Aerobiologia

, Volume 31, Issue 3, pp 367–380 | Cite as

Relationship between the genetic characteristics of Botrytis sp. airborne inoculum and meteorological parameters, seasons and the origin of air masses

  • Christel Leyronas
  • Fabien Halkett
  • Philippe C. Nicot
OriginalPaper

Abstract

Grey mould is a worldwide disease on many economically important crops. It is caused by two fungal species, Botrytis cinerea and B. pseudocinerea, which are mainly airborne dispersed. Although several studies have considered the abundance of airborne inoculum of B. cinerea in models forecasting the risk of grey mould epidemics, the genetic characteristics of this inoculum are poorly known. In the present study, airborne inoculum of B. cinerea and B. pseudocinerea was collected on 29 dates over a 2.5-year period on a site in south-eastern France. The 683 sampled isolates were genotyped with nine microsatellites markers, and 616 were identified as B. cinerea. The genetic structure of B. cinerea airborne inoculum was inferred with Bayesian assignment tests. Eight genetic clusters were identified. Cluster abundance showed temporal variation and was statistically linked to the season (P = 0.0009) and the origin of air masses (P < 0.0001). The proportion of isolates belonging to the species B. pseudocinerea was equal to 9.8 % on average, but it showed temporal variation; it tended to be higher in winter. This study is the first to provide information about the genetic characteristics of airborne inoculum of B. cinerea and B. pseudocinerea and to bring evidence of relationship with seasons, meteorological parameters and with the origin of air masses.

