Abstract
It has been clearly established that phytopathogenic fungi, bacteria, and viruses exert biotic stresses on plants. Much less is known, however, about the interactions between enological species of yeast and their host plants. In a previous study, we described how Saccharomyces cerevisiae, the most common enological yeast, can act as a grapevine (Vitis vinifera L.) pathogen, causing growth retardation or plant death. In the present in vitro study on 11 strains of yeast belonging to different genera, which often occur on the surfaces of vineyard grapes and V. vinifera, a link was found to exist between strain phytopathogenecity and pseudohyphal growth habits and/or endopolygalacturonase activity. The results obtained here are consistent with earlier findings showing that the phytopathogenicity of yeast strains depends on the filamentous growth process, and show that endopolygalacturonase alone is not responsible for the invasion of plants tissues. The mechanisms observed here may be of significant ecological importance and may help to explain the long periods of yeast survival found to occur in vineyards.
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References
F Banuett (1995) ArticleTitleGenetics of Ustilago maydis, a fungal pathogen that induces tumors in maize Annu Rev Genet Rev 29 179–208 Occurrence Handle1:CAS:528:DyaK28XlsFOi
F Banuett (1998) ArticleTitleSignaling in the yeasts: an informational cascade with links to the filamentous fungi Microbial Mol Biol Rev 62 249–274 Occurrence Handle1:CAS:528:DyaK1cXkt1OitLo%3D
JA Barnett RW Payne W Yarrow (2000) NoChapterTitle BibInstitutionalEditorNameCambridge University Press (Eds) Yeast: Characteristics and Identification EditionNumber3 University Press Cambridge 1–1138
F Cervone G Lorenzo ParticleDe B Aracri D Bellincampi C Caprari AJ Clark A Desiderio A Devoto F Leckie B Mattei L Nuss G Salvi (1996) The role of polygalacturonase, PGIP and pectin oligomers in fungal infection J Visser AGL Voragen (Eds) Progress in Biotechnology: Pectins and Pectinases Elsevier Amsterdam 191–205
PJ Cullen GF Sprague SuffixJr (2000) ArticleTitleGlucose depletion causes haploid invasive: growth in yeast Proc Natl Acad Sci 97 13619–13624 Occurrence Handle1:CAS:528:DC%2BD3cXoslygurk%3D Occurrence Handle11095711
A DeBary (1886) ArticleTitleVeber Einige Sclerotinien und Sclerotien-Krankheiten Bot Ztg 44 376–488
JR Dickinson (1996) ArticleTitle‘Fuel’ alcohols induce hyphal-like extensions and pseudohyphal formation in yeasts Microbiology 142 1391–1407 Occurrence Handle1:CAS:528:DyaK28XjvFGrur0%3D Occurrence Handle8704979 Occurrence Handle10.1099/13500872-142-6-1391
CA D'Souza J Heitman (2001) ArticleTitleConserved cAMP signaling cascades regulate fungal development and virulence FEMS Microbial Rev 25 349–364
GH Fleet (2002) The yeast ecology of wine grapes M Ciani (Eds) Biodiversity and Biotechnology of Wine Yeasts Research Signpost Trivandrum, India 1–19
V Frézier D Dubourdieu (1992) ArticleTitleEcology of yeast strains Saccharomyces cerevisiae during spontaneous fermentation in a Bordeaux winery Am J Enol Vitic 43 375–380
A Gainvors V Frézier H Lemaresquier C Lequart M Aigle A Belarbi (1994) ArticleTitleDetection of polygalacturonase, pectin-lyase and pectin-esterase activities in a Saccharomyces cerevisiae strain Yeast 10 1311–1319 Occurrence Handle10.1002/yea.320101008 Occurrence Handle1:CAS:528:DyaK2MXit1Cqtrg%3D Occurrence Handle7900420
