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United States Department of Agriculture

Agricultural Research Service

Research Project: MOLECULAR AND GENETIC MECHANISMS OF FUNGAL DISEASE RESISTANCE IN GRAIN CROPS Title: Meiosis Drives Extraordinary Genome Plasticity in the Haploid Fungal Plant Pathogen Mycosphaerella Graminicola

Authors
item Wittenberg, Alexnder H. - PLANT RES. INTERNATIONAL
item Van Der Lee, Theo - PLANT RES. INTERNATIONAL
item M'Barek, Sarrah - PLANT RES. INTERNATIONAL
item Ware, Sarah - PLANT RES. INTERNATIONAL
item Goodwin, Stephen
item Kilian, Andrzej - DIVERSITY ARRAYS, AUSTRAL
item Visser, Richard G. - PLANT RES. INTERNATIONAL
item Kema, Gert H. - PLANT RES INTERNATIONAL
item Schouten, Henk - PLANT RES INTERNATIONAL

Submitted to: PLoS One
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: March 27, 2009
Publication Date: June 10, 2009
Repository URL: http://hdl.handle.net/10113/36793
Citation: Wittenberg, A.J., Van Der Lee, T.A., M'Barek, S.B., Ware, S.B., Goodwin, S.B., Kilian, A., Visser, R.F., Kema, G.J., Schouten, H.J. 2009. Meiosis Drives Extraordinary Genome Plasticity in the Haploid Fungal Plant Pathogen Mycosphaerella Graminicola. PLoS One. Available: PLoSONE4(6):e5863.doi:10.1371/journal/pone.005863

Interpretive Summary: Septoria tritici blotch, caused by Mycosphaerella graminicola, is one of the most common and economically important fungal diseases of wheat worldwide. Control of the disease is hampered by high genetic diversity of the pathogen within field populations, which may be due to chromosomes that can be missing and therefore appear to be dispensable. To test the hypothesis that genetic variation can be generated during sexual reproduction, genetic analyses were performed in two independent crosses with a large number of molecular markers. These analyses revealed that the eight smallest chromosomes of M. graminicola could be dispensable. Chromosome numbers among progeny isolates varied widely, with some progeny missing up to three chromosomes, while other strains had two copies of one or more chromosomes. From 15-20% of the progeny isolates lacked one or more chromosomes that were present in both parents with no apparent effect on their fitness. High genome plasticity likely explains how this versatile pathogen can quickly adapt to new fungicides and host resistance genes. This is the first report of such a high number of dispensable chromosomes in a fungus and will be of great interest to geneticists and plant pathologists trying to understand the mechanisms by which new genetic variation is generated. Further analyses of the dispensable chromosomes may indicate how they can influence pathogenicity and fungicide resistance. Evolutionary biologists can use this information for a better understanding of the processes generating genetic variability within natural populations. The genetic mapping approach developed for this project will serve to guide future analyses of dispensable chromosomes in other organisms.

Technical Abstract: Meiosis in the plant-pathogenic fungus Mycosphaerella graminicola results in eight ascospores due to a mitotic division following the two meiotic divisions. The transient diploid phase allows for recombination among homologous chromosomes. However, some chromosomes of M. graminicola lack homologs and do not pair during meiosis. Because these chromosomes are not present universally in the genome of the organism they can be considered to be dispensable. To analyze the genetics of dispensable chromosomes, two segregating populations were generated by crossing genetically unrelated parent isolates that had pathogenicity towards durum or bread wheat, respectively. Detailed genetic analyses of these progenies using high-density mapping (1793 DArT, 258 AFLP and 25 SSR markers) and graphical genotyping revealed that M. graminicola has up to eight dispensable chromosomes, the highest number reported. These chromosomes vary from 0.39 to 0.77 Mb in size, and represent up to 40% of the genome in total. Chromosome numbers among progeny isolates varied widely, with some progeny missing up to three chromosomes, while other strains were disomic for one or more chromosomes. From 15-20% of the progeny isolates lacked one or more chromosomes that were present in both parents. The two high-density maps enabled the identification of individual twin isolates from a single ascus. Twin isolates shared the same missing or doubled chromosomes, showing that the chromosomal polymorphisms were mitotically stable and originated from nondisjunction during the second division and, less frequently, during the first division of fungal meiosis. High genome plasticity likely explains how this versatile pathogen can quickly overcome adverse biotic and abiotic conditions in wheat fields.

Last Modified: 12/17/2014
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