{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T21:01:25Z","timestamp":1792011685286,"version":"4.4.0"},"reference-count":63,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,7,8]],"date-time":"2021-07-08T00:00:00Z","timestamp":1625702400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>The plant disease onset is a complex event that occurs when the pathogen and the host encounter in a favorable environment. While the plant\u2013pathogen interaction has been much investigated, little attention has been given to the phenological synchrony of the event, especially when both plant and pathogen overwinter, as in the case of grapevines and the downy mildew agent, the oomycete <jats:italic>Plasmopara viticola<\/jats:italic>. Oospores allow this obligate parasite to survive grapevine dormancy and, germinating, produce inoculum for primary infections. During overwintering, environmental factors influence the potential oospore germination. This study aimed at investigating the existence of synchrony between the pathogen and the host by identifying and quantifying the most important factors determining oospore maturation and germination and the relationship existing with grapevine phenology. Generalized linear models (GLM and GLMM) were used to analyze the germination dynamics of the oospores overwintered in controlled and field conditions and incubated in isothermal conditions, and oospore viability tests were carried out at different time points. Results showed that the most indicative parameter to describe the germination dynamics is the time spent by the oospores from the start of overwintering. The oospores overwintered in field showed phenological traits related to grapevine phenology not observed in controlled conditions. In particular, they completed the maturation period by the end of grapevine dormancy and germinated more rapidly at plant sprouting, when grapevine reaches susceptibility. Overall, the oospores proved to be able to modulate their behavior in close relationship with grapevine, showing a great adaptation to the host\u2019s phenology.<\/jats:p>","DOI":"10.3389\/fmicb.2021.698586","type":"journal-article","created":{"date-parts":[[2021,7,8]],"date-time":"2021-07-08T09:13:40Z","timestamp":1625735620000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":20,"title":["The Study of the Germination Dynamics of Plasmopara viticola Oospores Highlights the Presence of Phenotypic Synchrony With the Host"],"prefix":"10.3389","volume":"12","author":[{"given":"Giuliana","family":"Maddalena","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppe","family":"Russo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvia L.","family":"Toffolatti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,7,8]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1201\/9781420066296.ch33","article-title":"Half-life theory of learning curves.","volume":"3","author":"Badiru","year":"2009","journal-title":"IEEE Syst. J."},{"key":"B2","doi-asserted-by":"publisher","first-page":"133","DOI":"10.20870\/oeno-one.2016.0.0.1780","article-title":"Climate vs grapevine pests and diseases worldwide: the first results of a global survey.","volume":"51","author":"Bois","year":"2017","journal-title":"OENO One"},{"key":"B3","doi-asserted-by":"publisher","first-page":"125","DOI":"10.5423\/PPJ.OA.09.2018.0194","article-title":"Factors affecting the vineyard populational diversity of Plasmopara viticola.","volume":"35","author":"Boso","year":"2019","journal-title":"Plant Pathol. J."},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1007\/s10681-017-1882-8","article-title":"Breeding for grapevine downy mildew resistance: a review of \u201comics\u201d approaches.","volume":"213","author":"Buonassisi","year":"2017","journal-title":"Euphytica"},{"key":"B5","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1016\/S0269-915X(00)80040-3","article-title":"The life-cycle of Plasmopara viticola, cause of downy mildew of vine.","volume":"14","author":"Burruano","year":"2000","journal-title":"Mycologist"},{"key":"B6","first-page":"1","article-title":"Preliminary investigation on the effect of soil moisture on oospore maturation in Plasmopara viticola.","volume":"31","author":"Burruano","year":"1992","journal-title":"Phytopathol. Mediterr."},{"key":"B7","first-page":"73","article-title":"Preliminary information on the effect of low temperatures on oospore germination in Plasmopara viticola.","volume":"29","author":"Burruano","year":"1990","journal-title":"Phytopathol. Mediterr."},{"key":"B8","first-page":"58","article-title":"Plasmopara viticola: three decades of observation in Sicily","author":"Burruano","year":"2006","journal-title":"Proceedings of the 5th International Workshop on Grapevine Downy nd Powdery Mildew"},{"key":"B9","first-page":"85","article-title":"Investigation on the germination of oospores of Plasmopara viticola differentiated in different localities.","volume":"28","author":"Burruano","year":"1989","journal-title":"Phytopathol. Mediterr."