Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola

• Published in: PloS one 2009-06, Vol.4 (6), p.e5863
• Main Authors: Wittenberg, A.H.J, Lee, T.A.J. van der, Ben M'Barek, S, Ware, S.B, Goodwin, S.B, Kilian, A, Visser, R.G.F, Kema, G.H.J, Schouten, H.J
• Format: Article
• Language: English
• Subjects: Algeria; Amplified fragment length polymorphism; Analysis; Antibiotics; Asci; Ascomycota - genetics; Ascomycota - physiology; Ascospores; BASIC BIOLOGICAL SCIENCES; Biointeracties and Plant Health; Bread; Chromosome Mapping; chromosome number; chromosome transmission; Chromosomes; Chromosomes, Fungal; Crosses, Genetic; crossing; Deoxyribonucleic acid; diploidy; Disjunction; DNA; Domestication; Drug resistance; durum wheat; EPS-4; Fungi; Gene mapping; Genes; Genes, Fungal; Genetic crosses; Genetic diversity; Genetic Linkage; Genetic Markers; Genetic polymorphisms; Genetics and Genomics/Chromosome Biology; Genetics and Genomics/Genome Projects; Genetics and Genomics/Microbial Evolution and Genomics; genome; Genome, Fungal; Genomes; Genomics; Genotyping; haploidy; Homologous recombination; Homology; Laboratories; Laboratorium voor Fytopathologie; Laboratorium voor Phytopathologie; Laboratorium voor Plantenveredeling; Laboratory of Phytopathology; Laboratory of Plant Breeding; leaf blotch; Meiosis; meiotic drive; microbial genetics; Microbiology/Plant-Biotic Interactions; microsatellite repeats; Models, Genetic; Mycosphaerella graminicola; Netherlands; Nondisjunction; Offspring; Parents; Pathogenicity; Pathogens; Plant Breeding; plant pathogenic fungi; Plant sciences; Plants - microbiology; Plastic properties; Plasticity; Polymerase Chain Reaction; PRI Biodiversiteit en Veredeling; PRI Biodiversity and Breeding; PRI Biointeractions en Plantgezondheid; Progeny; Science & Technology - Other Topics; Sequence Analysis, DNA; strains; Studies; Translocation, Genetic; Triticum aestivum; Triticum turgidum subsp. durum; Wheat
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0005863

Meiosis in the haploid 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 meiotic transmission of unequal chromosome numbers, two segregating populations were generated by crossing genetically unrelated parent isolates originating from Algeria and The Netherlands 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 in filamentous fungi. These chromosomes vary from 0.39 to 0.77 Mb in size, and represent up to 38% of the chromosomal complement. 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. Between 15-20% of the progeny isolates lacked one or more chromosomes that were present in both parents. The two high-density maps showed no recombination of dispensable chromosomes and hence, their meiotic processing may require distributive disjunction, a phenomenon that is rarely observed in fungi. The maps also enabled the identification of individual twin isolates from a single ascus that shared the same missing or doubled chromosomes indicating 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 could be among the strategies enabling this versatile pathogen to quickly overcome adverse biotic and abiotic conditions in wheat fields.