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, seque...

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Main Authors: Fabiano Sillo, Paolo Gonthier, Blakey Lockman, Takao Kasuga, Matteo Garbelotto
Format: Article
Language:English
Published: Wiley 2019-06-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.5238
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spelling doaj-533731cfe2f344ab971141b3835483042021-03-02T03:25:23ZengWileyEcology and Evolution2045-77582019-06-019116588660510.1002/ece3.5238Molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybridsFabiano Sillo0Paolo Gonthier1Blakey Lockman2Takao Kasuga3Matteo Garbelotto4Department of Agricultural, Forest and Food Sciences (DISAFA) University of Torino Grugliasco (TO) ItalyDepartment of Agricultural, Forest and Food Sciences (DISAFA) University of Torino Grugliasco (TO) ItalyPacific Northwest Region, State and Private Forestry USDA Forest Service Portland OregonCrops Pathology and Genetics Research Unit USDA Agricultural Research Service Davis CaliforniaDepartment of Agricultural, Forest and Food Sciences (DISAFA) University of Torino Grugliasco (TO) ItalyAbstract 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.https://doi.org/10.1002/ece3.5238forest pathogenHeterobasidionhybridizationrapid evolution
collection DOAJ
language English
format Article
sources DOAJ
author Fabiano Sillo
Paolo Gonthier
Blakey Lockman
Takao Kasuga
Matteo Garbelotto
spellingShingle Fabiano Sillo
Paolo Gonthier
Blakey Lockman
Takao Kasuga
Matteo Garbelotto
Molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybrids
Ecology and Evolution
forest pathogen
Heterobasidion
hybridization
rapid evolution
author_facet Fabiano Sillo
Paolo Gonthier
Blakey Lockman
Takao Kasuga
Matteo Garbelotto
author_sort Fabiano Sillo
title Molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybrids
title_short Molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybrids
title_full Molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybrids
title_fullStr Molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybrids
title_full_unstemmed Molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybrids
title_sort molecular analyses identify hybridization‐mediated nuclear evolution in newly discovered fungal hybrids
publisher Wiley
series Ecology and Evolution
issn 2045-7758
publishDate 2019-06-01
description 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.
topic forest pathogen
Heterobasidion
hybridization
rapid evolution
url https://doi.org/10.1002/ece3.5238
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