Partial pathogenicity chromosomes in Fusarium oxysporum are sufficient to cause disease and can be horizontally transferred

Abstract

In Fusarium oxysporum f.sp. lycopersici, all effector genes reported so faralso called SIX genesare located on a single accessory chromosome which is required for pathogenicity and can also be horizontally transferred to another strain. To narrow down the minimal region required for virulence, we selected partial pathogenicity chromosome deletion strains by fluorescence-assisted cell sorting of a strain in which the two arms of the pathogenicity chromosome were labelled with GFP and RFP respectively. By testing the virulence of these deletion mutants, we show that the complete long arm and part of the short arm of the pathogenicity chromosome are not required for virulence. In addition, we demonstrate that smaller versions of the pathogenicity chromosome can also be transferred to a non-pathogenic strain and they are sufficient to turn the non-pathogen into a pathogen. Surprisingly, originally non-pathogenic strains that had received a smaller version of the pathogenicity chromosome were much more aggressive than recipients with a complete pathogenicity chromosome. Whole genome sequencing analysis revealed that partial deletions of the pathogenicity chromosome occurred mainly close to repeats, and that spontaneous duplication of sequences in accessory regions is frequent both in chromosome deletion strains and in horizontal transfer strains.

Accessory Chromosome-Acquired Secondary Metabolism in Plant Pathogenic Fungi: The Evolution of Biotrophs Into Host-Specific Pathogens

“…Among some pathogenic fungi, the concept of an AC is nuanced by the presence of virulence factor genes involved in pathogenicity and/or secondary metabolite production, which play an important role in niche plant invasion and adaptation (Croll and McDonald, 2012). ACs conferring adaptive advantages such as pathogenicity are sometimes described as "conditionally dispensable" chromosomes (popularized by studies of Alternaria species; Tsuge, 2019) or "pathogenicity" chromosomes (Ma et al, 2010;van Dam et al, 2017;Li et al, 2020). ACs are of particular interest in fungal pathogen research due to their capacity for horizontal transfer between strains, which has been experimentally demonstrated to increase pathogen competence in previously deficient strains (He et al, 1998;Akagi et al, 2009;Ma et al, 2010;Shahi et al, 2016;van Dam et al, 2017;Li et al, 2020).…”

“…Compared to core chromosomes, genomic content of ACs are relatively dynamic (Vlaardingerbroek et al, 2016b;Habig et al, 2017;Möller et al, 2018;Plaumann et al, 2018). ACs can change in size during horizontal chromosome transfer, as higher concentrations of repetitive elements in ACs lead to intra-or interchromosome homologous recombination, resulting in deletions, translocations (Hedges and Deininger, 2007) and multiplication of gene loci (Li et al, 2020). Although exact mechanisms for horizontal chromosome transfer have yet to be fully elucidated, current hypotheses involve AC transfer events through heterokaryosis during hyphal anastomosis (Bertazzoni et al, 2018).…”

Tomato (Solanum lycopersicum L.) and Fusarium oxysporum f. sp. lycopersici interaction. A review

“…Likewise, the fungus is subdivided into races according to its ability to infect cultivars with different levels of resistance, a fact that is associated with mutations in avirulence genes and horizontal gene transfer (Sutherland et al 2013). Additionally, the evolution of the pathogenicity has been acquired through the horizontal chromosome transfer of nonpathogenic strains (Li et al 2020a;Inami et al 2014). Genetically, the physiological races are determined by the possession of different combinations of SIX proteins (Secreted In Xylem).…”

A Genomic Blueprint of Flax Fungal Parasite Fusarium oxysporum f. sp. lini

“…These observations regarding genome architecture gave momentum to the concept of a “two-speed genome”, as a driver of adaptive evolution [ 5 , 6 , 7 ]. A horizontal transfer of lineage-specific chromosomes between strains, both pathogenic and non-pathogenic, is feasible and may prove instrumental in host switches, as evidentiated by experiments with pathogens infecting tomatoes and cucurbits [ 2 , 8 , 9 , 10 ]. Furthermore, the two-speed model finds an indirect support in polyphyletic host preference of FOSC strains [ 4 ] and in grouping of pathogenic strains with non-pathogenic strains in population genomics studies [ 11 , 12 , 13 ].…”