Transposable elements contribute to the evolution of genomic diversity between strains of the plant pathogenic fungus Colletotrichum higginsianum

Ayako Tsushima 1,2 Pamela Gan 2 Naoyoshi Kumakura 2 Mari Narusaka 3 Yoshitaka Takano 4 Yoshihiro Narusaka 3 Ken Shirasu 1,2
1Graduate School of Science, The University of Tokyo, Tokyo, Japan
2Center for Sustainable Resource Science, RIKEN, Yokohama, Japan
3Plant Activation Research Group, Research Institute for Biological Sciences Okayama, Kaga-gun, Japan
4Graduate School of Agriculture, Kyoto University, Kyoto, Japan

The members of the genus Colletotrichum cause anthracnose disease on a broad range of crops and have a devastating economic impact. Further, the interaction between Colletotrichum higginsianum and its host, the model plant Arabidopsis thaliana, has been a useful pathosystem to study fungal hemibiotrophic infection of plants. Genomic analyses of other fungal plant pathogens have revealed that fast-evolving genomic compartments are often enriched in genes encoding effectors, which are diverse, small, secreted proteins involved in pathogenicity. In order to investigate if genomic compartmentalization exists in C. higginsianum, we sequenced the genome of strain MAFF305635-RFP from Japan with PacBio RSII, yielding an assembly of 49.8 Mb consisting of 28 contigs. This assembly was compared to the genome of strain IMI349063 from Trinidad and Tobago (Zampounis et al., 2016). The two strains are closely related, sharing 88.2 % of sequence (≥ 99 % identity, ≥ 15 kb). However, this analysis revealed the presence of extensive genomic rearrangements between the two strains. Among these, 6 inter-chromosomal translocations and 4 intra-chromosomal inversions were identified. Whole-genome comparisons also revealed the presence of strain-specific regions in the genome of this species including regions encoding strain-specific effector candidates. Interestingly, large-scale genomic rearrangements and strain-specific regions tend to associate with transposable elements. This result suggests that mobile elements may increase the genomic plasticity of this pathogen by contributing to homology-based recombination through their repetitive sequences and direct disruption through transpositions. The novel insights from this study will help pathogenicity-related gene mining of C. higginsianum by considering its dynamic genomic changes.