Skip to main content
  • Original Article
  • Published:

Phenotypic variation in the phenology of ascospore production between European populations of oak powdery mildew

Variabilité phénotypique dans la phénologie de la production d’ascospores entre populations européennes d’oïdium du chêne

Abstract

  • • Oak powdery mildew severity (Erysiphe alphitoides) is usually mild in Europe because epidemics start late in spring, at the end of the first oak growth unit maturation. However, the disease can occasionally be very severe when strong infection occurs early during the development of the first growth unit, suggesting that host-pathogen synchrony in spring could be a critical factor in disease severity.

  • • We studied the timing of ascospore production in a given environment for four E. alphitoides populations sampled from SW France to the Czech Republic to determine whether this trait shows variation within Europe.

  • • Timing of ascospore production was clearly influenced by environmental factors as chasmothecia from a single origin showed very different dates of optimal ascospore production when transferred for overwintering in locations with different climate. In common garden experiments, no differences were observed between populations for the date of optimal ascospore production.

  • • Results suggest little genetic differentiation for timing of ascospore production for E. alphitoides populations across Europe and therefore a lack of local adaptation to their host phenology. Availability in ascospore inoculum is limited during host budburst, explaining the low infection usually observed on the first oak growth unit.

Résumé

  • • L’oïdium du chêne (Erysiphe alphitoides) est généralement peu sévère en Europe, la maladie se développant tard au printemps, après le débourrement des chênes. E. alphitoides peut toutefois être sévère quand de fortes infections se produisent tôt durant le débourrement, suggérant que la synchronisation entre hôte et pathogène pourrait être un facteur déterminant la sévérité des épidémies.

  • • Nous avons caractérisé la dynamique de production d’ascospores dans un environnement donné pour quatre populations d’E. alphitoides échantillonnées du sud-ouest de la France à la République Tchèque pour tester si ce trait est variable en Europe.

  • • Des chasmothèces d’une même origine présentent des dates d’optima de production d’ascospores très différentes quand elles sont transférées durant l’hiver dans des zones à climats différents montrant que ce trait est sous dépendance de l’environnement. Par contre, les quatre populations ont la même date d’optimum de production d’ascospores quand elles sont placées dans un même environnement.

  • • Les résultats suggèrent que les populations d’E. alphitoides européennes ne sont pas différentiées génétiquement pour le timing de production d’ascospores et donc qu’elles ne sont pas localement adaptées à la phénologie de leur hôte. L’inoculum ascospores est très peu présent durant le débourrement, expliquant en partie l’absence d’infection sur la première unité de croissance des chênes.

References

  • Baker R.H.A., Sansford C.E., Gioli B., Miglietta F., Porter J.R., and Ewert F., 2005. Combining a disease model with a crop phenology model to assess and map pest risk: Karnal bunt disease (Tilletia indica) of wheat in Europe. In: Alford D.V. and Backhaus G.F. (Eds.), Plant protection and plant health in Europe: introduction and spread of invasive species, Humboldt University, Berlin, Germany, pp. 89–94.

    Google Scholar 

  • Biere A. and Honders S.J., 1996. Impact of flowering phenology of Silene alba and S. dioica on susceptibility to fungal infection and seed predation. Oikos 77: 467–480.

    Article  Google Scholar 

  • Braun U., 1995. The powdery mildews (Erysiphales) of Europe, Gustav Fischer Verlag, Jena, Germany.

    Google Scholar 

  • Bréda N., Granier A., and Aussenac G., 1995. Effects of thinning on soil water balance and trees water relations, transpiration and growth in an oak forest (Quercus petraea). Tree Physiol. 15: 295–306.

    PubMed  Google Scholar 

  • Cipollini D., 2002. Variation in the expression of chemical defenses in Alliaria petiolata (Brassicaceae) in the field and common garden. Am. J. Bot. 89: 1422–1430.

    Article  PubMed  CAS  Google Scholar 

  • Cleland C.C., Chuine I., Menzel A., Mooney H.A., and Schwartz M.D., 2007. Shifting plant phenology in response to global change. Trends Ecol. Evol. 22: 357–365.

    Article  Google Scholar 

  • Desprez-Loustau M.L. and Dupuis F., 1994. Variation in the phenology of shoot elongation between geographic provenances of maritime pine (Pinus pinaster) implications for the synchrony with the phenology of the twisting rust fungus, Melampsora pinitorqua. Ann. Sci. For. 51: 553–568.

    Article  Google Scholar 

  • Desprez-Loustau M.L., Belrose V., Bergot M., Capron G., Cloppet E., Husson C., Piou D., Reynaud G., Robin C., and Marçais B., 2008. Simulating effects of climate change on geographical range and impact of forest pathogenic fungi. In Desprez-Loustau (Coord.), Forests, carbon cycle and climate change, Editions Quae, coll. Science Update, pp. 258–288 (in press).

  • Ducousso A., Guyon J.P., and Krémer A., 1996. Latitudinal and altitudinal variation of bud burst in western populations of sessil oak (Quercus petraea (Matt) Liebl). Ann. Sci. For. 53: 775–782.

