Population genomics reveals historical and ongoing recombination in the Fusarium oxysporum species complex

Abstract

The Fusarium oxysporum species complex (FOSC) is a group of closely related plant pathogens long-considered strictly clonal, as sexual stages have never been recorded. Several studies have questioned whether recombination occurs in FOSC, and if it occurs its nature and frequency are unknown. We analysed 410 assembled genomes to answer whether FOSC diversified by occasional sexual reproduction interspersed with numerous cycles of asexual reproduction akin to a model of predominant clonal evolution (PCE). We tested the hypothesis that sexual reproduction occurred in the evolutionary history of FOSC by examining the distribution of idiomorphs at the mating locus, phylogenetic conflict and independent measures of recombination from genome-wide SNPs and genes. A phylogenomic dataset of 40 single copy orthologs was used to define structure a priori within FOSC based on genealogical concordance. Recombination within FOSC was tested using the pairwise homoplasy index and divergence ages were estimated by molecular dating. We called SNPs from assembled genomes using a k-mer approach and tested for significant linkage disequilibrium as an indication of PCE. We clone-corrected and tested whether SNPs were randomly associated as an indication of recombination. Our analyses provide evidence for sexual or parasexual reproduction within, but not between, clades of FOSC that diversified from a most recent common ancestor about 500 000 years ago. There was no evidence of substructure based on geography or host that might indicate how clades diversified. Competing evolutionary hypotheses for FOSC are discussed in the context of our results.

Diagnostics of Fusarium wilt in banana: Current status and challenges

“…There is also evidence to suggest that horizontal gene transfer and co-evolution played important roles in the pathogen's evolutionary history (Czislowski et al, 2018). Phylogenetic analyses based on whole genomes of Foc confirmed its polyphyletic origin and different molecular genotypes constituting the same race (McTaggart et al, 2021;. This paved the way for the proposal of various new species of Foc, prompted by the high genetic diversity of Foc lineages in its centre of origin, Indonesia, including the reclassification of TR4, which belongs to a single VCG (01213/16), into the new species F. odoratissimum (Maryani et al, 2019).…”

“…Research using approaches that consider whole genomes have brought greater insight into the evolution and genetic relationships within the F. oxysporum disease complex and Foc (Achari et al., 2020; Czislowski et al., 2018; McTaggart et al., 2021; Ordóñez et al., 2019; Raman et al., 2021). Phylogenetic analyses have demonstrated that the ability of Foc to cause disease has arisen independently multiple times, and that its pathogenicity towards specific banana cultivars is a polyphyletic trait (Fourie et al., 2009).…”

Molecular and Pathogenic Characterization of Fusarium Species Associated with Corm Rot Disease in Saffron from China

“…By applying a polyphasic taxonomic approach that combines morphological observations with DNA fingerprinting, and multilocus phylogenetic analysis (MLSA), numerous species have been delineated within Fusarium spp. complexes, leading to significant improvement in the Fusarium classification system [ 11 , 12 , 13 , 19 , 21 , 22 ].…”

Population genomics reveals meiotic recombination in Fusarium oxysporum

“…This could result in predominantly clonal evolution, even when the capability of sexual recombination is maintained ( 12 ). However, if F. oxysporum as a species would be generally asexual, one would, due to genetic drift, expect a skewed distribution toward one of the mating loci, while in fact several studies, including the one by Fayyaz et al, report more or less equal frequencies of the two mating type loci ( 7 , 13 , 14 ). No sexual structures have been observed for F. oxysporum although Fourie et al report protoperithecium-like structures that were formed after coincubating banana-infecting strains with different mating type loci ( 13 ).…”

“…Recently, McTaggart et al queried a global collection of 410 complete genomes of F. oxysporum with different host preferences for a variety of signatures of recombination. They concluded that sexual or parasexual reproduction has frequently taken place within phylogenetic species, but that most current lineages appear to evolve clonally ( 14 ). However, the authors also note that recombination was easier to detect in well-sampled clades.…”