Inferring the origin of primary inoculum of Zymoseptoria tritici from differential adaptation of resident and immigrant populations to wheat cultivars

European Journal of Plant Pathology

Volumn 145, Issue 2, 2016, Pages 393-404

  Morais, David ^a   Gélisse, Sandrine ^a   Laval, Valérie ^a   Sache, Ivan ^a   Suffert, Frédéric ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Aggressiveness trait; Host adaptation; Inoculum source; Mycosphaerella graminicola; Wheat

Indexed keywords

AGGRESSION; CULTIVAR; FIELD METHOD; FUNGUS; INOCULATION; LEAF; LESION; MONOCULTURE; PATHOGEN; WHEAT;

MYCOSPHAERELLA GRAMINICOLA; TRITICUM AESTIVUM;

EID: 84954327444     PISSN: 09291873     EISSN: 15738469     Source Type: Journal    
DOI: 10.1007/s10658-015-0853-y     Document Type: Article

References (53)

1. Ahmed, H. U., Mundt, C. C., & Coakley, S. M. (1995). Host-pathogen relationship of geographically diverse isolates of Septoria tritici and wheat cultivars. Plant Pathology, 44, 838–847.
2. Ahmed, H. U., Mundt, C. C., Hoffer, M. E., & Coakley, S. M. (1996). Selective influence of wheat cultivars on pathogenicity of Mycosphaerella graminicola (anamorph Septoria tritici). Phytopathology, 86, 454–458.
3. Andrivon, D., Pilet, F., Montarry, J., Hafidi, M., Corbière, R., Achbani, E. H., et al. (2007). Adaptation of Phytophthora infestans to partial resistance in potato: evidence from French and Moroccan populations. Phytopathology, 97, 338–343.
4. Anikster, Y., Buhnell, W. R., Eilam, T., Manisterski, J., & Roelfs, A. P. (1997). Puccinia recondita causing leaf rust on cultivated wheats, wild wheats, and rye. Canadian Journal of Botany, 75, 2082–2096.
5. Azzimonti, G., Lannou, C., Sache, I., & Goyeau, H. (2013). Components of quantitative resistance to leaf rust in wheat cultivars: diversity, variability and specificity. Plant Pathology, 62, 970–981.
6. Bathgate, J. A., & Loughman, R. (2001). Ascospores are a source of inoculum of phaeosphaeria nodorum, P. avenaria f. sp. avenaria and Mycosphaerella graminicola in Western Australia. Australasian Plant Pathology, 30, 317–322.
7. Berger, R. D. (1981). Comparison of the gompertz and logistic equations to describe plant disease progress. Phytopathology, 71, 716–719.
8. Burdon, J. J. (1993). The structure of pathogen populations in natural plant communities. Annual Review of Phytopathology, 31, 305–323.
9. Calderon, C., Ward, E., Freeman, J., Foster, S. J., & McCartney, H. A. (2002). Detection of airborne inoculum of Leptosphaeria maculans and Pyrenopeziza brassicae in oilseed rape crops by polymerase chain reaction (PCR) assays. Plant Pathology, 51, 303–310.
10. Carisse, O., Tremblay, D. M., Levesque, C. A., Gindro, K., Ward, P., & Houde, A. (2009). Development of a TaqMan real-time PCR assay for quantification of airborne conidia of Botrytis squamosa and management of botrytis leaf blight of onion. Phytopathology, 99, 1273–1280.
11. Clifford, B. C., & Clothier, R. B. (1974). Physiologic specialization of Puccinia hordei on barley hosts with non-hypersensitive resistance. Transactions of the British Mycological Society, 63, 421–430.
12. Combes, C. (2001). Ecology and evolution of intimate interactions. Chicago, USA: Chicago University Press.
13. Cowger, C., & Mundt, C. C. (2002). Aggressiveness of Mycosphaerella graminicola isolates from susceptible and partially resistant wheat cultivars. Phytopathology, 92, 624–630.
14. Duvivier, M., Dedeurwaerder, G., De Proft, M., Moreau, J. M., & Legrève, A. (2013). Real-time PCR quantification and spatio-temporal distribution of airborne inoculum of Mycosphaerella graminicola in Belgium. European Journal of Plant Pathology, 137, 325–341.
