Number of Candidate Effector Genes in Accessory Genomes Differentiates Pathogenic From Endophytic Fusarium oxysporum Strains

Abstract

The fungus Fusarium oxysporum (Fo) is widely known for causing wilt disease in over 100 different plant species. Endophytic interactions of Fo with plants are much more common, and strains pathogenic on one plant species can even be beneficial endophytes on another species. However, endophytic and beneficial interactions have been much less investigated at the molecular level, and the genetic basis that underlies endophytic versus pathogenic behavior is unknown. To investigate this, 44 Fo strains from non-cultivated Australian soils, grass roots from Spain, and tomato stems from United States were characterized genotypically by whole genome sequencing, and phenotypically by examining their ability to symptomlessly colonize tomato plants and to confer resistance against Fusarium Wilt. Comparison of the genomes of the validated endophytic Fo strains with those of 102 pathogenic strains revealed that both groups have similar genomes sizes, with similar amount of accessory DNA. However, although endophytic strains can harbor homologs of known effector genes, they have typically fewer effector gene candidates and associated non-autonomous transposons (mimps) than pathogenic strains. A pathogenic ‘lifestyle’ is associated with extended effector gene catalogs and a set of “host specific” effectors. No candidate effector genes unique to endophytic strains isolated from the same plant species were found, implying little or no host-specific adaptation. As plant-beneficial interactions were observed to be common for the tested Fo isolates, the propensity for endophytism and the ability to confer biocontrol appears to be a predominant feature of this organism. These findings allow prediction of the lifestyle of a Fo strain based on its genome sequence as a potential pathogen or as a harmless or even beneficial endophyte by determining its effectorome and mimp number.

Fusarium oxysporum effector clustering version 2: An updated pipeline to infer host range

“…oxysporum isolates fall inside main clade 2; 127 isolates belong to clade 3 and only 27 to clade 1. Two isolates do not clearly fall within one of the three clades in this tree; Fo65 (GCA_014324465.1) falls outside clade 1 and Fo24 (GCA_014337855.1) is positioned between clades 1 and 2/3, in line with the findings by (Constantin et al. 2021) .…”

“…When using this pipeline, F. oxysporum strains that belong to the same forma specialis are typically grouped together, solidifying the hypothesis that the effector repertoire of a F. oxysporum genome plays a role in determining the host range of a strain. FoEC has been used to classify uncharacterized F. oxysporum strains into potential formae speciales based on presence/absence patterns of putative effector genes ( Urbaniak et al., 2019 ; Constantin et al., 2021 ; Sabahi et al., 2021 ), considerably narrowing down the number of hosts to test in experimental procedures.…”

Fusarium oxysporum Effector Clustering version 2 (FoEC2): an updated pipeline to infer host range

“…The majority (381) of the 537 F. oxysporum isolates fall inside main clade 2; 127 isolates belong to clade 3 and only 27 to clade 1. Two isolates do not clearly fall within one of the three clades in this tree; Fo65 (GCA_014324465.1) falls outside clade 1 and Fo24 (GCA_014337855.1) is positioned between clades 1 and 2/3, in line with the findings by Constantin et al (2021). Many formae speciales clustering together in Figure 2 are polyphyletic, i.e., they occur in distinct clades within the core phylogeny.…”

Fungal Effectoromics: A World in Constant Evolution

“…Pathogenic interactions between plants and microorganisms such as Cladosporium fulvum -tomato [ 234 , 235 ]; Phytophthora infestans -potato [ 236 , 237 ], the Pseudomonas syringae species complex with various hosts [ 238 , 239 ], are prime examples of well-studied pathosystems utilized for fungi, oomycetes, bacteria, respectively, and are also the leading pathosystems in effector biology studies. A budding area of interest centers on effectors beyond the plant-pathogen interaction, with discoveries in non-pathogenic organisms such as mutualist mycorrhizal species [ 13 , 186 , 240 ] and endophytes [ 16 , 241 , 242 ] in interaction with the plant host. These organisms also modulate host immunity with the help of effectors to establish plant-beneficial interactions.…”