Unveiling the arsenal of apple bitter rot fungi: comparative genomics identifies candidate effectors, CAZymes and biosynthetic gene clusters in Colletotrichum species

Authors: KHODADADI, FATEMEH - University Of California, Riverside; LUCIANO-ROSARIO, DIANIRIS - Oak Ridge Institute For Science And Education (ORISE); Gottschalk, Christopher; Jurick, Wayne; ACIMOVIC, SRDJAN - Virginia Tech

Submitted to: The Journal of Fungi
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/9/2024
Publication Date: 7/16/2024
Citation: Khodadadi, F., Luciano-Rosario, D., Gottschalk, C.C., Jurick Ii, W.M., Acimovic, S. 2024. Unveiling the arsenal of apple bitter rot fungi: comparative genomics identifies candidate effectors, CAZymes and biosynthetic gene clusters in Colletotrichum species. The Journal of Fungi. 10(7):493. https://doi.org/10.3390/jof10070493.
DOI: https://doi.org/10.3390/jof10070493

Interpretive Summary: Many of the common apple varieties produced today are susceptible to Colletotrichum spp. which infects fruit before harvest and causes significant loss of fruit during storage. Colletrotrichum is a group/complex of fungal pathogens that result in the disease called bitter rot in apples and can infect many other fruits and vegetables. To investigate the mechanisms associated with infection by Colletotrichum spp., we set out to obtain genome sequences of selected strains isolated from infected fruit from the Mid-Atlantic region. Using the genomic data, we first conducted phylogenetic experiments to identify which species our isolates represent. We then utilized advanced bioinformatic tools to discover and document the presence of genes associated with species identity and/or involvement in the infection process. In addition, we documented the clusters of genes within each genome that are associated with the production of secondary metabolites which include toxins, hormones, and chemicals associated with food safety. Using this data, we found high similarity for genes associated with species identity and/or involved in the infection process, and gene clusters associated with secondary metabolites across all nine of the Colletotrichum isolates in our dataset. We additionally found the genome sequences supported previous species classification for the isolates, which provides a census for what species are problematic for the Mid-Atlantic region. The results presented in this study provide a platform to identify targets within the genome that could be used in new control strategies.

Technical Abstract: Bitter rot of apple is caused by Colletotrichum spp. and is a serious pre-harvest pathogen that can manifest in postharvest losses on late harvested fruit. In this study, we obtained genome sequences from four different Colletotrichum spp. that infect apple and cause diseases on other fruits, vegetables and flowers. Our genomic data was obtained from isolates/species that have not yet been sequenced that represent geographic-specific regions. Genome sequencing allowed construction of phylogenetic trees, which corroborated the overall concordance observed in prior MLST studies. Bioinformatic pipelines were used to discover CAZyme, effector and Secondary Metabolic (SM) gene clusters in all nine Colletotrichum isolates. We found redundancy and a high level of similarity across species regarding CAZyme classes and predicted cytoplastic and apoplastic effectors. SM gene clusters displayed the most diversity in type and the most common cluster was one that is responsible for alternapyrone. Our study provides a solid platform to identify targets for functional studies that underpin pathogenicity, virulence, and/or quiescence that can be targeted for development of new control strategies. With these new genomics resources, exploration via omics-based technologies using these isolates will help ascertain the biological underpinnings of their widespread success and observed geographic dominance in specific areas throughout the country.