JM Gancedo (2001) ArticleTitleControl of pseudohyphae formation in Saccharomyces cerevisiae FEMS Microbial Rev 25 107–123 Occurrence Handle1:CAS:528:DC%2BD3MXitl2lsw%3D%3D Occurrence Handle10.1111/j.1574-6976.2001.tb00573.x
CJ Gimeno PO Ljungdahi CA Styles GR Fink (1992) ArticleTitleUnipolar cell division in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS Cell 68 1077–1099 Occurrence Handle10.1016/0092-8674(92)90079-R Occurrence Handle1:CAS:528:DyaK38XhvFSrt7g%3D Occurrence Handle1547504
S Gognies A Belarbi (2002) ArticleTitleEndopolygalacturonase of Saccharomyces cerevisiae: involvement in pseudohyphae development of haploids and in pathogenicity on Vitis vinifera Plant Sci 163 759–769 Occurrence Handle10.1016/S0168-9452(02)00211-X Occurrence Handle1:CAS:528:DC%2BD38XnsVSgs7Y%3D
S Gognies A Belarbi E Ait Barka (2002) ArticleTitle Saccharomyces cerevisiae, a potential pathogen towards grapevine, Vitis vinifera FEMS Microbiol Ecol 37 143–150
Hartmann, C, Joseph, C, Millet, B (1998) In: Nathan (Ed.) Biologie et Physiologie de la plante.
Z Kang H Buchenauer (2002) ArticleTitleStudies on the infection process of Fusarium culmorum in wheat spikes. Degradation of host cell wall components and localization of trichothecene toxins in infected tissues Eur J Plant Phyto 108 653–660 Occurrence Handle1:CAS:528:DC%2BD38XnvVyis7c%3D
Kurtzman, CP, Fell, JW (1998) In: Elsevier (Ed.) The Yeasts, a Taxonomic Study, 4th ed. Amsterdam
MG Lambrechts FF Bauer J Marmur IS Pretorius (1996) ArticleTitleMuc1, a mucin-like protein which is regulated by Mss10, is critical for pseudohyphal differentiation in yeast Proc Natl Acad Sci U S A 93 8419–8424 Occurrence Handle10.1073/pnas.93.16.8419 Occurrence Handle1:CAS:528:DyaK28XkvFyks7k%3D Occurrence Handle8710886
WS Lo AM Dranginis (1998) ArticleTitleThe cell surface flocculin FLO11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae Mol Biol Cell 9 161–171 Occurrence Handle1:CAS:528:DyaK1cXnslCiug%3D%3D Occurrence Handle9436998
MC Lorenz NS Cutler J Heitman (2000) ArticleTitleCharacterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae Mol Biol Cell 11 183–199 Occurrence Handle1:CAS:528:DC%2BD3cXosFyjtA%3D%3D Occurrence Handle10637301
HD Madhani GR Fink (1997) ArticleTitleCombinatorial control required for the specificity of yeast MAPK signalling Science 275 1314–1317 Occurrence Handle10.1126/science.275.5304.1314 Occurrence Handle1:CAS:528:DyaK2sXhs1GrtLc%3D Occurrence Handle9036858
HD Madhani GR Fink (1998) ArticleTitleThe control of filamentous differentiation and virulence in fungi Trends Cell Biol 8 348–353 Occurrence Handle10.1016/S0962-8924(98)01298-7 Occurrence Handle1:CAS:528:DyaK1cXlvVCjs70%3D Occurrence Handle9728395
HD Madhani T Galitski ES Lander GR Fink (1999) ArticleTitleEffectors of a developmental mitogen-activated protein kinase cascade revealed by expression signatures of signaling mutants Proc Natl Acad Sci 96 12530–12535 Occurrence Handle10.1073/pnas.96.22.12530 Occurrence Handle1:CAS:528:DyaK1MXnt1yru7k%3D Occurrence Handle10535956
A Martini (1993) ArticleTitleOrigin and domestication of the wine yeast Saccharomyces cerevisiae J Wine Res 4 165–176
