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

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

doi:10.1093/gigascience/giae036

Cited by 3 publications

References 108 publications

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

Baroncelli,

Cobo-Díaz,

Benocci

et al. 2024

GigaScience

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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.

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

Baroncelli,

Cobo-Díaz,

Benocci

et al. 2024

GigaScience

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Genomic streamlining of seagrass-associatedColletotrichumsp. may be related to its adaptation to a marine monocot host

Ettinger,

Eisen,

Stajich

2024

Preprint

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Colletotrichumspp. have a complicated history of association with land plants. Perhaps most well-known as plant pathogens for the devastating effect they can have on agricultural crops, someColletotrichumspp. have been reported as beneficial plant endophytes. However, there have been only a handful of reports ofColletotrichumspp. isolated from aquatic plant hosts and their ecological role in the marine ecosystem is underexplored. To address this, we present the draft genome and annotation ofColletotrichumsp. CLE4, previously isolated from rhizome tissue from the seagrassZostera marina. This genome (48.03 Mbp in length) is highly complete (BUSCO ascomycota: 98.8%) and encodes 12,015 genes, of which 5.7% are carbohydrate-active enzymes (CAZymes) and 12.6% are predicted secreted proteins. Phylogenetic placement putsColletotrichumsp. CLE4 within theC. acutatumcomplex, closely related toC. godetiae. We found a 8.69% smaller genome size, 21.90% smaller gene count, and the absence of 591 conserved gene families inColletotrichumsp. CLE4 relative to other members of theC. acutatumcomplex, suggesting a streamlined genome possibly linked to its specialized ecological niche in the marine ecosystem. Machine learning analyses using CATAStrophy on CAZyme domains predict this isolate to be a hemibiotroph, such that it has a biotrophic phase where the plant is kept alive during optimal environmental conditions followed by a necrotrophic phase where the fungi actively serves a pathogen. While future work is still needed to definitively tease apart the lifestyle strategy ofColletotrichumsp. CLE4, this study provides foundational insight and a high-quality genomic resource for starting to understand the evolutionary trajectory and ecological adaptations of marine-plant associated fungi.

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Comparative Genomics Reveals Sources of Genetic Variability in the Asexual Fungal Plant Pathogen Colletotrichum lupini

Alkemade,

Hohmann,

Messmer

et al. 2024

Molecular Plant Pathology

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Fungal plant pathogens cause major crop losses worldwide, with many featuring compartmentalised genomes that include both core and accessory regions, which are believed to drive adaptation. The highly host‐specific fungus Colletotrichum lupini greatly impacts lupin (Lupinus spp.) cultivation. This pathogen is part of clade 1 of the C. acutatum species complex and comprises four genetically uniform, presumably clonal, lineages (I–IV). Despite this, variation in virulence and morphology has been observed within these lineages. To investigate the potential sources of genetic variability in this asexual fungus, we compared the genomes of 16 C. lupini strains and 17 related Colletotrichum species. Phylogenomics confirmed the presence of four distinct lineages, but further examination based on genome size, gene content, transposable elements (TEs), and deletions revealed that lineage II could be split into two groups, II‐A and II‐B. TE content varied between lineages and correlated strongly with genome size variation, supporting a role for TEs in genome expansion in this species. Pangenome analysis revealed a highly variable accessory genome, including a minichromosome present in lineages II, III, and IV, but absent in lineage I. Accessory genes and effectors appeared to cluster in proximity to TEs. Presence/absence variation of putative effectors was lineage‐specific, suggesting that these genes play a crucial role in determining host range. Notably, no effectors were found on the TE‐rich minichromosome. Our findings shed light on the potential mechanisms generating genetic diversity in this asexual fungal pathogen that could aid future disease management.

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

Cited by 3 publications

References 108 publications

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

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

Genomic streamlining of seagrass-associatedColletotrichumsp. may be related to its adaptation to a marine monocot host

Comparative Genomics Reveals Sources of Genetic Variability in the Asexual Fungal Plant Pathogen Colletotrichum lupini

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