The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen.
BACKGROUND
Chytridiomycota species (chytrids) belong to a basal lineage in the fungal kingdom. Inhabiting terrestrial and aquatic environments, most are free-living saprophytes but several species cause important diseases: e.g. Batrachochytrium dendrobatidis, responsible for worldwide amphibian decline; and Synchytrium endobioticum, causing potato wart disease. S. endobioticum has an obligate biotrophic lifestyle and isolates can be further characterized as pathotypes based on their virulence on a differential set of potato cultivars. Quarantine measures have been implemented globally to control the disease and prevent its spread. We used a comparative approach using chytrid mitogenomes to determine taxonomical relationships and to gain insights into the evolution and recent history of introductions of this plant pathogen.


RESULTS
We assembled and annotated the complete mitochondrial genome of 30 S. endobioticum isolates and generated mitochondrial genomes for five additional chytrid species. The mitochondrial genome of S. endobioticum is linear with terminal inverted repeats which was validated by tailing and PCR amplifying the telomeric ends. Surprisingly, no conservation in organisation and orientation of mitochondrial genes was observed among the Chytridiomycota except for S. endobioticum and its sister species Synchytrium microbalum. However, the mitochondrial genome of S. microbalum is circular and comprises only a third of the 72.9 Kbp found for S. endobioticum suggesting recent linearization and expansion. Four mitochondrial lineages were identified in the S. endobioticum mitochondrial genomes. Several pathotypes occur in different lineages, suggesting that these have emerged independently. In addition, variations for polymorphic sites in the mitochondrial genome of individual isolates were observed demonstrating that S. endobioticum isolates represent a community of different genotypes. Such communities were shown to be complex and stable over time, but we also demonstrate that the use of semi-resistant potato cultivars triggers a rapid shift in the mitochondrial haplotype associated with increased virulence.


CONCLUSIONS
Mitochondrial genomic variation shows that S. endobioticum has been introduced into Europe multiple times, that several pathotypes emerged multiple times, and that isolates represent communities of different genotypes. Our study represents the most comprehensive dataset of chytrid mitogenomes, which provides new insights into the extraordinary dynamics and evolution of mitochondrial genomes involving linearization, expansion and reshuffling.
['van de Vossenberg|Bart T L H|BTLH|0000-0003-1205-6119', 'Brankovics|Balázs|B|', 'Nguyen|Hai D T|HDT|', 'van Gent-Pelzer|Marga P E|MPE|', 'Smith|Donna|D|', 'Dadej|Kasia|K|', 'Przetakiewicz|Jarosław|J|', 'Kreuze|Jan F|JF|', 'Boerma|Margriet|M|', 'van Leeuwen|Gerard C M|GCM|', 'André Lévesque|C|C|', 'van der Lee|Theo A J|TAJ|']
D000818:Animals D001499:Bayes Theorem D005075:Biological Evolution D008411:Chytridiomycota D004272:DNA, Mitochondrial D005060:Europe D014644:Genetic Variation D054629:Genome, Mitochondrial D006239:Haplotypes D058977:Molecular Sequence Annotation D010802:Phylogeny D010935:Plant Diseases D010944:Plants D011790:Quarantine D015203:Reproducibility of Results D013045:Species Specificity D014774:Virulence
Chytridiomycota Mitochondrial haplotypes Fungal communities Pathotype formation Pest introduction Population dynamics