    Article  Google Scholar 

  • Edwards M.C. and Ayres P.G., 1982. Seasonal changes in resistance of Quercus petraea (sessile oak) leaves to Microsphaera alphitoides. Transactions of the British Mycological Society 78: 569–571.

    Article  Google Scholar 

  • Foex M.E., 1941. L’invasion des chênes d’Europe par le blanc ou oidium. Rev. Eaux For. 79: 338–349.

    Google Scholar 

  • Kerling L.C.P., 1966. The hibernation of the oak mildew. Acta Botanica Neerlandica 15: 76–83.

    Google Scholar 

  • Lebourgeois F., 2007. The sensitivity of forest ecosystems to climate: what Renecofor has taught us. Rendez-Vous Techniques, 15: 64–68.

    Google Scholar 

  • Jailloux F., Thind T., and Clerjeau M., 1998. Release, germination and pathogenicity of ascospores of Uncinula necator under controlled conditions. Can. J. Bot. 76: 777–781.

    Google Scholar 

  • Jensen J.S. and Hansen J.K., 2008. Geographical variation in phenology of Quercus petraea (Matt.) Liebl and Quercus robur L. oak grown in a greenhouse. Scand. J. For. Res. 23: 179–188.

    Article  Google Scholar 

  • Mc Donald B.A. and Linde C., 2002 Pathogen population genetics, evolutionary potential, and durable resistance. Ann. Rev. Phytopathol. 40: 349–379.

    Article  CAS  Google Scholar 

  • Marçais B. and Bréda N., 2006. Role of an opportunistic pathogen in the decline of stressed oak trees. J. Ecol. 94: 1214–1223.

    Article  Google Scholar 

  • Mmaga M.T., 2000. Winter survival and source of primary inoculum of powdery mildew of dogwood in Tenessee. Plant Dis. 84: 574–579.

    Article  Google Scholar 

  • Mougou A., Dutech C., and Desprez-Loustau M.L., 2008. New insights into the identity and origin of the causal agent of oak powdery mildew in Europe. For. Pathol. 38: 275–287.

    Google Scholar 

  • Oleksyn J., Modrzynski J., Tjoelker M.G., Zytkowiak R., Reich P.B., and Karolewski P., 1998. Growth and physiology of Picea abies populations from elevational transects: common garden evidence for altitudinal ecotypes and cold adaptation. Funct. Ecol. 12: 573–590.

    Article  Google Scholar 

  • Pearson R.C. and Gadoury D.M., 1987. Cleistothecia, the source of primary inoculum for grape powdery mildew in New York. Phytopathology 77: 1509–1514

    Article  Google Scholar 

  • Penman L.N. and Annis S.L., 2005. Leaf and flower blight caused by Monilinia vaccinii-corymbosi on lowbush blueberry: effects on yield and relationship to bud phenology. Phytopathology 95: 1174–1182.

    Article  PubMed  CAS  Google Scholar 

  • Raymond J., 1927. Le “blanc” du chêne. Annale des Epiphyties 13: 94–129.

    Google Scholar 

  • Roslin T., Laine A.L., and Gripenberg S., 2007. Spatial population structure in an obligate plant pathogen colonizing oak Quercus robur. Funct. Ecol. 21: 1168–1177.

    Article  Google Scholar 

  • Scotti-Saintagne C., Bodénès C., Barreneche T., Bertocchi E., Plomion C., and Kremer A., 2004. Detection of quantitative trait loci controlling bud burst and height growth in Quercus robur L. Theor. Appl. Genet. 109: 1648–1659.

    Article  CAS  Google Scholar 

  • Soutrenon A., 1998. Une experimentation pluri-annuelle confirme l’impact de l’oïdium sur de jeunes sujets. Les cahiers du DSF, 1–2000 (la santé des forets [France] en 1997), Min. Agri. Pêche (DERF), Paris, 93–94.

    Google Scholar 

  • Spark T.H. and Carey P.D., 1995. The response of species to climate over two centuries: an analysis of the Marsham phenological record, 1736–1947. J. Ecol. 83: 321–329.

    Article  Google Scholar 

  • Thomas F.M., Blank R., and Hartmann G., 2002. Abiotic and biotic factors and their interactions as causes of oak decline in central Europe. For. Pathol. 32: 277–307.

    Google Scholar 

  • Van Ash M. and Visser M.E., 2007. Phenology of forest caterpillars and their host trees: the importance of synchrony. Ann. Rev. Entomol. 52: 37–55.

    Article  Google Scholar 

  • Visser M.E. and Holleman L.J.M., 2001. Warmer springs disrupt the synchrony of oak and winter moth phenology. Proceedings of the Royal Society London Series B 268: 89–94.

    Google Scholar 

  • Woodward R.C., Waldie J.S.L., and Steven H.M., 1929. Oak mildew and its control in forest nurseries. Forestry 3: 38–56.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Benoit Marçais.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marçais, B., Kavkova, M. & Desprez-Loustau, ML. Phenotypic variation in the phenology of ascospore production between European populations of oak powdery mildew. Ann. For. Sci. 66, 814 (2009). https://doi.org/10.1051/forest/2009077

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1051/forest/2009077

Keywords

Mots-clés