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Molecular Biology Reports

, Volume 38, Issue 5, pp 3327–3337 | Cite as

Characterization of a F-box gene up-regulated by phytohormones and upon biotic and abiotic stresses in grapevine

  • Sandra Paquis
  • Florence Mazeyrat-Gourbeyre
  • Olivier Fernandez
  • Jérôme Crouzet
  • Christophe Clément
  • Fabienne Baillieul
  • Stéphan DoreyEmail author
Article

Abstract

F-box proteins are key components of the ubiquitin (Ub)/26S proteasome pathway that mediates selective degradation of regulatory proteins involved in a wide variety of cellular processes affecting eukaryotic cells. In plants, F-box genes form one of the largest multigene superfamilies and control many important biological functions. Among the F-box genes characterized to date only few have been involved in the regulation of plant defense responses. Moreover, no F-box genes have been studied and characterized in grapevine. Using a differential display approach we isolated a F-box gene (BIG-24.1), which is up-regulated during Botrytis cinerea infection of grapevine leaves. BIG-24.1 encodes a polypeptide of 386 amino acids with a conserved F-box domain in the N-terminus region and a kelch domain. By investigating expression profiles of BIG-24.1, we show that the gene expression is strongly stimulated in B. cinerea infected berries and in grapevine cells challenged by MAMP rhamnolipids, a non-host bacterium and an endophytic rhizobacterium. The gene is also strongly induced by abiotic stresses including UV-C and wounding or by salicylic acid, methyl-jasmonate, ethylene and abscisic acid that are known to be involved in defense signalling pathways. In addition, sequence analysis of the BIG-24.1 promoter revealed the presence of several regulatory elements involved in the activation of plant defense responses.

Keywords

Abiotic stress Biotic stress Defense responses F-box Phytohormones Plant 

Notes

Acknowledgments

We thank Cathy Hachet and Fanja Rabenoelina for technical support. This work was supported by a fund from Europôl’Agro.

