The Ascomycete Verticillium longisporum Is a Hybrid and a Plant Pathogen with an Expanded Host Range

Abstract

Hybridization plays a central role in plant evolution, but its overall importance in fungi is unknown. New plant pathogens are thought to arise by hybridization between formerly separated fungal species. Evolution of hybrid plant pathogens from non-pathogenic ancestors in the fungal-like protist Phytophthora has been demonstrated, but in fungi, the most important group of plant pathogens, there are few well-characterized examples of hybrids. We focused our attention on the hybrid and plant pathogen Verticillium longisporum, the causal agent of the Verticillium wilt disease in crucifer crops. In order to address questions related to the evolutionary origin of V. longisporum, we used phylogenetic analyses of seven nuclear loci and a dataset of 203 isolates of V. longisporum, V. dahliae and related species. We confirmed that V. longisporum was diploid, and originated three different times, involving four different lineages and three different parental species. All hybrids shared a common parent, species A1, that hybridized respectively with species D1, V. dahliae lineage D2 and V. dahliae lineage D3, to give rise to three different lineages of V. longisporum. Species A1 and species D1 constituted as yet unknown taxa. Verticillium longisporum likely originated recently, as each V. longisporum lineage was genetically homogenous, and comprised species A1 alleles that were identical across lineages.

Verticillium Infection Triggers VASCULAR-RELATED NAC DOMAIN7–Dependent de Novo Xylem Formation and Enhances Drought Tolerance in Arabidopsis

“…First, we confirmed by comparative sequence analysis of the ribosomal internal transcribed spacer region (Inderbitzin et al, 2011) that the Verticillium isolate used in our studies (VL43; first described in Zeise and von Tiedemann, 2001) belongs to the species V. longisporum (see Supplemental Table 1 and Supplemental Figure 1 online). Next, we analyzed in detail V. longisporum-induced symptom development on Arabidopsis by inoculating ecotype Columbia (Col-0) seedlings using the root-dipping method described below.…”

“…Of the five plant pathogenic Verticillium species V. dahliae, V. albo-atrum, V. tricorpus, V. nubilum, and V. longisporum (Klosterman et al, 2009a(Klosterman et al, , 2009bInderbitzin et al, 2011), the latter specifically infects cruciferous plants, including the economically important host plant Brassica napus and the model plant Arabidopsis thaliana (Zeise and von Tiedemann, 2002). Originally considered a long-spored variant of V. dahliae, the near-diploid species V. longisporum was recently suggested to represent the result of a parasexual hybridization between V. dahliae and V. albo-atrum and was classified as a species (Karapapa et al, 1997).…”

“…Originally considered a long-spored variant of V. dahliae, the near-diploid species V. longisporum was recently suggested to represent the result of a parasexual hybridization between V. dahliae and V. albo-atrum and was classified as a species (Karapapa et al, 1997). Despite controversial views on this matter, several recent molecular studies support the taxonomic status of V. longisporum as a new Verticillium species and the importance of hybrid formation within this genus of phytopathogenic fungi (Klosterman et al, 2009a(Klosterman et al, , 2009bCollado-Romero et al, 2010;Inderbitzin et al, 2011).…”

The interspecific fungal hybrid Verticillium longisporum displays sub-genome-specific gene expression

“…As 414 species A1 and D1 are hitherto unfound in their haploid state, V. dahliae was used for 415 expression pattern comparison as it only recently diverged from species D1 and therefore 416 likely resembles D1 gene expression [37]. Unfortunately, species A1 currently lacks a known 417 sister species that could be used in the gene expression comparison (Fig 3A).…”

Cylindrocladiella hahajimaensis, a new species of Cylindrocladiella transferred from Verticillium

“…During recent studies of Verticillium evolution and taxonomy (Inderbitzin et al 2011a;Inderbitzin et al 2011b), we received the ex-holotype culture of 'V. hahajimaense' isolated from soil in Japan using cucumber seeds as bait (Watanabe et al 2001).…”