},{"key":"B10","first-page":"19","article-title":"Effect of water on oospore germination in Plasmopara viticola.","volume":"26","author":"Burruano","year":"1987","journal-title":"Phytopathol. Mediterr."},{"key":"B11","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1007\/s10658-015-0748-y","article-title":"Development of grape downy mildew (Plasmopara viticola) under northern viticulture conditions: influence of fall disease incidence.","volume":"144","author":"Carisse","year":"2016","journal-title":"Eur. J. Plant Pathol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1111\/j.1744-7348.1960.tb03498.x","article-title":"Studies of the biology of Sclerotium cepivorum Berk.","volume":"48","author":"Coley-Smith","year":"1960","journal-title":"Ann. Appl. Biol."},{"key":"B13","author":"Cox","year":"1989","journal-title":"Analysis of Binary Data"},{"key":"B14","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/j.ijfoodmicro.2009.02.005","article-title":"Significance of the physiological state of fungal spores.","volume":"134","author":"Dantigny","year":"2009","journal-title":"Int. J. Food Microbiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1111\/j.1420-9101.2009.01881.x","article-title":"Are plant pathogen populations adapted for encounter with their host? A case study of phenological synchrony between oak and an obligate fungal parasite along an altitudinal gradient.","volume":"23","author":"Desprez-Loustau","year":"2010","journal-title":"J. Evol. Biol."},{"key":"B16","first-page":"355","article-title":"Patterns of phenology in populations of zoosporic fungi","author":"Dick","year":"1992","journal-title":"The Fungal Community"},{"key":"B17","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1046\/j.1365-2672.2003.02133.x","article-title":"Dormant ascospores of Talaromyces macrosporus are activated to germinate after treatment with ultra high pressure.","volume":"96","author":"Dijksterhuis","year":"2003","journal-title":"J. Appl. Microbiol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"3897","DOI":"10.1016\/j.cub.2020.07.057","article-title":"Identification of the first oomycete mating-type locus sequence in the grapevine downy mildew pathogen, Plasmopara viticola.","volume":"30","author":"Dussert","year":"2020","journal-title":"Curr. Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"8923","DOI":"10.1007\/s00253-016-7787-y","article-title":"At-line determining spore germination of Penicillium chrysogenum bioprocesses in complex media.","volume":"100","author":"Ehgartner","year":"2016","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1007\/BF01976387","article-title":"Development of a stochastic spore germination model.","volume":"91","author":"Eisensmith","year":"1985","journal-title":"Netherlands J. Plant Pathol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1111\/j.1744-7909.2005.00031.x","article-title":"Thermal hardening: a new seed vigor enhancement tool in rice.","volume":"47","author":"Farooq","year":"2005","journal-title":"J. Integr. Plant Biol."},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2019.00951","article-title":"Colonization of different grapevine tissues by Plasmopara viticola\u2014a histological study.","volume":"10","author":"Fr\u00f6bel","year":"2019","journal-title":"Front. Plant Sci."},{"key":"B23","first-page":"66","article-title":"Indagini sulla formazione e sulla germinazione delle oospore di Plasmopara viticola.","volume":"20","author":"Galbiati","year":"1984","journal-title":"Riv. di Patol. Veg."},{"key":"B24","doi-asserted-by":"publisher","first-page":"3","DOI":"10.14601\/Phytopathol_Mediterr-9360","article-title":"Plasmopara viticola: a review of knowledge on downy mildew of grapevine and effective disease management.","volume":"50","author":"Gessler","year":"2011","journal-title":"Phytopathol. Mediterr."},{"key":"B25","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1111\/j.1365-3059.2005.01208.x","article-title":"Importance of secondary inoculum of Plasmopara viticola to epidemics of grapevine downy mildew.","volume":"54","author":"Gobbin","year":"2005","journal-title":"Plant Pathol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1007\/bf02873609","article-title":"The physiology of spore germination in fungi.","volume":"16","author":"Gottlieb","year":"1950","journal-title":"Bot. Rev."},{"key":"B27","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.ijfoodmicro.2011.07.030","article-title":"Modeling germination of fungal spores at constant and fluctuating temperature conditions.","volume":"152","author":"Gougouli","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"B28","author":"Griffin","year":"1994","journal-title":"Fungal Physiology"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.3390\/insects9030102","article-title":"Sleeping beauties: horizontal transmission via resting spores of species in the entomophthoromycotina.","volume":"9","author":"Hajek","year":"2018","journal-title":"Insects"},{"key":"B30","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1111\/j.1365-313X.2009.04116.x","article-title":"Germinator: a software package for high-throughput scoring and curve fitting of Arabidopsis seed germination.","volume":"62","author":"Joosen","year":"2010","journal-title":"Plant J."