101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens

Haridas, Sajeet; Albert, Réka; Binder, Manfred; Bloem, J.; LaButti, Kurt; Salamov, Asaf; Andreopoulos, Bill; Baker, Scott E.; Barry, Kerrie; Bills, Gerald F.; Bluhm, Burton H.; Cannon, Charles H.; Castanera, Raúl; Culley, David E.; Daum, Christopher; Ezra, D.; Gonzalez, Jennifer B; Henrissat, Bernard; Kuo, Alan; Liang, Chen; Lipzen, Anna; Lutzoni, François; Magnuson, Jon; Mondo, Stephen J.; Nolan, Matt; Ohm, Robin A.; Pangilinan, Jasmyn; Park, H.-J.; Ramı́rez, Lucı́a; Alfaro, Michael E.; Sun, Hui; Tritt, Andrew; Yoshinaga, Yuko; Zwiers, L.H.; Turgeon, Benjamin; Goodwin, Stephen B.; Spatafora, Joseph W.; Crous, Pedro W.; Grigoriev, Igor V.

doi:10.1016/j.simyco.2020.01.003

Cited by 149 publications

(143 citation statements)

References 51 publications

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“…Whole-genome level approaches are increasingly employed in fungi to surmount issues of resolution and support in single- and multi-marker studies (Gladieux et al 2015 ; Magain et al 2017 ; Lorch et al 2018 ; Kobmoo et al 2019 ; Morin et al 2019 ; Haridas et al 2020 ). For prokaryotes, the computationally inexpensive assessment of average nucleotide identity (ANI) has proven popular, although maximum-likelihood methods are also being applied (Parks et al 2018 ).…”

Section: Species: From Concepts To Identificationmentioning

confidence: 99%

Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding?

et al. 2020

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True fungi (Fungi) and fungus-like organisms (e.g. Mycetozoa, Oomycota) constitute the second largest group of organisms based on global richness estimates, with around 3 million predicted species. Compared to plants and animals, fungi have simple body plans with often morphologically and ecologically obscure structures. This poses challenges for accurate and precise identifications. Here we provide a conceptual framework for the identification of fungi, encouraging the approach of integrative (polyphasic) taxonomy for species delimitation, i.e. the combination of genealogy (phylogeny), phenotype (including autecology), and reproductive biology (when feasible). This allows objective evaluation of diagnostic characters, either phenotypic or molecular or both. Verification of identifications is crucial but often neglected. Because of clade-specific evolutionary histories, there is currently no single tool for the identification of fungi, although DNA barcoding using the internal transcribed spacer (ITS) remains a first diagnosis, particularly in metabarcoding studies. Secondary DNA barcodes are increasingly implemented for groups where ITS does not provide sufficient precision. Issues of pairwise sequence similarity-based identifications and OTU clustering are discussed, and multiple sequence alignment-based phylogenetic approaches with subsequent verification are recommended as more accurate alternatives. In metabarcoding approaches, the trade-off between speed and accuracy and precision of molecular identifications must be carefully considered. Intragenomic variation of the ITS and other barcoding markers should be properly documented, as phylotype diversity is not necessarily a proxy of species richness. Important strategies to improve molecular identification of fungi are: (1) broadly document intraspecific and intragenomic variation of barcoding markers; (2) substantially expand sequence repositories, focusing on undersampled clades and missing taxa; (3) improve curation of sequence labels in primary repositories and substantially increase the number of sequences based on verified material; (4) link sequence data to digital information of voucher specimens including imagery. In parallel, technological improvements to genome sequencing offer promising alternatives to DNA barcoding in the future. Despite the prevalence of DNA-based fungal taxonomy, phenotype-based approaches remain an important strategy to catalog the global diversity of fungi and establish initial species hypotheses.

