Lifestyle Transitions in Fusarioid Fungi are Frequent and Lack Clear Genomic Signatures

Abstract

The fungal genus Fusarium (Ascomycota) includes well-known plant pathogens that are implicated in diseases worldwide, and many of which have been genome sequenced. The genus also encompasses other diverse lifestyles, including species found ubiquitously as asymptomatic-plant inhabitants (endophytes). Here, we produced structurally annotated genome assemblies for five endophytic Fusarium strains, including the first whole-genome data for Fusarium chuoi. Phylogenomic reconstruction of Fusarium and closely related genera revealed multiple and frequent lifestyle transitions, the major exception being a monophyletic clade of mutualist insect symbionts. Differential codon usage bias and increased codon optimisation separated Fusarium sensu stricto from allied genera. We performed computational prediction of candidate secreted effector proteins (CSEPs) and carbohydrate-active enzymes (CAZymes)—both likely to be involved in the host–fungal interaction—and sought evidence that their frequencies could predict lifestyle. However, phylogenetic distance described gene variance better than lifestyle did. There was no significant difference in CSEP, CAZyme, or gene repertoires between phytopathogenic and endophytic strains, although we did find some evidence that gene copy number variation may be contributing to pathogenicity. Large numbers of accessory CSEPs (i.e., present in more than one taxon but not all) and a comparatively low number of strain-specific CSEPs suggested there is a limited specialisation among plant associated Fusarium species. We also found half of the core genes to be under positive selection and identified specific CSEPs and CAZymes predicted to be positively selected on certain lineages. Our results depict fusarioid fungi as prolific generalists and highlight the difficulty in predicting pathogenic potential in the group.

Fusariumand Allied Fusarioid Taxa (FUSA). 1

“…Additionally, arguments for recognising distinct genera in the terminal fusarioid clade of the Nectriaceae were presented by Crous et al . (2021b) and Hill et al . (2022) .…”

Tapping Culture Collections for Fungal Endophytes: First Genome Assemblies for Three Genera and Five Species in theAscomycota

“…For strains which only had short-read data, the assembly pipeline from Hill et al (2022) was used, comparing ABySS v2.0.2 ( Simpson 2009 ), MEGAHIT v1.2.9 ( Li 2016 ) and SPAdes v3.11.1 ( Bankevich 2012 ). If we were also able to obtain long-read sequence data for strains, hybrid assembly was performed with comparison across three tools: Flye v2.6 ( Kolmogorov et al 2019 ), Raven v1.6.1 ( Vaser and Šikić 2021 ), and hybridSPAdes v3.11.1 ( Antipov et al 2016 ).…”

“…Factors controlling whether a fungus exhibits endophytism versus pathogenicity are not well defined. Case-study comparisons between closely related pathogens and endophytes have started to reveal lineage-specific patterns or mechanisms that may contribute to lifestyle ( Hacquard 2016 ; Niehaus 2016 ; Stauber et al 2020 ; Hill et al 2022 ), however we have no indication of whether they will hold true for all ascomycete endophytes, which are spread across the entire phylum ( Huang 2018 ; U’Ren 2019 ). If we are to better understand endophytism, and therefore improve the chance of predicting the pathogenic potential of fungal strains, comparisons across a broader taxonomic scale are needed.…”

Intraspecific Comparative Analysis Reveals Genomic Variation of Didymella arachidicola and Pathogenicity Factors Potentially Related to Lesion Phenotype

“…Notably, hemibiotrophic fungi have a narrow host range and can establish an initial biotrophic phase, then switch to a necrotrophic phase [ 12 , 14 , 15 ]. The shift of fungi lifestyles has been revealed to include switching between the same fungal species with different lifestyles isolated from different host plants [ 16 ] or different host cultivars [ 17 , 18 ] and between different fungal species of the same genus isolated from different host plants [ 19 , 20 ]. We have previously found two different leaf lesion phenotypes of PWB in China: reticulation type (R type) and blotch type (B type) (Unpublished work).…”

“…Different lifestyles of fungi are highly connected to their secretome (secreted effectors, carbohydrate-active enzymes, transporters, etc. ), which are secreted from penetration to tissue destruction [ 19 , 20 , 21 ]. Comparing variations in the secretome will facilitate our understanding of how fungi interact with their hosts.…”