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

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Title: Genome evolution and transcriptome plasticity is associated with adaptation to monocot and dicot plants in Colletotrichum fungi
Authors: Baroncelli, Riccardo, Cobo-Díaz, José, 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, Drula, Elodie, Henrissat, Bernard, Grigoriev, Igor, Crouch, Jo Anne, de Vries, Ronald, Sukno, Serenella, Thon, Michael
Contributors: Tecnologia de los Alimentos, Facultad de Veterinaria, Terrapon, Nicolas, Universidad de Salamanca España = University of Salamanca Spain, Laboratoire Universitaire de Biodiversité et Ecologie Microbienne (LUBEM), Université de Brest (UBO), Universiteit Utrecht / Utrecht University Utrecht, Microbiology and Kluyver Centre for Genomics of Industrial Fermentation, Fungal Physiology, CBS‑KNAW Fungal Biodiversity Centre and Fungal, United States Department of Energy Joint Genome Institute, Department of Energy / Joint Genome Institute (DOE), Los Alamos National Laboratory (LANL), University of California Berkeley (UC Berkeley), University of California (UC), US Department of Energy Joint Genome Institute, U.S Department of Energy, U.S. Department of Energy Washington (DOE)-U.S. Department of Energy Washington (DOE), Joint Genome Institute (JGI), United States Department of Energy, Helsingin yliopisto = Helsingfors universitet = University of Helsinki, Biodiversité et Biotechnologie Fongiques (BBF), Aix Marseille Université (AMU)-École Centrale de Marseille (ECM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Architecture et fonction des macromolécules biologiques (AFMB), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), United States Department of Agriculture (USDA), Science Faculty, Université Mohammed V de Rabat Agdal (UM5)
Source: Gigascience
GREDOS. Repositorio Institucional de la Universidad de Salamanca
Universidad de Salamanca (USAL)
BULERIA. Repositorio Institucional de la Universidad de León
Universidad de León
GigaScience, vol 13
Publisher Information: Oxford University Press (OUP), 2024.
Publication Year: 2024
Subject Terms: 3309 Tecnología de Los Alimentos, [SDV]Life Sciences [q-bio], Tecnología de los alimentos, Plant Biology, 3103 Agronomía, MESH: Colletotrichum, 3105 Genetics (for-2020), MESH: Adaptation, MESH: Plant Diseases, fungal genetics, plant pathogens, genomics, evolution, Fungal genomics, Anthracnose, MESH: Phylogeny, Phylogeny, 2. Zero hunger, Genome, 3107 Microbiology (for-2020), Biological Sciences, fungal genomics, Plant cell walls, Adaptation, Physiological, [SDV] Life Sciences [q-bio], Molecular (mesh), Fungal, hongos, plant cell walls, Genome, Fungal, Biotechnology, Fungal (mesh), Evolution, Physiological, Biotechnology (rcdc), Phylogeny (mesh), Microbiology, 3104 Evolutionary Biology (for-2020), Evolution, Molecular, MESH: Gene Expression Profiling, Comparative transcriptomics, comparative transcriptomics, MESH: Evolution, Genetics, Colletotrichum, Physiological (mesh), MESH: Genome, Adaptation, fungal evolution, genome, Plant Diseases, Evolutionary Biology, anthracnose, genoma, 31 Biological Sciences (for-2020), Genetics (rcdc), MESH: Transcriptome, Research, Gene Expression Profiling, Human Genome, Fungi, Molecular, 15. Life on land, Transcriptome (mesh), Human Genome (rcdc), Gene Expression Profiling (mesh), Colletotrichum (mesh), Fungal evolution, fungi, Plant Diseases (mesh), Transcriptome, 3108 Plant Biology (for-2020)
Description: 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.
Document Type: Article
Other literature type
File Description: application/pdf
Language: English
ISSN: 2047-217X
DOI: 10.1093/gigascience/giae036
DOI: 10.1093/gigascience/giae036/7701018
Access URL: https://pubmed.ncbi.nlm.nih.gov/38940768
http://hdl.handle.net/10366/162114
https://hdl.handle.net/10612/24351
https://academic.oup.com/gigascience/article/doi/10.1093/gigascience/giae036/7701018
https://pure.knaw.nl/portal/en/publications/357bfb75-363c-4001-bdee-cc743c71e090
https://hdl.handle.net/20.500.11755/357bfb75-363c-4001-bdee-cc743c71e090
https://doi.org/10.1093/gigascience/giae036
https://research-portal.uu.nl/en/publications/a58c3c29-b880-4b5e-b928-375366307b92
https://doi.org/10.1093/gigascience/giae036
https://hdl.handle.net/10612/24351
https://escholarship.org/content/qt3dc2r85v/qt3dc2r85v.pdf
https://escholarship.org/uc/item/3dc2r85v
Rights: CC BY
URL: http://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
Accession Number: edsair.doi.dedup.....87aad54b6271dd30f6bcc07b616cc47d
Database: OpenAIRE
Description
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.
ISSN:2047217X
DOI:10.1093/gigascience/giae036