Wageningen UR, Droevendaalsesteeg 1, Biointeractions and Plant Health & Plant Breeding, 6708, PB, Wageningen, The Netherlands.
Dutch National Plant Protection Organization, National Reference Centre, Geertjesweg 15, 6706EA, Wageningen, The Netherlands.
BMC Evol Biol. 2018 Sep 10;18(1):136. doi: 10.1186/s12862-018-1246-6.
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.
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.
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.
壶菌门物种（壶菌）属于真菌界的一个基础谱系。栖息于陆地和水生环境中，大多数是自由生活的腐生菌，但有几个物种会引起重要疾病：例如，引起全球两栖动物减少的蛙壶菌；以及导致马铃薯疣病的Synchytrium endobioticum。S. endobioticum 具有专性生物营养生活方式，并且根据其在不同马铃薯品种上的毒力，可以将分离株进一步表征为致病型。全球已实施检疫措施来控制该疾病并防止其传播。我们使用比较方法，利用壶菌线粒体基因组来确定分类学关系，并深入了解这种植物病原体的进化和最近的传入历史。
我们组装并注释了 30 个 S. endobioticum 分离株的完整线粒体基因组，并生成了另外五个壶菌物种的线粒体基因组。S. endobioticum 的线粒体基因组是线性的，具有末端反向重复序列，这通过尾随和 PCR 扩增端粒得到了验证。令人惊讶的是，除了 S. endobioticum 和其姐妹种 Synchytrium microbalum 之外，在壶菌门中没有观察到线粒体基因的组织和方向的保守性。然而，S. microbalum 的线粒体基因组是圆形的，仅包含 S. endobioticum 中发现的 72.9 Kbp 的三分之一，这表明最近发生了线性化和扩张。在 S. endobioticum 线粒体基因组中鉴定出四个线粒体谱系。不同谱系中出现了几种致病型，表明这些是独立出现的。此外，还观察到单个分离株的线粒体基因组中多态性位点的变异，表明 S. endobioticum 分离株代表了不同基因型的群落。这种群落随着时间的推移被证明是复杂而稳定的，但我们也证明，使用半抗性马铃薯品种会触发与毒力增加相关的线粒体单倍型的快速转变。
线粒体基因组的变异表明，S. endobioticum 已多次传入欧洲，多个致病型已多次出现，并且分离株代表了不同基因型的群落。我们的研究代表了最全面的壶菌线粒体基因组数据集，为涉及线性化、扩张和重排的线粒体基因组的非凡动态和进化提供了新的见解。
