Submitted to: Gigascience
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/25/2024
Publication Date: 6/28/2024
Citation: Baroncelli, R., Cobo-Diaz, J.F., Benocci, T., Peng, M., Battaglia, E., Haridas, S., Andreopoulos, W., Labutti, K., Pangilinan, J., Lipzen, A., Koriabine, M., Bauer, D., Le Floch, G., Makela, M.R., Drula, E., Henrissat, B., Grigoriev, I.V., Crouch, J., De Vries, R.P., Sukno, S.A., Thon, M.R. 2024. Genome evolution and transcriptome plasticity associated with adaptation to monocot and eudicot plants in Colletotrichum fungi. Gigascience 13:1-18. https://doi.org/10.1093/gigascience/giae036.
DOI: https://doi.org/10.1093/gigascience/giae036

Interpretive Summary: Fungi cause billions of dollars of damage to agricultural crops and natural resources in the United States each year. How fungi cause plant diseases is not known, especially at the very basic level of genes. This work studied a group of fungi that cause anthracnose disease of countless crops worldwide. Using genome data, scientists were able to reveal the core genes and processes that the anthracnose fungi use to break down plant cells into nutrients that the fungi can consume, which ultimately leads to plant disease. This information is useful to scientists who are working to understand the genetic basis of how fungi cause plant diseases and the interactions that occur between a fungal pathogen and its host.

Technical Abstract: Colletotrichum fungi infect a wide diversity of monocot and eudicot hosts, causing plant diseases on almost all economically important crops worldwide. In addition to its economic impact, Colletotrichum is a suitable model for the study of gene family evolution on a fine scale to uncover events in the genome that are associated with the evolution of biological characters important for host interactions. Here, we present the genome sequences of 30 Colletotrichum species, 18 of them newly sequenced, covering the taxonomic diversity within the genus. A time-calibrated tree revealed that the Colletotrichum ancestor diverged in the late Cretaceous around 70 million years ago (mya) in parallel with the diversification of flowering plants. We provide evidence of independent host jumps from eudicots to monocots during the evolution of this pathogen, coinciding with a progressive shrinking of the degradative arsenal and expansions in lineage specific genes. Comparative transcriptomics of four reference species with different evolutionary histories and adapted to different hosts revealed similarity in gene content but high diversity in the modulation of their transcription profiles. Only a few orthologs show similar expression profiles on different plant cell walls. Combining genome sequences and expression profiles we identified a set of core genes, such as specific transcription factors, involved in plant cell wall degradation in Colletotrichum. Together, these results indicate that the ancestral Colletotrichum were associated with eudicot plants and certain branches progressively adapted to different monocot hosts, reshaping part of the degradative and transcriptional arsenal.