Lineage structure of the Fusarium oxysporum Species Complex (FOSC) based on a dataset of 41 full-length genes from the core genomes of 545 isolates: its implications in taxonomy and diagnostics

Authors: GEISER, DAVID - Pennsylvania State University; JIMENEZ-GASCO, MARIA - Pennsylvania State University; KANG, SEOGCHAN - Pennsylvania State University; LI, NINGXIAO - University Of California; Martin, Frank; O Donnell, Kerry

Submitted to: Mycological Society of America
Publication Type: Abstract Only
Publication Acceptance Date: 4/22/2022
Publication Date: N/A
Citation: N/A

Interpretive Summary:

Technical Abstract: The Fusarium oxysporum Species Complex (FOSC; Nectriaceae, Hypocreales), encompassing F. oxysporum sensu lato and F. foetens, represents one of the most important groups of fungal plant pathogens, causing economically devastating vascular wilt and other diseases on over 100 economically important hosts. In addition, some isolates can be endophytic, exist as saprobes, or cause serious infections in humans and other animals. Despite its importance, F. oxysporum has remained taxonomically unsettled, and the non-monophyletic nature of many of its 100+ described formae speciales and lack of appropriate genomic markers have confounded diagnostics. We identified 41 putatively orthologous protein-coding genes that map to core genome regions and extracted their full-length DNA sequences from genome assemblies of 545 diverse F. oxysporum isolates generated in this study or previously by other groups. Sequences were aligned with F. commune and F. foetens as outgroups, which produced an alignment totaling 69,180 sites and 323 unique clone-corrected ingroup taxa. Data were subjected to partitioned maximum likelihood phylogenetic analyses using the IQ-TREE software package. The resulting phylogenetic structure resolved nodes with strong (>99%) ultrafast bootstrap support that correspond to 16 lineages, mostly identified in previously published work. F. foetens resolved among ingroup lineages in most of the individual gene trees, leading us to treat it as a distinct ingroup lineage. Despite high bootstrap values, most FOSC lineages were resolved in only a minority of individual gene trees, consistent with high levels of incomplete lineage sorting and recent common ancestry for the group. The greatest pairwise distance (uncorrected-p) between the 17 lineages was 0.0152 nucleotide substitutions per site. A splits-tree network of the concatenated dataset suggests that FOSC lineages and F. foetens emerged from a highly reticulated ancestral assemblage. Some lineages corresponded well with formally described species within FOSC based on 3-4 genes, but others were not supported by the larger dataset. Informative patterns of diversity within formae speciales and endophytic isolates from the same host indicate the utility of a phylogenomic perspective in reconstructing the evolution of these pathogens and developing novel diagnostic tools. The novel dataset presented in this study provides a framework for using complete core and accessory genome assemblies to characterize FOSC isolates at a fine level, and it is adaptable to an amplicon-based approach to study populations. Based on the observed low levels of sequence divergence and high levels of incomplete lineage sorting, as well as the natural history of F. oxysporum, we argue that genetic structure within this group is best interpreted as a pattern of divergent lineages within a single species.