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

Authors: SILLO, FABIANO - University Of Torino; GONTHIER, PAOLO - University Of Torino; LOCKMAN, BLAKEY - Us Forest Service (FS); Kasuga, Takao; GARBELOTTO, MATTEO - University Of California

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/23/2019
Publication Date: 5/9/2019
Citation: Sillo, F., Gonthier, P., Lockman, B., Kasuga, T., Garbelotto, M. 2019. Molecular analyses identify hybridization-mediated nuclear evolution in newly discovered fungal hybrids. Ecology and Evolution. 00:1–18. https://doi.org/10.1002/ece3.5238.
DOI: https://doi.org/10.1002/ece3.5238

Interpretive Summary: Fungi belonging to the genus Heterobasidion have the dubious honor of being the most damaging pathogens to conifers in most of the temperate regions of the Northern Hemisphere. There are two Heterobasidion species in the US and in a high elevation alpine larch stand in Montana, the dominant fungal pathogen Heterobasidion occidentale has hybridized with a locally rare Eastern North American population of H. irregulare. This discovery demonstrates that alpine larch can be a universal host favouring interspecific hybridization between H. occidentale and H. irregulare resulted in rapid evolution of a novel genome.

Technical Abstract: Hybridization may be a major driver in the evolution of plant pathogens. In a high elevation alpine larch stand in Montana, the dominant fungal pathogen Heterobasidion occidentale has hybridized with a locally rare Eastern North American population of H. irregulare. Sequence analysis of one mitochondrial and four nuclear loci performed on 11 Heterobasidion genotypes indicated that hybridization has increased allelic diversity by generating novel alleles unreported in either parental species. Sequence data and ploidy analysis through flow cytometry confirmed that all heterokaryotic genotypes were not first generation hybrids, but were instead the result of multiple backcrosses, indicating the fertility of hybrids. Additionally, all admixed genotypes possessed the H. occidentale mitochondrion, indicating that the hybrid progeny may have been backcrossing mostly with H. occidentale. A major consequence of the uniparental backcrossing between hybrids and H. occidentale has been the rapid evolution of the H. irregulare genome as indicated by the results of ABBA/BABA and Tajima’s tests. Based on phylogenetic analysis, Bayesian assignment, and ordination tests, H. irregulare alleles in hybrids are clearly distinct from all known H. irregulare alleles. 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 favoring interspecific hybridization between H. occidentale and H. irregulare and the asymmetric rapid evolution of a novel genome, derived from that of the rare H. irregulare parental species, but clearly distinct from it.