15. Fraaije, B. A., Cools, H. J., Fountaine, J., Lovell, D. J., Motteram, J., West, J. S., et al. (2005). Role of ascospores in further spread of QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola. Phytopathology, 95, 933–941.
16. Gandon, S., & Van Zandt, P. A. (1998). Local adaptation and host-parasite interactions. Trends in Ecology and Evolution, 13, 214–216.
17. Gautier, A., Marcel, T., Confais, J., Crane, C., Kema, G., Suffert, F., et al. (2014). Development of a rapid multiplex SSR genotyping method to study populations of the fungal plant pathogen Zymoseptoria tritici. BMC Research Notes, 7, 373.
18. Giraud, T. (2006). Selection against migrant pathogens: the immigrant inviability barrier in pathogens. Heredity, 97, 316–318.
19. Gladieux, P., Guérin, F., Giraud, T., Caffier, V., Lemaire, C., Parisi, L., et al. (2011). Emergence of novel fungal pathogens by ecological speciation: importance of the reduced viability of immigrants. Molecular Ecology, 20, 4521–4532.
20. Holmes, R. J., & Dennis, J. I. (1985). Accessory hosts of wheat stripe rust in Victoria, Australia. Transactions of the British Mycological Society, 85, 159–160.
21. Jin, Y., Szabo, L. J., & Carson, M. (2010). Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology, 100, 432–435.
22. Kaczmarek, J., Jedryczka, M., Cools, H. J., Fitt, B. D. L., Lucas, J. A., & Latunde-Dada, A. O. (2012). Quantitative PCR analysis of abundance of airborne propagules of leptosphaeria species in air samples from different regions of Poland. Aerobiologia, 28, 199–212.
23. Kaltz, O., & Shykoff, J. A. (1998). Local adaptation in host-parasite systems. Heredity, 81, 361–370.
24. Kaltz, O., Gandon, S., Michalakis, Y., & Shykoff, J. (1999). Local maladaptation in the anther-smut fungus to its host plant evidence from a cross-inoculation experiment. Evolution, 53, 395–407.
25. Karolewski, Z., Kaczmarek, J., Jedryczka, M., Cools, H. J., Fraaije, B. A., Lucas, J. A., et al. (2012). Detection and quantification of airborne inoculum of Pyrenopeziza brassicae in Polish and UK winter oilseed rape crops by real-time PCR assays. Grana, 51, 270–279.
26. Kawecki, T., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7, 1225–1241.
27. Kolmer, J. A., & Leonard, K. J. (1986). Genetic selection and adaptation of Cochliobolus heterostrophus to corn hosts with partial resistance. Phytopathology, 76, 774–777.
28. Laine, A. L. (2007). Detecting local adaptation in a natural plant-pathogen metapopulation: a laboratory vs. field transplant approach. Journal of Evolutionary Biology, 20, 1665–1673.
29. Laine, A. L. (2008). Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecological Letters, 11, 327–337.
30. Landschoot, S., Audenaert, K., Waegeman, W., Pycke, B., Bekaert, B., De Baets, B., et al. (2011). Connection between primary Fusarium inoculum on gramineous weeds, crop residues and soil samples and the final population on wheat ears in Flanders, Belgium. Crop Protection, 30, 1297–1305.
31. Lannou, C. (2012). Variation and selection of quantitative traits in plant pathogens. Annual Review of Phytopathology, 50, 319–338.
32. Linde, C. C., Zhan, J., & McDonald, B. A. (2002). Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology, 92, 946–955.
33. Montarry, J., Corbière, R., Lesueur, S., Glais, I., Andrivon, D. (2006). Does selection by resistant hosts trigger local adaptation in plant-pathogen systems? Journal of Evolution Biology, 19, 522--531.
34. Montarry, J., Glais, I., Corbière, R., & Andrivon, D. (2008). Adaptation to the most abundant host genotype in an agricultural plant-pathogen system - potato late blight. Evolutionary Biology, 21, 1397–1407.
