Comparative genomic and transcriptomic analyses of trans-kingdom pathogen Fusarium solani species complex reveal degrees of compartmentalization

Hoh, Daphne Z.; Lee, Hsin-Han; Wada, Naohisa; Liu, Wei-An; Lu, Min R.; Lai, Cheng-Kuo; Ke, Huei-Mien; Sun, Pei-Feng; Tang, Sen-Lin; Chung, Wen-Hsin; Chen, Ying-Lien; Chung, Chia-Lin; Tsai, Isheng Jason

doi:10.1186/s12915-022-01436-7

Comparative genomic and transcriptomic analyses of trans-kingdom pathogen Fusarium solani species complex reveal degrees of compartmentalization

Journal Article · Thu Oct 20 00:00:00 EDT 2022 · BMC Biology

DOI:https://doi.org/10.1186/s12915-022-01436-7· OSTI ID:2471088

Hoh, Daphne Z. ^[1]; Lee, Hsin-Han ^[2]; Wada, Naohisa ^[2]; Liu, Wei-An ^[2]; Lu, Min R. ^[2]; Lai, Cheng-Kuo ^[3]; Ke, Huei-Mien ^[2]; Sun, Pei-Feng ^[1]; Tang, Sen-Lin ^[1]; Chung, Wen-Hsin ^[4]; Chen, Ying-Lien ^[5]; Chung, Chia-Lin ^[5]; ^[6]

Academia Sinica, Taipei (Taiwan); National Taiwan Normal University, Taipei (Taiwan)
Academia Sinica, Taipei (Taiwan)
Academia Sinica, Taipei (Taiwan); National Taiwan Univ., Taipei (Taiwan)
National Chung Hsing Univ., Taichung (Taiwan)
National Taiwan Univ., Taipei (Taiwan)
Academia Sinica, Taipei (Taiwan); National Taiwan Normal University, Taipei (Taiwan); National Taiwan Univ., Taipei (Taiwan)

Background: The Fusarium solani species complex (FSSC) comprises fungal pathogens responsible for mortality in a diverse range of animals and plants, but their genome diversity and transcriptome responses in animal pathogenicity remain to be elucidated. We sequenced, assembled and annotated six chromosome-level FSSC clade 3 genomes of aquatic animal and plant host origins. We established a pathosystem and investigated the expression data of F. falciforme and F. keratoplasticum in Chinese softshell turtle (Pelodiscus sinensis) host. Results: Comparative analyses between the FSSC genomes revealed a spectrum of conservation patterns in chromosomes categorised into three compartments: core, fast-core (FC), and lineage-specific (LS). LS chromosomes contribute to variations in genomes size, with up to 42.2% of variations between F. vanettenii strains. Each chromosome compartment varied in structural architectures, with FC and LS chromosomes contain higher proportions of repetitive elements with genes enriched in functions related to pathogenicity and niche expansion. We identified differences in both selection in the coding sequences and DNA methylation levels between genome features and chromosome compartments which suggest a multi-speed evolution that can be traced back to the last common ancestor of Fusarium. We further demonstrated that F. falciforme and F. keratoplasticum are opportunistic pathogens by inoculating P. sinensis eggs and identified differentially expressed genes also associated with plant pathogenicity. These included the most upregulated genes encoding the CFEM (Common in Fungal Extracellular Membrane) domain. Conclusions: The high-quality genome assemblies provided new insights into the evolution of FSSC chromosomes, which also serve as a resource for studies of fungal genome evolution and pathogenesis. This study also establishes an animal model for fungal pathogens of trans-kingdom hosts.

View Accepted Manuscript (DOE)

Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: Academia Sinica; National Science and Technology Council; USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2471088

Journal Information:: BMC Biology, Journal Name: BMC Biology Journal Issue: 1 Vol. 20; ISSN 1741-7007

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Comparative genomics and prediction of conditionally dispensable sequences in legume–infecting Fusarium oxysporum formae speciales facilitates identification of candidate effectors Williams, Angela; Sharma, Mamta; Thatcher, Louise Figshare https://doi.org/10.6084/m9.figshare.c.3632327	collection	January 2016
Amphibian chytridiomycosis: a review with focus on fungus-host interactions Rooij, Pascale Van; Martel, An; Haesebrouck, Freddy Figshare https://doi.org/10.6084/m9.figshare.c.3640196	collection	January 2015
ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees Zhang, Chao; Rabiee, Maryam; Sayyari, Erfan figshare https://doi.org/10.6084/m9.figshare.c.4093409.v1	collection	January 2018

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59 BASIC BIOLOGICAL SCIENCES
Animal pathogenicity
Chromosome evolution
Fusarium solani species complex
Genome compartments
Opportunistic pathogen
Turtle

Additional file 1 of Comparative genomic and transcriptomic analyses of trans-kingdom pathogen Fusarium solani species complex reveal degrees of compartmentalization Hoh, Daphne Z.; Lee, Hsin-Han; Wada, Naohisa https://doi.org/10.6084/m9.figshare.21376426.v1 The current record is supplemented by this dataset	dataset	January 2022
Comparative genomic and transcriptomic analyses of trans-kingdom pathogen Fusarium solani species complex reveal degrees of compartmentalization Hoh, Daphne Z.; Lee, Hsin-Han; Wada, Naohisa https://doi.org/10.6084/m9.figshare.c.6259510 The current record is supplemented by this collection	collection	January 2022

Comparative genomic and transcriptomic analyses of trans-kingdom pathogen Fusarium solani species complex reveal degrees of compartmentalization

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