Keywords

Spores Grey mould Genetic clusters Diversity Botrytis 

References

  1. Adjebli, A., Leyronas, C., Aissat, K., & Nicot, P. C. (2014). Comparison of Botrytis cinerea populations collected from tomato greenhouses in Northern Algeria. Journal of Phytopathology,. doi:10.1111/jph.12289.Google Scholar
  2. Amato, P., Parazols, M., Sancelme, M., Mailhot, G., Laj, P., & Delort, A. M. (2007). An important oceanic source of micro-organisms for cloud water at the Puy de Dôme (France). Atmospheric Environment, 41, 8253–8263.CrossRefGoogle Scholar
  3. Arnaud-Haond, S., Duarte, C. M., Alberto, F., & Serrao, E. A. (2007). Standardizing methods to address clonality in population studies. Molecular Ecology, 16, 5115–5139.CrossRefGoogle Scholar
  4. Bardin, M., Decognet, V., & Nicot, P. C. (2014). Remarkable predominance of a small number of genotypes in greenhouse populations of Botrytis cinerea. Phytopathology,. doi:10.1094/PHYTO-10-13-0271-R.Google Scholar
  5. Berrie, A. M., Harris, D. C., Xu, X.-M., & Burgess, C. M. (2002). A potential system for managing Botrytis and powdery mildew in main season strawberries. ISHS Acta Horticulturae (ISHS), 567, 647–649.Google Scholar
  6. Blanco, C., de los Santos, B., & Romero, F. (2006). Relationship between concentrations of Botrytis cinerea conidia in air, environmental conditions, and the incidence of grey mould in strawberry flowers and fruits. European Journal of Plant Pathology, 114, 415–425.CrossRefGoogle Scholar
  7. Broome, J. C., English, J. T., Marois, J. J., Latorre, B. A., & Aviles, J. C. (1995). Development of an infection model for Botrytis bunch rot of grapes based on wetness duration and temperature. Phytopathology, 85, 97–102.CrossRefGoogle Scholar
  8. Celle-Jeanton, H., Travi, Y., Loÿe-Pilot, M. D., Huneau, F., & Bertrand, G. (2009). Rainwater chemistry at a Mediterranean inland station (Avignon, France): local contribution versus long-range supply. Atmospheric Research, 91, 118–126.CrossRefGoogle Scholar
  9. Decognet, V., Bardin, M., Trottin-Caudal, Y., & Nicot, P. C. (2009). Rapid change in the genetic diversity of Botrytis cinerea populations after the introduction of strains in a tomato glasshouse. Phytopathology, 99, 185–193.CrossRefGoogle Scholar
  10. Diaz, M. R., Iglesias, I., & Jato, M. V. (1997). Airborne concentrations of Botrytis, Uncinula and Plasmopara spores in a vineyard in Leiro-Ourense (N.W. Spain). Aerobiologia, 13, 31–35.CrossRefGoogle Scholar
  11. Diaz, M. R., Iglesias, I., & Jato, V. (1998). Seasonal variation of airborne fungal spore concentrations in a vineyard of North-West Spain. Aerobiologia, 14, 221–227.CrossRefGoogle Scholar
  12. Draxler, R. R. & Rolph, G. D. (2011). HYSPLIT (HYbrid Single-Particle Lagrangian Integrated Trajectory) Model access via NOAA ARL READY Website (http://ready.arl.noaa.gov/HYSPLIT.php). NOAA Air Resources Laboratory, Silver Spring, MD.
  13. Edwards, S. G., & Seddon, B. (2001). Selective media for the specific isolation and enumeration of Botrytis cinerea conidia. Letters in Applied Microbiology, 32, 63–66.CrossRefGoogle Scholar
  14. Elad, Y., Williamson, B., Tudzynski, P., & Delen, N. (2004). Botrytis spp. and diseases they cause in agricultural systems—An introduction. In Y. Elad, B. Williamson, P. Tudzynski, & N. Delen (Eds.), Botrytis: biology, pathology and control (pp. 1–6). Dordrecht: Kluwer Academic Publishers.Google Scholar
  15. Esterio, M., Muñoz, G., Ramos, C., Cofré, G., Estévez, R., Salinas, A., & Auger, J. (2011). Characterization of Botrytis cinerea isolates present in Thompson seedless table grapes in the central valley of Chile. Plant Disease, 95, 683–690.CrossRefGoogle Scholar
  16. Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.Google Scholar
  17. Fekete, É., Fekete, E., Irinyi, L., Karaffa, L., Arnyasi, M., Asadollahi, M., & Sandor, E. (2012). Genetic diversity of a Botrytis cinerea cryptic species complex in Hungary. Microbiological Research, 167, 283–291.CrossRefGoogle Scholar
  18. Fernández-González, M., Rodríguez-Rajo, F. J., Jato, V., Escuredo, O., & Aira, M. J. (2011). Estimation of yield ‘Loureira’ variety with an aerobiological and phenological model. Grana, 50, 63–72.CrossRefGoogle Scholar
  19. Fournier, E., & Giraud, T. (2008). Sympatric genetic differentiation of a generalist pathogenic fungus, Botrytis cinerea, on two different host plants, grapevine and bramble. Journal of Evolutionary Biology, 21, 122–132.Google Scholar
  20. Fournier, E., Giraud, T., Loiseau, A., Vautrin, D., Estoup, A., Solignac, M., et al. (2002). Characterization of nine polymorphic microsatellite loci in the fungus Botrytis cinerea (Ascomycota). Molecular Ecology Notes, 2, 253–255.CrossRefGoogle Scholar
  21. Goyeau, H., Halkett, F., Zapater, M. F., Carlier, J., & Lannou, C. (2007). Clonality and host selection in the wheat pathogenic fungus Puccinia triticina. Fungal Genetics and Biology, 44, 474–483.CrossRefGoogle Scholar
  22. Guillot, G. (2008). Inference of structure in subdivided populations at low levels of genetic differentiation-the correlated allele frequencies model revisited. Bioinformatics, 24, 2222–2228.CrossRefGoogle Scholar
  23. Guillot, G., Mortier, F., & Estoup, A. (2005). GENELAND: a computer package for landscape genetics. Molecular Ecology Notes, 5, 712–715.CrossRefGoogle Scholar
  24. Harrison, J. G., & Lowe, R. (1987). Wind dispersal of conidia of Botrytis spp. pathogenic to Vicia faba. Plant Pathology, 36, 5–15.CrossRefGoogle Scholar
  25. Isenegger, D. A., Macleod, W. J., Ford, R., & Taylor, P. W. J. (2008). Genotypic diversity and migration of clonal lineages of Botrytis cinerea from chickpea fields of Bangladesh inferred by microsatellite markers. Plant Pathology, 57, 967–973.CrossRefGoogle Scholar
