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.
Highlights
Increased globalization and world trade have resulted in a rise in the number of novel pathosystems, that is, plant diseases caused by new plant pathogens × host species combinations (Depotter, Seidl, Wood, & Thomma, 2016; Stukenbrock, 2016a, 2016b)
A crucial role in the generation of novel plant pathogens has been ascribed to hybridization between species, a process in which the combination of two or more genomes in a single organ‐ ism can lead to rapid adaptive evolution (Brasier, 2000; Depotter et al, 2016; McDonald & Stukenbrock, 2016; Olson & Stenlid, 2002; Schardl & Craven, 2003; Stukenbrock, 2016a, 2016b)
Hybridization followed by reproductive isolation has been reported to contribute to rapid speciation in yeast (Leducq et al, 2016), and the same has been hypothesized to occur in some filamentous fungi (Gladieux et al, 2014; Kohn, 2005) and in fungus‐like oomycetes (Schardl & Craven, 2003)
Summary
Increased globalization and world trade have resulted in a rise in the number of novel pathosystems, that is, plant diseases caused by new plant pathogens × host species combinations (Depotter, Seidl, Wood, & Thomma, 2016; Stukenbrock, 2016a, 2016b). Trees obtained from heterozygotic gpd and RPB2 sequences, which harbored ambiguous bases, showed heterokaryotic isolates as being placed in an intermediate position in between reference sequences from the putative parental species H. irregulare and H. occidentale (Figures S5 and S6). When ambiguity in alleles was resolved by manual assignment of bases based on parental allele frequencies, the alignment of sequences showed that each heterokaryotic isolate possessed two distinct types of gpd and RPB2 alleles, one clearly related to H. irregulare and one clearly related to H. occidentale (Figures S2 and S3). Topology of the tree based on ITS cloned sequences was similar to that obtained with EF‐1α sequences, with a statistically well‐sup‐ ported H. irregulare‐like cluster distinct from H. irregulare including one allele from each heterokaryotic isolate (Figure S8). Parental contributions to the allelic makeup of H. irregulare‐like alleles, expressed as inheritance probabilities, were 62.56% and 37.44% for the H. irregulare and the H. occidentale clus‐ ter, respectively
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