References

  1. 1.
    Ait Barka E, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72:7246–7252PubMedCrossRefGoogle Scholar
  2. 2.
    Andrade MA, Gonzalez-Guzman M, Serrano R, Rodriguez PL (2001) A combination of the F-box motif and kelch repeats defines a large Arabidopsis family of F-box proteins. Plant Mol Biol 46:603–614PubMedCrossRefGoogle Scholar
  3. 3.
    Bézier A, Lambert B, Baillieul F (2002) Study of defense-related gene expression in grapevine leaves and berries infected with Botrytis cinerea. Eur J Plant Pathol 108:111–120CrossRefGoogle Scholar
  4. 4.
    Bézier A, Mazeyrat-Gourbeyre F, Bonomelli A, Varnier AL, Paquis S, Hachet C, Manteau S, Dorey S, Dhondt-Cordelier C, Clément C, Baillieul F (2007) Identification of grapevine genes regulated upon Botrytis cinerea infection by differential display. In: Jeandet P, Clément C, Conreux A (eds) Macromolecules and secondary metabolites of grapevine and wine, Intercept, Lavoisier, Paris, London, pp 69–74Google Scholar
  5. 5.
    Bonomelli A, Mercier L, Franchel J, Baillieul F, Benizri E, Mauro MC (2004) Response of grapevine defenses to UV-C exposure. Am J Enol Vitic 55:51–59Google Scholar
  6. 6.
    Bordiec S, Paquis S, Lacroix H, Dhondt S, Ait Barka E, Kauffmann S, Jeandet P, Mazeyrat-Gourbeyre F, Clement C, Baillieul F, Dorey S (2010) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot. doi: 10.1093/jxb/erq291
  7. 7.
    Borie B, Jeandet P, Parize A, Bessis R, Adrian M (2004) Resveratrol and stilbene synthase mRNA production in grapevine leaves treated with biotic and abiotic phytoalexin elicitors. Am J Enol Vitic 55:60–64Google Scholar
  8. 8.
    Chico JM, Chini A, Fonseca S, Solano R (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 11:486–494PubMedCrossRefGoogle Scholar
  9. 9.
    Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68:81–92PubMedCrossRefGoogle Scholar
  10. 10.
    Compant S, Reiter B, Sessitsch A, Nowak J, Clement C, Ait Barka E (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693PubMedCrossRefGoogle Scholar
  11. 11.
    Derckel JP, Baillieul F, Manteau S, Audran JC, Haye B, Lambert B, Legendre L (1999) Differential induction of grapevine defenses by two strains of Botrytis cinerea. Phytopathology 89:197–203PubMedCrossRefGoogle Scholar
  12. 12.
    Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371PubMedCrossRefGoogle Scholar
  13. 13.
    Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedCrossRefGoogle Scholar
  14. 14.
    Fujita M, Mizukado S, Fujita Y, Ichikawa T, Nakazawa M, Seki M, Matsui M, Yamaguchi-Shinozaki K, Shinozaki K (2007) Identification of stress-tolerance-related transcription-factor genes via mini-scale Full-length cDNA Over-eXpressor (FOX) gene hunting system. Biochem Biophys Res Commun 364:250–257PubMedCrossRefGoogle Scholar
  15. 15.
    Garreton V, Carpinelli J, Jordana X, Holuigue L (2002) The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol 130:1516–1526PubMedCrossRefGoogle Scholar
  16. 16.
    Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook, Humana Press, pp 571–607Google Scholar
  17. 17.
    Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791PubMedCrossRefGoogle Scholar
  18. 18.
    Ho MS, Ou C, Chan YR, Chien CT, Pi H (2008) The utility F-box for protein destruction. Cell Mol Life Sci 65:1977–2000PubMedCrossRefGoogle Scholar
  19. 19.
    Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467PubMedCrossRefGoogle Scholar
  20. 20.
    Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483PubMedCrossRefGoogle Scholar
  21. 21.
    Kazan K (2006) Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends Plant Sci 11:109–112PubMedCrossRefGoogle Scholar
  22. 22.
    Kim HS, Delaney TP (2002) Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell 14:1469–1482PubMedCrossRefGoogle Scholar
  23. 23.
    Klotz KL, Lagrimini LM (1996) Phytohormone control of the tobacco anionic peroxidase promoter. Plant Mol Biol 31:565–573PubMedCrossRefGoogle Scholar
  24. 24.
    Kurepa J, Wang S, Li Y, Smalle J (2009) Proteasome regulation, plant growth and stress tolerance. Plant Signal Behav 4:924–927PubMedCrossRefGoogle Scholar
  25. 25.
    Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9:631–638PubMedCrossRefGoogle Scholar
  26. 26.
    Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126–143PubMedCrossRefGoogle Scholar
  27. 27.
    Meier U (2001) Growth stages of mono- and dicotyledonous plants. BBCH monograph. In: Meier U (ed) Grapevine. Blackwell Wissenschaft-verlag, Berlin, pp 93–95Google Scholar
  28. 28.
    Niggeweg R, Thurow C, Kegler C, Gatz C (2000) Tobacco transcription factor TGA2.2 is the main component of as-1-binding factor ASF-1 and is involved in salicylic acid- and auxin-inducible expression of as-1-containing target promoters. J Biol Chem 275:19897–19905PubMedCrossRefGoogle Scholar
