Molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybrids

Abstract

Hybridization may be a major driver in the evolution of plant pathogens. In a high elevation Alpine larch stand in Montana, a novel hybrid fungal pathogen of trees originating from the mating of Heterobasidion irregulare with H. occidentale has been recently discovered. In this study, sequence analyses of one mitochondrial and four nuclear loci from 11 Heterobasidion genotypes collected in the same Alpine larch stand indicated that hybridization has increased allelic diversity by generating novel polymorphisms unreported in either parental species. Sequence data and ploidy analysis through flow cytometry confirmed that heterokaryotic (n + n) genotypes were not first‐generation hybrids, but were the result of multiple backcrosses, indicating hybrids are fertile. Additionally, all admixed genotypes possessed the H. occidentale mitochondrion, indicating that the hybrid progeny may have been backcrossing mostly with H. occidentale. Based on reticulate phylogenetic network analysis by PhyloNet, Bayesian assignment, and ordination tests, alleles can be defined as H. irregulare‐like or H. occidentale‐like. H. irregulare‐like alleles are clearly distinct from all known H. irregulare alleles and are derived from the admixing of both Heterobasidion species. Instead, all but one H. occidentale alleles found in hybrids, although novel, were not clearly distinct from alleles found in the parental H. occidentale population. This discovery demonstrates that Alpine larch can be a universal host favouring the interspecific hybridization between H. irregulare and H. occidentale and the hybridization‐mediated evolution of a nucleus, derived from H. irregulare parental species but clearly distinct from it.

Heterothallism and potential hybridization events inferred for twenty-two yellow morel species

“…Hybridization is now widely recognized to be an important evolutionary process which might play a crucial role in speciation (Gross and Rieseberg 2005;Mallet 2007;Schumer et al 2014;Taylor and Larson 2019). Hybridization followed by reproductive isolation has been reported to contribute to rapid speciation of yeast (Leducq et al 2016) and the same has been supposed to occur in some filamentous fungi (Kohn 2005;Gladieux et al 2014;Sillo et al 2019). Du et al (2012) reported the 85.2% of the species in the Esculenta Clade (including almost 90% of the Chinese species lineages) diversified and went through rapid speciation in East Asia since the middle Miocene, which might have contributed to the potential hybridization and gene transfer events detected in the Esculenta Clade.…”

Multiplex real‐time PCR assays for the detection and identification of Heterobasidion species attacking conifers in Europe

“…These results, and the weak cross‐reaction observed for H. occidentale DNA with the H. parviporum test, reflect the close phylogenetic relationship between these species that diverged quite recently (Chen et al , ). Future studies should therefore clarify the frequency of hybridization among Heterobasidion species and shed some light on their viability in natural populations, with the help of other nuclear markers, such as the ones used for recently described H. occidentale × H. irregulare hybrids (Sillo et al , ). However, the observation of double positive signals following the H. abietinum and H. parviporum real‐time PCR assays with some DNA from some of the H. parviporum pure cultures suggests caution, and it is recommended that all four species‐specific assays are run for the analysis of environmental samples.…”

“…However, their ecology and geographic distribution overlap to a large extent (Garbelotto & Gonthier, ) and they can co‐occur in the same stands (Gonthier et al , ; Sedlák & Tomšovský, ; Gonthier, ). In addition, several studies have shown incomplete species barriers between some species, with rare hybrids being found in forests (Garbelotto et al , ; Gonthier & Garbelotto, ; Sedlák & Tomšovský, ; Sillo et al , ).…”

Genic introgression from an invasive exotic fungal forest pathogen increases the establishment potential of a sibling native pathogen

“…Stukenbrock (2016) suggested that studies integrating genomic and experimental data are pivotal to understand the evolution of fungal hybrids in nature. Whereas fungal hybrid genotypes can be generated and studied in vitro (Olson and Stenlid 2001;Giordano et al 2018), hybrids resulting from natural selection are difficult to find in nature, given that only a few cases of ongoing hybridization are known (Garbelotto et al 1996;Gonthier and Garbelotto 2011;Hughes et al 2013;Pryszcz et al 2014;Menardo et al 2016;Sillo et al 2019).…”