Fashionably late partners have more fruitful encounters: Impact of the timing of co-infection and pathogenicity on sexual reproduction in Zymoseptoria tritici

Fungal Genetics and Biology

Volumn 92, Issue , 2016, Pages 40-49

  Suffert, Frédéric ^a   Delestre, Ghislain ^a   Carpentier, Florence ^a   Gazeau, Gwilherm ^a   Walker, Anne Sophie ^a   Gélisse, Sandrine ^a   Duplaix, Clémentine ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Aggressiveness; Ascospore; Asexual multiplication; Fitness trait; Latent period; Mating type; Mycosphaerella graminicola; Pathogenicity; Sexual reproduction; Trade off; Transmission

Indexed keywords

ADULT PLANT; ARTICLE; ASCOSPORE; ASCOSPOROGENESIS; BIOLOGICAL TRAIT; CONTROLLED STUDY; CORRELATION ANALYSIS; CROSS BREEDING; EXPERIMENTAL STUDY; FITNESS TRAIT; FUNGAL REPRODUCTION; GENOTYPE; LATENT PERIOD; MIXED INFECTION; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; SPOROGENESIS; WHEAT; ZYMOSEPTORIA TRITICI; ASCOMYCETES; FUNGUS SPORE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PLANT DISEASE; PLANT LEAF; REPRODUCTION; REPRODUCTIVE FITNESS;

ASCOMYCOTA; GENETIC FITNESS; GENOTYPE; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANT LEAVES; REPRODUCTION; SPORES, FUNGAL; TRITICUM;

EID: 84966800426     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2016.05.004     Document Type: Article

References (44)

