Investigation of the diversity of effector genes in the banana pathogen, Fusarium oxysporum f. sp. cubense, reveals evidence of horizontal gene transfer

Abstract

It is hypothesized that the virulence of phytopathogenic fungi is mediated through the secretion of small effector proteins that interfere with the defence responses of the host plant. In Fusarium oxysporum, one family of effectors, the Secreted In Xylem (SIX) genes, has been identified. We sought to characterize the diversity and evolution of the SIX genes in the banana-infecting lineages of F. oxysporum f. sp. cubense (Foc). Whole-genome sequencing data were generated for the 23 genetic lineages of Foc, which were subsequently queried for the 14 known SIX genes (SIX1-SIX14). The sequences of the identified SIX genes were confirmed in a larger collection of Foc isolates. Genealogies were generated for each of the SIX genes identified in Foc to further investigate the evolution of the SIX genes in Foc. Within Foc, variation of the SIX gene profile, including the presence of specific SIX homologues, correlated with the pathogenic race structure of Foc. Furthermore, the topologies of the SIX gene trees were discordant with the topology of an infraspecies phylogeny inferred from EF-1α/RPB1/RPB2 (translation elongation factor-1α/RNA polymerase II subunit I/RNA polymerase II subunit II). A series of topological constraint models provided strong evidence for the horizontal transmission of SIX genes in Foc. The horizontal inheritance of pathogenicity genes in Foc counters previous assumptions that convergent evolution has driven the polyphyletic phylogeny of Foc. This work has significant implications for the management of Foc, including the improvement of diagnostics and breeding programmes.

Evidence for horizontal gene transfer and separation of effector recognition from effector function revealed by analysis of effector genes shared between cape gooseberry‐ and tomato‐infecting formae speciales of Fusarium oxysporum

“…spp. lilii and cubense (Czislowski et al., ; van Dam et al., ) suggests that SIX7 may be separable, both physically and functionally, from SIX10 and SIX12 . Moreover, SIX10 and SIX12 are not arranged in divergent orientation, and so cannot be transcribed coordinately from a shared promoter, as is the case for SIX3 and SIX5.…”

The multi-speed genome ofFusarium oxysporumreveals association of histone modifications with sequence divergence and footprints of past horizontal chromosome transfer events

“…Interestingly, host-preference in FOSC is often polyphyletic [44-56]. Several studies revealed putative horizontal transfer events of effector genes between FOSC strains that infect the same host [40,57-59], indicating that horizontal transfer may play an important role in host switches [39,40,56,60,61]. Of the four accessory chromosomes in Fol4287, chromosome 14 is undoubtedly a pathogenicity chromosome: all fourteen SIX (Secreted In Xylem) genes – known effector genes in tomato-infecting Fusarium oxysporum – are located on chromosome 14 [62] (and our unpublished observations).…”

Comparison of Secreted in Xylem (SIX) genes in two fusarium wilt pathogens of ornamental palms

“…lycopersici , which has two sequence variants of SIX8 (Schmidt et al , ), and f. sp. cubense , which has four sequence variants of SIX8 and three variants of SIX9 (Fraser‐Smith et al , ; Czislowski et al , ).…”

“…Ma et al (2010) then demonstrated the LS regions of Fol could be horizontally transferred to a nonpathogenic strain, transforming it into a pathogen. Multiple studies have since hypothesized that the SIX genes have been horizontally transferred between formae speciales of F. oxysporum (Fraser-Smith et al, 2014;Laurence et al, 2015;Taylor et al, 2016;van Dam et al, 2017;Czislowski et al, 2018).…”