The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen

Abstract

BackgroundChytridiomycota 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.ResultsWe 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.ConclusionsMitochondrial 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.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1246-6) contains supplementary material, which is available to authorized users.

TheSynchytrium endobioticumAvrSen1 triggers a Hypersensitive Response in Sen1 potatoes while natural variants evade detection

“…Out of sequence data generated by Van de Vossenberg et al . (10), fourteen isolates were selected because of their >10 x median sequence coverage and known pathotype identity (Fig. S1).…”

“…The presence of the AvrSen1 gene or its variants could be determined in seventeen of thirty S. endobioticum isolates sequenced by Van de Vossenberg et al . (10) by mapping of Illumina sequence reads to the MB42 genome. In addition, PacBio SMRT CCS reads generated from the AvrSen1 amplicon allowed the detection of AvrSen1 gene or its variants for three additional isolates.…”

“…4). Based on variation of the mitochondrial genome, S. endobioticum isolates clustered in four major groups (haplogroups), representing separate introductions from which pathotypes 2(G1) and 6(O1) emerged multiple times independently (10).…”

“…Distribution of AvrSen1 and its variants among S. endobioticum isolates visualized in the mitochondrial haplotype network from Van de Vossenberg et al . (10). Colors represent the presence of AvrSen1 or its variants for a given isolate as identified from read-mapping to the MB42 genome or through PacBio amplicon sequencing.…”

“…Comparative analysis of thirty S. endobioticum isolates using their mitochondrial genome sequences, showed that the pathogen was introduced multiple times in Europe and successively several pathotypes emerged in parallel. Interestingly, single isolates we found to represent populations of distinct genotypes (10).…”