19. L Ge JZ Liu WS Wong WLW Hsiao K Chong ZK Xu SF Yang SD Kung N Li (2000) ArticleTitleIdentification of a novel multiple environmental factor-responsive 1-aminocyclopropane-1-carboxylate synthase gene from tobacco Plant Cell Environ 23 1169–1182 Occurrence Handle10.1046/j.1365-3040.2000.00618.x Occurrence Handle1:CAS:528:DC%2BD3cXos1yms7k%3D

    Article  CAS  Google Scholar 

  20. MC Gómez-Jiménez AJ Matilla D Garrido (1998) ArticleTitleIsolation and characterization of a cDNA encoding an ACC oxidase from Cicer arietinum and its expression during embryogenesis and seed germination Aust J Plant Physiol 25 765–773

    Google Scholar 

  21. R Johnson JR Ecker (1998) ArticleTitleEthylene gas signal transduction pathway: molecular perspective Annu Rev Genet 32 227–254 Occurrence Handle10.1146/annurev.genet.32.1.227 Occurrence Handle1:CAS:528:DyaK1MXjvFWlsw%3D%3D Occurrence Handle9928480

    Article  CAS  PubMed  Google Scholar 

  22. CM Karssen S Zagorski J Kepczynski SPC Groot (1989) ArticleTitleKey role for endogenous gibberellins in the control of seed germination Ann Bot-London 63 71–80 Occurrence Handle1:CAS:528:DyaL1MXhtlahurc%3D

    CAS  Google Scholar 

  23. J Kepczynski E Kepczynska (1997) ArticleTitleEthylene in seed dormancy and germination Physiol Plant 101 720–726 Occurrence Handle10.1034/j.1399-3054.1997.1010407.x Occurrence Handle1:CAS:528:DyaK1cXivFaksA%3D%3D

    Article  CAS  Google Scholar 

  24. M Kooznneef CM Karssen (1994) Seed dormancy and germination CR Somerville EM Meyerowitz (Eds) Arabidopsis 1994 Cold Spring Harbour Laboratory Press New York 313–334

    Google Scholar 

  25. KA Lawton SL Potter S Uknes J Ryals (1994) ArticleTitleAcquired resistance signal transduction in Arabidopsis is ethylene independent Plant Cell 6 581–588 Occurrence Handle10.1105/tpc.6.5.581 Occurrence Handle1:CAS:528:DyaK2cXltlSis78%3D Occurrence Handle12244251

    Article  CAS  PubMed  Google Scholar 

  26. MCC Lizada SF Yang (1979) ArticleTitleSimple and sensitive assay for 1-aminocyclopropane-1-carboxylic acid Anal Biochem 100 140–145 Occurrence Handle1:CAS:528:DyaL3cXlsVChuw%3D%3D Occurrence Handle543532

    CAS  PubMed  Google Scholar 

  27. O Lorenzo D Rodríguez G Nicolás PL Rodríguez C Nicolás (2001) ArticleTitleA new protein phosphatase 2C (FsPP2C1) induced by ABA is specifically expressed in dormant seeds of Fagus sylvatica L Plant Physiol 125 1949–1956 Occurrence Handle10.1104/pp.125.4.1949 Occurrence Handle1:CAS:528:DC%2BD3MXjtFKqur4%3D Occurrence Handle11299374

    Article  CAS  PubMed  Google Scholar 

  28. AJ Matilla (2000) ArticleTitleEthylene in seed formation and germination Seed Sci Res 10 111–126 Occurrence Handle1:CAS:528:DC%2BD3cXlsFKksbs%3D

    CAS  Google Scholar 

  29. JA Nadeau SZ Xion H Nair SD O’Neill (1993) ArticleTitleTemporal and spatial regulation of 1-aminocyclopropane-1-carboxylate oxidase in the pollination-induced senescence of orchid flowers Plant Physiol 103 31–39 Occurrence Handle10.1104/pp.103.1.31 Occurrence Handle1:CAS:528:DyaK2cXntlelsw%3D%3D Occurrence Handle7516081

    Article  CAS  PubMed  Google Scholar 

  30. C Nicolás G Nicolás D Rodríguez (1996) ArticleTitleAntagonistic effects of abscisic acid and gibberellic acid on the breaking of dormancy of Fagus sylvatica seeds Physiol Plant 96 244–250 Occurrence Handle10.1034/j.1399-3054.1996.960212.x

    Article  Google Scholar 

  31. C Nicolás D Rodríguez F Poulsen EN Eriksen G Nicolás (1997) ArticleTitleThe expression of an abscisic acid responsive Glycine-Rich protein coincides with the level of seed dormancy in Fagus sylvatica Plant Cell Physiol 38 1303–1310 Occurrence Handle9522463

    PubMed  Google Scholar 

  32. WR Pearson DJ Lipman (1988) ArticleTitleImproved tools for biological sequence analysis Proc Natl Acad Sci USA 85 2444–2448 Occurrence Handle1:CAS:528:DyaL1cXktFyit78%3D Occurrence Handle3162770

    CAS  PubMed  Google Scholar 

  33. L Petruzelli I Coraggio G Leubner-Metzger (2000) ArticleTitleEthylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclopropane-1-carboxylic acid oxidase Planta 211 144–149 Occurrence Handle10.1007/s004250000274 Occurrence Handle10923715