1. Abang M.M., Baum M., Ceccarelli S., Grando S., Linde C.C., Yahyaoui A., Zhan J., McDonald B.A. Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology 2006, 96:1214-1222.
2. van den Berg F., Bacaer N., Metz J.A.J., Lannou C., van den Bosch F. Periodic host absence can select for higher or lower parasite transmission rates. Evol. Ecol. 2011, 25:121-137.
3. Castel M., Mailleret L., Andrivon D., Ravigné V., Hamelin F.M. Allee effects and the evolution of polymorphism in cyclic parthenogens. Am. Nat. 2013, 183:75-88.
4. Clinckemaillie A., Dedeurwaerder G., Duvivier M., Moreau J.M., Legrève A. Presence of airborne inoculum of Mycosphaerella graminicola and occurrence of sexual reproduction during the growing season in Belgium. Phytopathology 2010, 100:S26.
5. Clément J.A.J., Magalon H., Glais I., Jacquot E., Andrivon D. To be or not to be solitary: Phytophthora infestans' dilemma for optimizing its reproductive fitness in multiple infections. PLoS One 2012, 7:e37838.
6. Clément J.A.J., Magalon H., Pelle R., Marquer B., Andrivon D. Alteration of pathogenicity-linked life-history traits by resistance of its host Solanum tuberosum impacts sexual reproduction of the plant pathogenic oomycete Phytophthora infestans. J. Evol. Biol. 2010, 23:2668-2676.
7. Cowger C., Mundt C.C. Aggressiveness of Mycosphaerella graminicola isolates from susceptible and partially resistant wheat cultivars. Phytopathology 2002, 92:624-630.
8. Cowger C., McDonald B.A., Mundt C.C. Frequency of sexual reproduction by Mycosphaerella graminicola on partially resistant wheat cultivars. Phytopathology 2002, 92:1175-1181.
9. Day J.P., Shattock R.C. Aggressiveness and other factors relating to displacement of populations of Phytophthora infestans in England and Wales. Eur. J. Plant Pathol. 1997, 103:379-391.
10. Duvivier M., Dedeurwaerder G., De Proft M., Moreau J.M., Legrève A. Real-time PCR quantification and spatio-temporal distribution of airborne inoculum of Mycosphaerella graminicola in Belgium. Eur. J. Plant Pathol. 2013, 137:325-341.
11. Duvivier M. Distribution of the Airborne Inoculum of Wheat Leaf Rust and Septoria tritici Blotch 2015, (PhD thesis), Université Catholique de Louvain, Belgique, 181p.
12. Eriksen L., Munk L. The occurrence of Mycosphaerella graminicola and its anamorph Septoria tritici in winter wheat during the growing season. Eur. J. Plant Pathol. 2003, 109:253-259.
13. Eyal Z. The response of field-inoculated wheat cultivars to mixtures of Septoria tritici isolates. Euphytica 1992, 61:25-35.
14. Gautier A., Marcel T., Confais J., Crane C., Kema G., Suffert F., Walker A.S. Development of a rapid multiplex SSR genotyping method to study populations of the fungal plant pathogen Zymoseptoria tritici. BMC Res. Notes 2014, 7:373.
15. Halperin T., Schuster S., Pnini-Cohen S., Zilberstein A., Eyal Z. The suppression of pycnidial production on wheat seedlings following sequential inoculation by isolates of Septoria tritici. Phytopathology 1996, 86:728-732.
16. Hildebrand P.D. Dispersal of plant pathogens. Encyclopedia of Pest Management 2002, 193-196. Marcel Dekker, New-York. D. Pimentel (Ed.).
17. Ingold C.T. Spore discharge in the ascomycetes. New Phytol. 1933, 32:175-196.
18. Kema G.H.J., Verstappen E.C.P., Todorova M., Waalwijk C. Successful crosses and molecular tetrad and progeny analyses demonstrate heterothallism in Mycosphaerella graminicola. Curr. Genet. 1996, 30:251-258.
19. Kema G.H.J., Ware S., Van Der Lee T., Wittenberg A., Diaz C., Goodwin S.B., De Waard M., M'Barek S. The dodge of blotch: saving sex in Mycosphaerella graminicola. Book of Abstracts of the 10th European Conference on Fungal Genetics, Noordwijkerhout, The Netherlands, 29 March-1 April 2010 2010, 37.
20. Laine A.L., Barrès B. Epidemiological and evolutionary consequences of life-history trade-offs in pathogens. Plant Pathol. 2013, 62:96-105.
21. Li H., Barbetti M., Sivasithamparam K.A. Concomitant inoculation of an avirulent strain of Leptosphaeria maculans prevents break-down of a single dominant gene-based resistance in Brassica napus cv. Surpass 400 by a virulent strain. Field Crops Res. 2006, 95:206-211.
22. Li H., Tapper N., Dean N., Barbetti M., Sivasithamparam K.A. Enhanced pathogenicity of Leptosphaeria maculans pycnidiospores from paired co-inoculation of Brassica napus cotyledons with ascospores. Ann. Bot. 2006, 97:1151-1156.
23. Linde C.C., Zhan J., McDonald B.A. Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 2002, 92:946-955.
24. McDonald B.A., Mundt C.C. How knowledge of pathogen population biology informs management of Septoria tritici blotch. Phytopathology 2016, (accepted for publication).
25. Metcalfe, R.J., 1998. Selection for resistance to demethylation inhibitor fungicides in Mycosphaerella graminicola on wheat. PhD Thesis, Université University of Reading, UK.
26. Morais D., Laval V., Sache I., Suffert F. Comparative pathogenicity of sexual and asexual spores of Zymoseptoria tritici (Septoria tritici blotch) on wheat leaves. Plant Pathol. 2015, 6:1429-1439.
27. Morais D., Sache I., Suffert F., Laval V. Is onset of Septoria tritici blotch epidemics related to local availability of ascospores?. Plant Pathol. 2016, 65:250-260.
28. Pariaud B., van den Berg F., van den Bosch F., Powers S.J., Kaltz O., Lannou C. Shared influence of pathogen and host genetics on a trade-off between latent period and spore production capacity in the wheat pathogen, Puccinia triticina. Evol. Appl. 2013, 6:303-312.
29. Pasco C., Montarry J., Marquer B., Andrivon D. And the nasty ones lose in the end: foliar pathogenicity trades off with asexual transmission in the Irish famine pathogen Phytophthora infestans. New Phytol. 2015, 209:334-342.
30. R Core Team R: A Language and Environment for Statistical Computing 2013, R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
31. Schürch S., Roy B.A. Comparing single- vs. mixed-genotype infections of Mycosphaerella graminicola on wheat: effects on pathogen virulence and host tolerance. Evol. Ecol. 2004, 18:1-14.
32. Scott P.R., Sanderson F.R., Benedikz P. Occurrence of Mycosphaerella graminicola, teleomorph of Septoria tritici, on wheat debris in the UK. Plant Pathol. 1988, 37:285-290.
33. Sommerhalder R.J., McDonald B.A., Mascher F., Zhan J. Effect of hosts on competition among clones and evidence of differential selection between pathogenic and saprophytic phases in experimental populations of the wheat pathogen Phaeosphaeria nodorum. Evol. Biol. 2011, 11:188.
34. Suffert F., Sache I. Relative importance of different types of inoculum to the establishment of Mycosphaerella graminicola in wheat crops in north-west Europe. Plant Pathol. 2011, 60:878-889.
35. Suffert F., Sache I., Lannou C. The early stages of Septoria tritici blotch epidemics of winter wheat: build-up, overseasoning, and discharge of primary inoculum. Plant Pathol. 2011, 60:166-177.
36. Suffert F., Sache I., Lannou C. Assessment of quantitative traits of aggressiveness in Mycosphaerella graminicola on adult wheat plants. Plant Pathol. 2013, 62:1330-1341.
37. Suffert F., Ravigné V., Sache I. Seasonal changes drive short-term selection for fitness traits in the wheat pathogen Zymoseptoria tritici. Appl. Environ. Microbiol. 2015, 81:6367-6379.
38. Susi H., Laine A.L. Pathogen life-history trade-offs revealed in allopatry. Evolution 2013, 67:3362-3370.
39. Trail F., Xu H., Loranger R., Gadoury D. Physiological and environmental aspects of ascospore discharge in Gibberella zeae (anamorph Fusarium graminearum). Mycologia 2002, 94:181-189.
40. Ware S.B. Aspects of Sexual Reproduction in Mycosphaerella graminicola Species on Wheat and Barley: Genetic Studies on Specificity, Mapping, and Fungicide Resistance 2006, (PhD thesis), Wageningen University, The Netherlands.
41. Waalwijk C.O., Mendes O., Verstappen E.C., De Waard M.A., Kema G.H. Isolation and characterization of the mating-type idiomorphs from the wheat septoria leaf blotch fungus Mycosphaerella graminicola. Fungal Genet. Biol. 2002, 35:277-286.
42. Wittenberg A.H.J., van der Lee T.A.J., Ben M'Barek S., Ware S.B., Goodwin S.B., Kilian A., Visser R.G.F., Kema G.H.J., Schouten H.J. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 2009, 4:e5863.
43. Zelikovitch N., Eyal Z. Reduction in pycnidial coverage after inoculation of wheat with mixtures of isolates of Septoria tritici. Plant Dis. 1991, 75:907-910.
44. Zhan J., Mundt C.C., Hoffer M.E., McDonald B. Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem. J. Evol. Biol. 2002, 15:634-647.