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1445","DOI":"10.1094\/PHYTO-95-1445","article-title":"Seasonal development of ontogenic resistance to downy mildew in grape berries and rachises.","volume":"95","author":"Kennelly","year":"2005","journal-title":"Phytopathology"},{"key":"B32","doi-asserted-by":"publisher","first-page":"512","DOI":"10.1094\/PHYTO-97-4-0512","article-title":"Primary infection, lesion productivity, and survival of sporangia in the grapevine downy mildew pathogen Plasmopara viticola.","volume":"97","author":"Kennelly","year":"2007","journal-title":"Phytopathology"},{"key":"B33","doi-asserted-by":"publisher","first-page":"1068","DOI":"10.1111\/1567-1364.12202","article-title":"Comparison of methods used for assessing the viability and vitality of yeast cells.","volume":"14","author":"Kwolek-Mirek","year":"2014","journal-title":"FEMS Yeast Res."},{"key":"B34","first-page":"80","article-title":"Effect of temperature on oospore germination in Plasmopara viticola (Berk et Curt.) Berl. et De Toni.","volume":"25","author":"Laviola","year":"1986","journal-title":"Phytopathol. Mediterr."},{"key":"B35","doi-asserted-by":"publisher","first-page":"390","DOI":"10.1094\/PHYTO.2000.90.4.390","article-title":"Variation and heritability of phenology in the fungus Monilinia vaccinii-corymbosi on blueberry.","volume":"90","author":"Lehman","year":"2000","journal-title":"Phytopathology"},{"key":"B36","first-page":"17","article-title":"Observations on oospore production by Plasmopara viticola in floating leaf discs in artificial culture.","volume":"5","author":"Lehoczky","year":"1956","journal-title":"Vitis"},{"key":"B37","first-page":"66","article-title":"Ph\u00e4nologische entwicklungsstadien der weinrebe (Vitis vinifera L. ssp. vinifera).","volume":"49","author":"Lorenz","year":"1994","journal-title":"Vitic. Enol. Sci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1038\/s41564-021-00888-x","article-title":"Fungal taxonomy and sequence-based nomenclature.","volume":"6","author":"L\u00fccking","year":"2021","journal-title":"Nat. Microbiol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"13434","DOI":"10.1073\/pnas.1305533110","article-title":"Community-level phenological response to climate change.","volume":"110","author":"Ovaskainen","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B40","doi-asserted-by":"publisher","first-page":"6764","DOI":"10.1128\/AEM.02521-13","article-title":"Modeling of fungal and bacterial spore germination under static and dynamic conditions.","volume":"79","author":"Peleg","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"B41","first-page":"43","article-title":"Studies on Plasmopara viticola oospore germination in Trentino, Italy.","volume":"26","author":"Pertot","year":"2003","journal-title":"IOBC WPRS Bull."},{"key":"B42","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1016\/j.ecolmodel.2008.05.006","article-title":"How to evaluate models: observed vs. predicted or predicted vs. observed?","volume":"216","author":"Pi\u00f1eiro","year":"2008","journal-title":"Ecol. Modell."},{"key":"B43","first-page":"237","article-title":"Influence des conditions climatiques en automne sur la maturation des oospores de Plasmopara viticola et sur la gravit\u00e9 des attaques de Mildiou au printemps: Mod\u00e9lisation du phenomene","author":"Ronzon Tran Manh Sung","year":"1989","journal-title":"Proceedings of a meeting of the EC Experts\u2019 Group, Thessaloniki 6-8 October 1987"},{"key":"B44","doi-asserted-by":"publisher","first-page":"938","DOI":"10.1094\/pd-72-0938","article-title":"Techniques for formation, maturation, and germination of Plasmopara viticola oospores under controlled conditions.","volume":"72","author":"Ronzon-Tran Manh Sung","year":"1988","journal-title":"Plant Dis."},{"key":"B45","doi-asserted-by":"publisher","first-page":"957","DOI":"10.1111\/j.1365-3059.2007.01685.x","article-title":"Effect of water on germination of Plasmopara viticola oospores.","volume":"56","author":"Rossi","year":"2007","journal-title":"Plant Pathol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1111\/j.1365-3059.2007.01738.x","article-title":"Estimating the germination dynamics of Plasmopara viticola oospores using hydro-thermal time.","volume":"57","author":"Rossi","year":"2008","journal-title":"Plant Pathol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1111\/j.1365-2338.2003.00670.x","article-title":"Development of overwintering oospores of Plasmopara viticola and severity of primary foci in relation to climate.","volume":"33","author":"Rouzet","year":"2003","journal-title":"EPPO Bull."