AM McKay (1988) ArticleTitleA plate assay method for the detection of fungal polygalacturonase secretion FEMS Microbiol Lett 56 355–358 Occurrence Handle10.1016/0378-1097(88)90088-2 Occurrence Handle1:CAS:528:DyaL1MXhtlSqsbw%3D
R Mortimer M Polsinelli (1999) ArticleTitleOn the origins of wine yeast Res Microbiol 150 IssueID3 199–204 Occurrence Handle10.1016/S0923-2508(99)80036-9 Occurrence Handle1:STN:280:DyaK1M3ks1Gltg%3D%3D Occurrence Handle10229949
HU Mosch GR Fink (1997) ArticleTitleDissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae Genetics 145 IssueID3 671–684 Occurrence Handle1:CAS:528:DyaK2sXmsVakt7g%3D Occurrence Handle9055077
T Murashige F Skoog (1962) ArticleTitleA revised medium for rapid growth and biomass assays with tobacco tissue cultures Physiol Plant 15 473–497 Occurrence Handle1:CAS:528:DyaF3sXksFKm
RA Prade D Zhan P Ayoudi AJ Mort (1999) ArticleTitlePectins, pectinases and plant–microbe interactions Biotechnol Genet Eng Rev 16 361–391 Occurrence Handle1:CAS:528:DyaK1MXkvVyjsro%3D Occurrence Handle10819085
IS Pretorius (2000) ArticleTitleTailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking Yeast 16 675–729 Occurrence Handle10.1002/1097-0061(20000615)16:8<675::AID-YEA585>3.0.CO;2-B Occurrence Handle1:CAS:528:DC%2BD3cXktl2it78%3D Occurrence Handle10861899
S Rainieri C Zambonelli Y Kaneko (2003) ArticleTitle Saccharomyces sensu stricto: systematics, genetic diversity and evolution J Biosci Bioeng 96 IssueID1 1–9 Occurrence Handle1:CAS:528:DC%2BD3sXnsFyksbg%3D Occurrence Handle16233475
A Rementeria JA Rodriguez A Cadaval R Amenabar JR Muguruza FL Hernando MJ Sevilla (2003) ArticleTitleYeast associated with spontaneous fermentations of white wines from the “Txakoli de Bizkaia” region (Basque Country, North Spain) Int J Food Microbiol 1 IssueID86(1–2) 201–207
RL Roberts GR Fink (1994) ArticleTitleElements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth Genes Dev 8 2974–2985 Occurrence Handle1:CAS:528:DyaK2MXivVWrt7o%3D Occurrence Handle8001818
S Scherer PT Magee (1990) ArticleTitleGenetics of Candida albicans Microbiol Rev 54 226–241 Occurrence Handle1:CAS:528:DyaK3cXmtVGmtrY%3D Occurrence Handle2215421
D Schuller H Alves S Dequin M Casal (2005) ArticleTitleEcological survey of Saccharomyces cerevisiae strains from vineyards in the Vinho Verde Region of Portugal FEMS Microbiol Ecol 51 167–177 Occurrence Handle1:CAS:528:DC%2BD2cXhtFGhtr3J Occurrence Handle16329865
D Dyk ParticleVan IS Pretorius FF Bauer (2005) ArticleTitleMss11p is a central element of the regulatory network that controls FLO11 expression and invasive growth in Saccharomyces cerevisiae Genetics 169 IssueID1 91–106 Occurrence Handle15466424
Acknowledgments
The authors would like to thank Mrs Jessica Blanc for her careful reading of the manuscript. This research was supported by a grant from Europol'agro.
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Gognies, S., Barka, E.A., Gainvors-Claisse, A. et al. Interactions Between Yeasts and Grapevines: Filamentous Growth, Endopolygalacturonase and Phytopathogenicity of Colonizing Yeasts. Microb Ecol 51, 109–116 (2006). https://doi.org/10.1007/s00248-005-0098-y
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DOI: https://doi.org/10.1007/s00248-005-0098-y