Maintenance of Sex-Related Genes and the Co-Occurrence of Both Mating Types in Verticillium dahliae

Abstract

Verticillium dahliae is a cosmopolitan, soilborne fungus that causes a significant wilt disease on a wide variety of plant hosts including economically important crops, ornamentals, and timber species. Clonal expansion through asexual reproduction plays a vital role in recurring plant epidemics caused by this pathogen. The recent discovery of recombination between clonal lineages and preliminary investigations of the meiotic gene inventory of V. dahliae suggest that cryptic sex appears to be rare in this species. Here we expanded on previous findings on the sexual nature of V. dahliae. Only 1% of isolates in a global collection of 1120 phytopathogenic V. dahliae isolates contained the MAT1-1 idiomorph, whereas 99% contained MAT1-2. Nine unique multilocus microsatellite types comprised isolates of both mating types, eight of which were collected from the same substrate at the same time. Orthologs of 88 previously characterized sex-related genes from fungal model systems in the Ascoymycota were identified in the genome of V. dahliae, out of 93 genes investigated. Results of RT-PCR experiments using both mating types revealed that 10 arbitrarily chosen sex-related genes, including MAT1-1-1 and MAT1-2-1, were constitutively expressed in V. dahliae cultures grown under laboratory conditions. Ratios of non-synonymous (amino-acid altering) to synonymous (silent) substitutions in V. dahliae MAT1-1-1 and MAT1-2-1 sequences were indistinguishable from the ratios observed in the MAT genes of sexual fungi in the Pezizomycotina. Patterns consistent with strong purifying selection were also observed in 18 other arbitrarily chosen V. dahliae sex-related genes, relative to the patterns in orthologs from fungi with known sexual stages. This study builds upon recent findings from other laboratories and mounts further evidence for an ancestral or cryptic sexual stage in V. dahliae.

A distinct and genetically diverse lineage of the hybrid fungal pathogen Verticillium longisporum population causes stem striping in British oilseed rape

“…longisporum is an interspecific hybrid between two separate Verticillium species (Inderbitzin et al, 2011b;Depotter et al, 2016a). Interspecific hybrids are regularly found to be impaired in their sexual reproduction (Greig, 2009;Bertier et al, 2013), although this should be of little significance for V. longisporum as a sexual stage has not been described for any of the Verticillium species (Short et al, 2014). However, mating types, meiosis-specific genes and genomic recombination between clonal lineages have been observed for V. dahliae (Milgroom et al, 2014;Short et al, 2014).…”

“…The repetitive character of these regions makes them more prone to mutation than non‐repetitive sequences due to unequal crossing‐over and replication slippage, generally revealing high degrees of polymorphism (Levinson and Gutman, ). Several population studies previously used SSR loci to describe diversity within Verticillium populations (Atallah et al ., ; Short et al ., ). However, hitherto, no population studies have been performed on V. longisporum .…”

Dynamic virulence‐related regions of the plant pathogenic fungus Verticillium dahliae display enhanced sequence conservation

“…Currently, 10 Verticillium species are described, which are divided in two phylogenetic clusters, i.e., clade Flavexudans and clade Flavnonexudans (Inderbitzin et al, ). Verticillium species are thought to have a predominant, if not exclusive, asexual reproduction as a sexual cycle has never been described for any of the species (Short, Gurung, Hu, Inderbitzin, & Subbarao, ). Nevertheless, Verticillium dahliae still appears to have the machinery for sexual recombination, as mating types and meiosis‐specific genes occur (Short et al, ).…”

“…Nevertheless, Verticillium dahliae still appears to have the machinery for sexual recombination, as mating types and meiosis‐specific genes occur (Short et al, ). However, a severely skewed mating type ratio in the global V. dahliae population (99% vs. 1%; Short et al, ) combined with the low mobility of V. dahliae due to its soil‐borne nature makes sexual recombination only a marginal phenomenon at most. In V. dahliae , the most notorious plant pathogen within the genus that infects hundreds of plant species (Inderbitzin & Subbarao, ), mechanisms different from meiotic recombination were shown to contribute to the genomic diversity, including large‐scale genomic rearrangements, horizontal gene transfer, and transposable element (TE) activity (Faino et al, ; de Jonge et al, , ; Seidl & Thomma, ; Shi‐Kunne, van Kooten, Depotter, Thomma, & Seidl, ).…”

Verticillium longisporum, the invisible threat to oilseed rape and other brassicaceous plant hosts

“…Verticillium albo-atrum, V. alfalfae, V. non-alfalfae and V. longisporum are also vascular pathogens, albeit with a more restricted host range. Members of the genus reproduce asexually and a sexual stage has not yet been described for any Verticillium species (Short et al, 2014).…”