Genome evolution and transcriptome plasticity is associated with adaptation to monocot and dicot plants in Colletotrichum fungi

• Published in: Gigascience 2024-01, Vol.13
• Main Authors: Baroncelli, Riccardo, Cobo-Díaz, José F, Benocci, Tiziano, Peng, Mao, Battaglia, Evy, Haridas, Sajeet, Andreopoulos, William, LaButti, Kurt, Pangilinan, Jasmyn, Lipzen, Anna, Koriabine, Maxim, Bauer, Diane, Le Floch, Gaetan, Mäkelä, Miia R, Drula, Elodie, Henrissat, Bernard, Grigoriev, Igor V, Crouch, Jo Anne, de Vries, Ronald P, Sukno, Serenella A, Thon, Michael R
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - genetics; anthracnose; Biological effects; Biological evolution; Cell walls; Colletotrichum; Colletotrichum - genetics; Colletotrichum - pathogenicity; comparative transcriptomics; Cretaceous; Economic importance; Evolution; Evolution, Molecular; Evolutionary genetics; Flowering; fungal evolution; fungal genomics; Fungi; Gene Expression Profiling - methods; Gene families; Gene regulation; Gene sequencing; Genome, Fungal; Genomes; Host plants; Phylogeny; plant cell walls; Plant diseases; Plant Diseases - genetics; Plant Diseases - microbiology; Plant layout; Plants (botany); Substrates; Transcription factors; Transcriptome; Transcriptomes; Transcriptomics
• ISSN: 2047-217X; 2047-217X
• DOI: 10.1093/gigascience/giae036

Abstract Background Colletotrichum fungi infect a wide diversity of monocot and dicot hosts, causing diseases on almost all economically important plants worldwide. Colletotrichum is also a suitable model for studying gene family evolution on a fine scale to uncover events in the genome associated with biological changes. Results Here we present the genome sequences of 30 Colletotrichum species covering the diversity within the genus. Evolutionary analyses revealed that the Colletotrichum ancestor diverged in the late Cretaceous in parallel with the diversification of flowering plants. We provide evidence of independent host jumps from dicots to monocots during the evolution of Colletotrichum, coinciding with a progressive shrinking of the plant cell wall degradative arsenal and expansions in lineage-specific gene families. Comparative transcriptomics of 4 species adapted to different hosts revealed similarity in gene content but high diversity in the modulation of their transcription profiles on different plant substrates. Combining genomics and transcriptomics, we identified a set of core genes such as specific transcription factors, putatively involved in plant cell wall degradation. Conclusions These results indicate that the ancestral Colletotrichum were associated with dicot plants and certain branches progressively adapted to different monocot hosts, reshaping the gene content and its regulation.