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Section: Species: From Concepts To Identificationmentioning

confidence: 99%

Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding?

et al. 2020

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“…For example, the three subphyla differ in their genome sizes, with the genomes of Pezizomycotina species being notably larger (~42 Mb) than those of Saccharomycotina (~13 Mb) and Taphrinomycotina (~14 Mb) ( 26 ). While several recent studies have analyzed major lineages within the two largest subphyla (in terms of number of described species), Saccharomycotina ( 2 , 19 , 27 ) and Pezizomycotina ( 28 , 29 ), comparisons of genome evolution across the two subphyla are lacking. For example, a recent analysis of the tempo and mode of genome evolution in 332 Saccharomycotina found evidence of high evolutionary rates and reductive evolution across this subphylum ( 2 ), but whether budding yeasts are faster evolving than filamentous fungi remains unknown.…”

Section: Introductionmentioning

confidence: 99%

Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota

et al. 2020

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Ascomycota, the largest and most well-studied phylum of fungi, contains three subphyla: Saccharomycotina (budding yeasts), Pezizomycotina (filamentous fungi), and Taphrinomycotina (fission yeasts). Despite its importance, we lack a comprehensive genome-scale phylogeny or understanding of the similarities and differences in the mode of genome evolution within this phylum. By examining 1107 genomes from Saccharomycotina (332), Pezizomycotina (761), and Taphrinomycotina (14) species, we inferred a robust genome-wide phylogeny that resolves several contentious relationships and estimated that the Ascomycota last common ancestor likely originated in the Ediacaran period. Comparisons of genomic properties revealed that Saccharomycotina and Pezizomycotina differ greatly in their genome properties and enabled inference of the direction of evolutionary change. The Saccharomycotina typically have smaller genomes, lower guanine-cytosine contents, lower numbers of genes, and higher rates of molecular sequence evolution compared with Pezizomycotina. These results provide a robust evolutionary framework for understanding the diversity and ecological lifestyles of the largest fungal phylum.

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“…In recent years, the 1000 Fungal Genomes Project (https://mycocosm.jgi.doe.gov/programs/fungi/1000fungalgenomes.jsf) has greatly expanded the availability of genomes from diverse understudied taxa across the fungal tree of life 25 . Additionally, efforts focused on specific ecological or evolutionary groups, such as the Y1000+ Project (http://y1000plus.org) that aims to sequence all known species of the subphylum Saccharomycotina 26 , the Dothideomycetes project that aims to study plant pathogenic fungi 27 , and the Aspergillus genome project that aims to examine the metabolic dexterity of this diverse genus of fungi 28 (https://jgi.doe.gov/aspergillus-all-in-thefamily-focused-genomic-comparisons), have greatly increased the availability of genomes from specific lineages.…”

Section: Introductionmentioning

confidence: 99%

A genome-scale phylogeny of Fungi; insights into early evolution, radiations, and the relationship between taxonomy and phylogeny

Steenwyk

Chang

et al. 2020

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Phylogenomic studies based on genome-scale amounts of data have greatly improved understanding of the tree of life. Despite their diversity, ecological significance, and biomedical and industrial importance, large-scale phylogenomic studies of Fungi are lacking. Furthermore, several evolutionary relationships among major fungal lineages remain controversial, especially those at the base of the fungal phylogeny. To begin filling these gaps and assess progress toward a genome-scale phylogeny of the entire fungal kingdom, we compiled a phylogenomic data matrix of 290 genes from the genomes of 1,644 fungal species that includes representatives from most major fungal lineages; we also compiled 11 additional data matrices by subsampling genes or taxa based on filtering criteria previously shown to improve phylogenomic inference. Analyses of these 12 data matrices using concatenation- and coalescent-based approaches yielded a robust phylogeny of the kingdom in which ∼85% of internal branches were congruent across data matrices and approaches used. We found support for several relationships that have been historically contentious (e.g., for the placement of Wallemiomycotina (Basidiomycota), as sister to Agaricomycotina), as well as evidence for polytomies likely stemming from episodes of ancient diversification (e.g., at the base of Basidiomycota). By examining the relative evolutionary divergence of taxonomic groups of equivalent rank, we found that fungal taxonomy is broadly aligned with genome sequence divergence, but also identified lineages, such as the subphylum Saccharomycotina, where current taxonomic circumscription does not fully account for their high levels of evolutionary divergence. Our results provide a robust phylogenomic framework to explore the tempo and mode of fungal evolution and directions for future fungal phylogenetic and taxonomic studies.

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101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens

Cited by 149 publications

References 51 publications

Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding?

Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding?

Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota

A genome-scale phylogeny of Fungi; insights into early evolution, radiations, and the relationship between taxonomy and phylogeny

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