    Article  PubMed  Google Scholar 

  34. PL Roach IJ Clifton V Fulop K Harlos GJ Burton J Hajdu I Anderson CI Schofield JE Baldwin (1995) ArticleTitleCrystal structure of isopenicilin N synthase is the first from a new structural family of enzymes Nature 375 700–704 Occurrence Handle10.1038/375700a0 Occurrence Handle1:CAS:528:DyaK2MXmsFKrt7c%3D Occurrence Handle7791906

    Article  CAS  PubMed  Google Scholar 

  35. MC Rodríguez-Gacio AJ Matilla (2001) ArticleTitleThe last step of the ethylene biosynthesis pathway in turnip tops (Brassica rapa) and its inhibition during desiccation Physiol Plant 112 273–279 Occurrence Handle10.1034/j.1399-3054.2001.1120216.x Occurrence Handle11454233

    Article  PubMed  Google Scholar 

  36. MC Rodríguez-Gacio C Nicolás AJ Matilla (2004) ArticleTitleThe final step of the ethylene biosynthesis pathway in turnip tops (Brassica rapa L. cv. Rapa): molecular characterization of the 1-aminocyclopropane-1-carboxylate oxidase BrACO1 throughout zygotic embryogenesis and germination of heterogeneous seeds Physiol Plant 121 132 Occurrence Handle10.1111/j.0031-9317.2004.00300.x Occurrence Handle15086827

    Article  PubMed  Google Scholar 

  37. P Ververidis P John (1991) ArticleTitleComplete recovery in vitro of ethylene-forming enzyme activity Phytochemistry 30 725–727 Occurrence Handle10.1016/0031-9422(91)85241-Q Occurrence Handle1:CAS:528:DyaK3MXhsF2mu74%3D

    Article  CAS  Google Scholar 

  38. LA Voesenek JJ Benschop J Bou MC Cox HW Groeneveld FF Millenaar RA Vreeburg AJ Peeters (2003) ArticleTitleInteractions between plant hormones regulate submergence-induced shoot elongation in the flooding tolerant dicot Rumex palustris Ann Bot-London 91 205–211 Occurrence Handle10.1093/aob/mcf116 Occurrence Handle1:CAS:528:DC%2BD3sXitVCksbg%3D

    Article  CAS  Google Scholar 

  39. WH Vriezen R Hulzink C Mariani LA Voeseneck (1999) ArticleTitle1-aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynthesis in Rumex palustris during submergence Plant Physiol 121 189–196 Occurrence Handle10.1104/pp.121.1.189 Occurrence Handle1:CAS:528:DyaK1MXmtFGlsbo%3D Occurrence Handle10482674

    Article  CAS  PubMed  Google Scholar 

  40. KLC Wang H Li JR Ecker (2002) ArticleTitleEthylene biosynthesis and signaling networks The Plant Cell . IssueIDsuppl S131–S151

    Google Scholar 

  41. NN Wang SF Yang YY Charng (2001) ArticleTitleDifferential expresión of 1-aminocyclopropane-1-carboxylate synthase genes during orchid flower senescence induced by the protein phosphatase inhibitor okadaic acid Plant Physiol 126 253–260 Occurrence Handle10.1104/pp.126.1.253 Occurrence Handle1:CAS:528:DC%2BD3MXjslWjsbg%3D Occurrence Handle11351088

    Article  CAS  PubMed  Google Scholar 

  42. SF Yang (1969) ArticleTitleEthylene evolution from 2-chloroethylphosphonic acid Plant Physiol 44 1203–1204 Occurrence Handle1:CAS:528:DyaE3cXitlOg

    CAS  Google Scholar 

  43. SF Yang NE Hoffman (1984) ArticleTitleEthylene biosynthesis and its regulation in higher plants Annu Rev Plant Physiol 35 155–189 Occurrence Handle10.1146/annurev.pp.35.060184.001103 Occurrence Handle1:CAS:528:DyaL2cXkvVOnsrg%3D

    Article  CAS  Google Scholar 

  44. Z Zhang CJ Schofield JE Baldwin P Thomas P John (1995) ArticleTitleExpression, purification and characterization of 1-aminocyclopropane-1-carboxylate oxidase from tomato in Escherichia coli Biochem J 307 77–85 Occurrence Handle1:CAS:528:DyaK2MXkvFCitbc%3D Occurrence Handle7717997

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants BFI2000-1361 from the Ministerio de Ciencia y Tecnología (Spain) and SA010/02 from Junta de Castilla y León.

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Authors and Affiliations

  1. Departamento de Fisiología Vegetal, Centro Hispano-Luso de Investigaciones Agrarias, Facultad de Biología, Universidad de Salamanca, Campus Miguel de Unamuno, 37007 Salamanca, Spain

    Angel Pablo Calvo, Carlos Nicolás, Oscar Lorenzo, Gregorio Nicolás & Dolores Rodríguez

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  1. Angel Pablo Calvo
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  2. Carlos Nicolás
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  3. Oscar Lorenzo
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  4. Gregorio Nicolás
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  5. Dolores Rodríguez
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Correspondence to Dolores Rodríguez.

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Calvo, A.P., Nicolás, C., Lorenzo, O. et al. Evidence for Positive Regulation by Gibberellins and Ethylene of ACC Oxidase Expression and Activity During Transition From Dormancy to Germination in Fagus sylvatica L. Seeds. J Plant Growth Regul 23, 44–53 (2004). https://doi.org/10.1007/s00344-004-0074-7

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