  29. 29.
    Ogawa M, Hanada A, Yamuchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604PubMedCrossRefGoogle Scholar
  30. 30.
    Oono Y, Seki M, Nanjo T, Narusaka M, Fujita M, Satoh R, Satou M, Sakurai T, Ishida J, Akiyama K, Iida K, Maruyama K, Satoh S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca 7000 full-length cDNA microarray. Plant J 34:868–887PubMedCrossRefGoogle Scholar
  31. 31.
    Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655PubMedCrossRefGoogle Scholar
  32. 32.
    Petit AN, Baillieul F, Vaillant-Gaveau N, Jacquens L, Conreux A, Jeandet P, Clement C, Fontaine F (2009) Low responsiveness of grapevine flowers and berries at fruit set to UV-C irradiation. J Exp Bot 60:1155–1162PubMedCrossRefGoogle Scholar
  33. 33.
    Rawat R, Xu ZF, Yao KM, Chye ML (2005) Identification of cis-elements for ethylene and circadian regulation of the Solanum melongena gene encoding cysteine proteinase. Plant Mol Biol 57:629–643PubMedCrossRefGoogle Scholar
  34. 34.
    Redman J, Whitecraft J, Johnson C, Arias J (2002) Abiotic and biotic stress differentially stimulate as-1 element activity in Arabidopsis. Plant Cell Rep 21:180–185CrossRefGoogle Scholar
  35. 35.
    Robert N, Ferran J, Breda C, Coutos-Thévenot P, Boulay M, Buffard D, Esnault R (2001) Molecular characterization of the incompatible interaction of Vitis vinifera leaves with Pseudomonas syringae pv. pisi: expression o genes coding for stilbene synthase and class 10 PR protein. Eur J Plant Pathol 107:249–261CrossRefGoogle Scholar
  36. 36.
    Robert N, Roche K, Lebeau Y, Breda C, Boulay M, Esnault R, Buffard D (2002) Expression of grapevine chitinase genes in berries and leaves infected by fungal or bacterial pathogens. Plant Sci 162:389–400CrossRefGoogle Scholar
  37. 37.
    Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590PubMedCrossRefGoogle Scholar
  38. 38.
    Somers DE, Fujiwara S (2009) Thinking outside the F-box: novel ligands for novel receptors. Trends Plant Sci 14:206–213PubMedCrossRefGoogle Scholar
  39. 39.
    Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M, Witucka-Wall H, Gibon Y, Usadel B, Poree F, Piques MC, Von Korff M, Steinhauser MC, Keurentjes JJ, Guenther M, Hoehne M, Selbig J, Fernie AR, Altmann T, Stitt M (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci USA 106:10348–10353PubMedCrossRefGoogle Scholar
  40. 40.
    Sun L, Shi L, Li W, Yu W, Liang J, Zhang H, Yang X, Wang Y, Li R, Yao X, Yi X, Shang Y (2009) JFK, a Kelch domain-containing F-box protein, links the SCF complex to p53 regulation. Proc Natl Acad Sci USA 106:10195–10200PubMedCrossRefGoogle Scholar
  41. 41.
    Tan X, Zheng N (2009) Hormone signaling through protein destruction: a lesson from plants. Am J Physiol Endocrinol Metab 296:E223–E227PubMedCrossRefGoogle Scholar
  42. 42.
    van den Burg HA, Tsitsigiannis DI, Rowland O, Lo J, Rallapalli G, Maclean D, Takken FL, Jones JD (2008) The F-box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato. Plant Cell 20:697–719PubMedCrossRefGoogle Scholar
  43. 43.
    Varnier AL, Sanchez L, Vatsa P, Boudesocque L, Garcia-Brugger A, Rabenoelina F, Sorokin A, Renault JH, Kauffmann S, Pugin A, Clément C, Baillieul F, Dorey S (2009) Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine. Plant Cell Environ 32:178–193PubMedCrossRefGoogle Scholar
  44. 44.
    Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Dematte L, Mraz A, Battilana J, Stormo K, Costa F, Tao Q, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Van de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2:e1326PubMedCrossRefGoogle Scholar
  45. 45.
    Wang Z, Dai L, Jiang Z, Peng W, Zhang L, Wang G, Xie D (2005) GmCOI1, a soybean F-box protein gene, shows ability to mediate jasmonate-regulated plant defense and fertility in Arabidopsis. Mol Plant-Microbe Interact 18:1285–1295PubMedCrossRefGoogle Scholar
  46. 46.
    Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094PubMedCrossRefGoogle Scholar
  47. 47.
    Xu G, Ma H, Nei M, Kong H (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci USA 106:835–840PubMedCrossRefGoogle Scholar
  48. 48.
    Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T, Tschaplinski TJ, Weston DJ, Ranjan P, Tuskan GA (2008) The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148:1189–1200PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Sandra Paquis
    • 1
  • Florence Mazeyrat-Gourbeyre
    • 1
  • Olivier Fernandez
    • 1
  • Jérôme Crouzet
    • 1
  • Christophe Clément
    • 1
  • Fabienne Baillieul
    • 1
  • Stéphan Dorey
    • 1
    Email author
  1. 1.URVVC-SE-EA 2069, Stress, Défenses et Reproduction des PlantesUniversité de Reims Champagne-ArdenneReims cedex 2France

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