35. Morais, D. (2015c) Components of the early stages of Septoria tritici blotch epidemics (Zymoseptoria tritici): quantity, efficiency and origin of primary inoculum. PhD Thesis, AgroParisTech, Paris, France, 206 p. [https://hal-uag.archives-ouvertes.fr/tel-01142864/document]
36. Morais, D., Sache, I., Suffert, F., & Laval, V. (2015a). Is the onset of septoria tritici blotch epidemics related to local pool of ascospores? Plant Pathology. doi:10.1111/ppa.1240 (in press).
37. Morais, D., Laval, V., Sache, I., & Suffert, F. (2015b). Comparative pathogenicity of sexual and asexual spores of Zymoseptoria tritici (septoria tritici blotch) on wheat leaves. Plant Pathology, 64, 1429–1439.
38. Pariaud, B., Ravigné, V., Halkett, F., Goyeau, H., Carlier, J., & Lannou, C. (2009a). Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathology, 58, 409–424.
39. Pariaud, B., Robert, C., Goyeau, H., & Lannou, C. (2009b). Aggressiveness components and adaptation to a host cultivar in wheat leaf rust. Phytopathology, 99, 869–878.
40. Roelfs, A. P. (1985). Wheat and rye stem rust. In A. P. Roelfs, & W. R. Bushnell (Eds.), The cereal rusts, Diseases, Distribution, Epidemiology, and Control (vol. II, pp. 3–37). Orlando, FL, USA: Academic Press.
41. Shaw, M. W., & Royle, D. J. (1989). Airborne inoculum as a major source of Septoria tritici (Mycosphaerella graminicola) infections in winter wheat crops in the UK. Plant Pathology, 38, 35–43.
42. Strange, R. (2003). Introduction to plant pathology. Chichester, UK: John Wiley & Sons.
43. Suffert, F., & Sache, I. (2011). Relative importance of different types of inoculum to the establishment of Mycosphaerella graminicola in wheat crops in north-west Europe. Plant Pathology, 60, 878–889.
44. Suffert, F., Sache, I., & Lannou, C. (2011). The early stages of septoria tritici blotch epidemics of winter wheat: build-up, overseasoning, and release of primary inoculum. Plant Pathology, 60, 166–177.
45. Suffert, F., Sache, I., & Lannou, C. (2013). Assessment of quantitative traits of aggressiveness in Mycosphaerella graminicola on adult wheat plants. Plant Pathology, 62, 1330–1341.
46. Suffert, F., Ravigné, V., & Sache, I. (2015). Can short-term selection for fitness traits in a fungal plant pathogen be driven by seasonal changes? A case study in the wheat pathogen Zymoseptoria tritici. Applied and Environmental Microbiology, 81, 6367–6379.
47. Wang, H. G., Yang, X. B., & Ma, Z. H. (2010). Long-distance spore transport of wheat stripe rust pathogen from Sichuan, Yunnan, and Guizhou in southwestern China. Plant Disease, 94, 873–880.
48. Zadoks, J. C., Chang, T. T., & Konzak, C. F. (1974). A decimal code for growth stages of cereals. Weed Research, 14, 415–421.
49. Zhan, J., & McDonald, B. A. (2004). The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola. Fungal Genetics and Biology, 41, 590–599.
50. Zhan, J., & McDonald, B. A. (2013a). Field-based experimental evolution of three cereal pathogens using a mark-release-recapture strategy. Plant Pathology, 62, 106–114.
51. Zhan, J., & McDonald, B. A. (2013b). Experimental measures of pathogen competition and relative fitness. Annual Review of Phytopathology, 51, 131–153.
52. Zhan, J., Mundt, C. C., & McDonald, B. A. (1998). Measuring immigration and sexual reproduction in field populations of Mycosphaerella graminicola. Phytopathology, 88, 1330–1337.
53. Zhan, J., Mundt, C. C., & McDonald, B. A. (2001). Using restriction fragment length polymorphisms to assess temporal variation and estimate the number of ascospores that initiate epidemics in field populations of Mycosphaerella graminicola. Phytopathology, 91, 1011–1017.