  26. Jarvis, W. R. (1962). The dispersal of spores of Botrytis cinerea Fr. in a raspberry plantation. Transactions of the British Mycological Society, 45, 549–559.CrossRefGoogle Scholar
  27. Johnston, P. R., Hoksbergen, K., Park, D., & Beever, R. E. (2013). Genetic diversity of Botrytis in New Zealand vineyards and the significance of its seasonal and regional variation. Plant Pathology, 63, 888–898.CrossRefGoogle Scholar
  28. Karchani-Balma, S., Gautier, A., Raies, A., & Fournier, E. (2008). Geography, plants and growing systems shape the genetic structure of Tunisian Botrytis cinerea populations. Phytopathology, 98, 1271–1279.CrossRefGoogle Scholar
  29. Leroux, P., Chapeland, F., Desbrosses, D., & Gredt, M. (1999). Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Protection, 18, 687–697.CrossRefGoogle Scholar
  30. Leroux, P., Fritz, R., Debieu, D., Albertini, C., Lanen, C., Bach, J., et al. (2002). Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Management Science, 58, 876–888.CrossRefGoogle Scholar
  31. Leyronas, C., & Nicot, P. C. (2013). Monitoring viable airborne inoculum of Botrytis cinerea in the South-East of France over 3 years: Relation with climatic parameters and the origin of air masses. Aerobiologia, 29, 291–299.CrossRefGoogle Scholar
  32. Leyronas, C., Duffaud, M., & Nicot, P. C. (2012). Compared efficiency of the isolation methods for Botrytis cinerea. Mycology: An International Journal on Fungal Biology, 3, 221–225.Google Scholar
  33. Leyronas, C., Bryone, F., Duffaud, M., Troulet, C., & Nicot, P. C. (2015a). Assessing host specialization of Botrytis cinerea on lettuce and tomato by genotypic and phenotypic characterization. Plant Pathology, 64, 119–127.Google Scholar
  34. Leyronas, C., Duffaud, M., Parès, L., Jeannequin, B., & Nicot, P. C. (2015b). Flow of Botrytis cinerea inoculum between lettuce crop and soil. Plant Pathology,. doi:10.1111/ppa.12284.Google Scholar
  35. Ma, Z., & Michailides, T. J. (2005). Genetic structure of Botrytis cinerea populations from different host plants in California. Plant Disease, 89, 1083–1089.CrossRefGoogle Scholar
  36. Mirzaei, S., Goltapeh, E. M., Shams-Bakhsh, M., Safaie, N., & Chaichi, M. (2009). Genetic and phenotypic diversity among Botrytis cinerea isolates in Iran. Journal of Phytopathology, 157, 474–482.CrossRefGoogle Scholar
  37. Muñoz, G., Hinrichsen, P., Brygoo, Y., & Giraud, T. (2002). Genetic characterisation of Botrytis cinerea populations in Chile. Mycological Research, 106, 594–601.CrossRefGoogle Scholar
  38. Nicot, P. C., Mermier, M., Vaissière, B. E., & Lagier, J. (1996). Differential spore production by Botrytis cinerea on agar medium and plant tissue under near-ultraviolet light-absorbing polyethylene film. Plant Disease, 80, 555–558.CrossRefGoogle Scholar
  39. Oliveira, M., Guerner-Moreira, J., Mesquita, M. M., & Abreu, I. (2009). Important phytopathogenic airborne fungal spores in a rural area: incidence of Botrytis cinerea and Oidium spp. AAEM, 16, 197–204.Google Scholar
  40. Rajaguru, B. A. P., & Shaw, M. W. (2010). Genetic differentiation between hosts and locations in populations of latent Botrytis cinerea in southern England. Plant Pathology, 59, 1081–1090.CrossRefGoogle Scholar
  41. Rasiukevièiûtë, N., Valiuðkaitë, A., Survilienë-Radzevièë, E., & Supronienë, S. (2013). Investigation of Botrytis cinerea risk forecasting model of strawberry in Lithuania. Proceedings of the Latvian academy of sciences, 67(195), 198.Google Scholar
  42. Raymond, M., & Rousset, F. (1995). GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248–249.Google Scholar
  43. Rodríguez-Rajo, F. J., Jato, V., Fernández-González, M., & Aira, M. J. (2010). The use of aerobiological methods for forecasting Botrytis spore concentrations in a vineyard. Grana, 49, 56–65.CrossRefGoogle Scholar
  44. Rolph, G.D. (2011) Real-time Environmental Applications and Display sYstem (READY). http://ready.arl.noaa.gov. NOAA Air Resources Laboratory, Silver Spring, MD.
  45. Salameh, T., Drobinski, P., Menut, L., Bessagnet, B., Flamant, C., Hodzic, A., & Vautard, R. (2007). Aerosol distribution over the western Mediterranean basin during a Tramontane/Mistral event. Annales Geophysicae, 25, 2271–2291.CrossRefGoogle Scholar
  46. Shtienberg, D., & Elad, Y. (1997). Incorporation of weather forecasting in integrated, biological-chemical management of Botrytis cinerea. Phytopathology, 87(332), 340.Google Scholar
  47. Walker, A. S., Gautier, A., Confais, J., Martinho, D., Viaud, M., Le Pêcheur, P., et al. (2011). Botrytis pseudocinerea, a new cryptic species causing gray mold in French vineyards in sympatry with Botrytis cinerea. Phytopathology, 101, 1433–1445.CrossRefGoogle Scholar
  48. Walker, A. S., Micoud, A., Rémuson, F., Grosman, J., Gredt, M., & Leroux, P. (2013). French vineyards provide information that opens ways for effective resistance management of Botrytis cinerea (grey mould). Pest Management Science, 69, 667–678.CrossRefGoogle Scholar
  49. Walker, A. S., Gladieux, P., Decognet, V., Fermaud, M., Confais, J., Roudet, J., et al. (2014). Population structure and temporal maintenance of the multihost fungal pathogen Botrytis cinerea: causes and implications for disease management. Environmental Microbiology,. doi:10.1111/1462-2920.12563.Google Scholar
  50. Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Christel Leyronas
    • 1
  • Fabien Halkett
    • 2
    • 3
  • Philippe C. Nicot
    • 1
  1. 1.UR0407 Pathologie VégétaleINRAMontfavetFrance
  2. 2.UMR 1136 Interactions Arbres-MicroorganismesINRAChampenouxFrance
  3. 3.UMR 1136 Interactions Arbres-MicroorganismesUniversité de LorraineVandoeuvre-Lès-NancyFrance

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