},{"key":"B48","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1007\/s00122-018-3203-6","article-title":"Construction of a high-density linkage map and QTL detection of downy mildew resistance in Vitis aestivalis-derived \u2018Norton.\u2019.","volume":"132","author":"Sapkota","year":"2019","journal-title":"Theor. Appl. Genet."},{"key":"B49","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2020.562432","article-title":"Rpv29, Rpv30 and Rpv31: three novel genomic loci associated with resistance to Plasmopara viticola in Vitis vinifera.","volume":"11","author":"Sargolzaei","year":"2020","journal-title":"Front. Plant Sci."},{"key":"B50","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1111\/j.1439-0434.2006.01136.x","article-title":"Characterization of genotype and mating type in European isolates of Plasmopara viticola.","volume":"154","author":"Scherer","year":"2006","journal-title":"J. Phytopathol."},{"key":"B51","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2020.01202","article-title":"A real-time PCR assay for the quantification of Plasmopara viticola oospores in grapevine leaves.","volume":"11","author":"Si Ammour","year":"2020","journal-title":"Front. Plant Sci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"A3.B.1","DOI":"10.1002\/0471142735.ima03bs21","article-title":"Trypan blue exclusion test of cell viability.","volume":"21","author":"Strober","year":"1997","journal-title":"Curr. Protoc. Immunol"},{"key":"B53","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1111\/nph.12646","article-title":"Ecological and evolutionary implications of spatial heterogeneity during the off-season for a wild plant pathogen.","volume":"202","author":"Tack","year":"2014","journal-title":"New Phytol."},{"key":"B54","first-page":"47","article-title":"Germination dynamics and viability of Plasmopara viticola oospores in advances in downy mildew research,","author":"Toffolatti","year":"2007","journal-title":"Proceedings of the 2nd International Downy Mildews Symposium"},{"key":"B55","doi-asserted-by":"publisher","first-page":"2822","DOI":"10.1002\/ps.5072","article-title":"A time-course investigation of resistance to the carboxylic acid amide mandipropamid in field populations of Plasmopara viticola treated with anti-resistance strategies.","volume":"74","author":"Toffolatti","year":"2018","journal-title":"Pest Manag. Sci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1094\/pd-74-0120","article-title":"Simulation of the date of maturity of Plasmopara viticola oospores to predict the severity of primary infections in grapevine.","volume":"74","author":"Tran Manh Sung","year":"1990","journal-title":"Plant Dis."},{"key":"B57","doi-asserted-by":"publisher","first-page":"1196","DOI":"10.1111\/nph.13312","article-title":"The importance of the microbiome of the plant holobiont.","volume":"206","author":"Vandenkoornhuyse","year":"2015","journal-title":"New Phytol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1007\/BF02344698","article-title":"Estimating germinability of Plasmopara viticola oospores by means of neural networks.","volume":"38","author":"Vercesi","year":"2000","journal-title":"Med. Biol. Eng. Comput."},{"key":"B59","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1007\/s10658-010-9635-8","article-title":"A new approach to modelling the dynamics of oospore germination in Plasmopara viticola.","volume":"128","author":"Vercesi","year":"2010","journal-title":"Eur. J. Plant Pathol."},{"key":"B60","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1017\/S095375629800700X","article-title":"A cytological and ultrastructural study on the maturation and germination of oospores of Plasmopara viticola from overwintering vine leaves.","volume":"103","author":"Vercesi","year":"1999","journal-title":"Mycol. Res."},{"key":"B61","doi-asserted-by":"publisher","first-page":"661","DOI":"10.1016\/j.funbio.2010.06.001","article-title":"Phytophthora kernoviae oospore maturity, germination, and infection.","volume":"114","author":"Widmer","year":"2010","journal-title":"Fungal Biol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1046\/j.1365-3059.2001.00573.x","article-title":"Heterothallism in Plasmopara viticola.","volume":"50","author":"Wong","year":"2001","journal-title":"Plant Pathol."},{"key":"B63","author":"Zar","year":"2010","journal-title":"Biostatistical Analysis."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2021.698586\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,8]],"date-time":"2021-07-08T09:14:06Z","timestamp":1625735646000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2021.698586\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7,8]]},"references-count":63,"alternative-id":["10.3389\/fmicb.2021.698586"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2021.698586","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,8]]},"article-number":"698586"}}