Meiotic recombination in the offspring of Microbotryum hybrids and its impact on pathogenicity

Abstract

Background Hybridization is a central mechanism in evolution, producing new species or introducing important genetic variation into existing species. In plant-pathogenic fungi, adaptation and specialization to exploit a host species are key determinants of evolutionary success. Here, we performed experimental crosses between the two pathogenic Microbotryum species, M. lychnidis-dioicae and M. silenes-acaulis that are specialized to different hosts. The resulting offspring were analyzed on phenotypic and genomic levels to describe genomic characteristics of hybrid offspring and genetic factors likely involved in host-specialization. Results Genomic analyses of interspecific fungal hybrids revealed that individuals were most viable if the majority of loci were inherited from one species. Interestingly, species-specific loci were strictly controlled by the species’ origin of the mating type locus. Moreover we detected signs of crossing over and chromosome duplications in the genomes of the analyzed hybrids. In Microbotryum, mitochondrial DNA was found to be uniparentally inherited from the a2 mating type. Genome comparison revealed that most gene families are shared and the majority of genes are conserved between the two species, indicating very similar biological features, including infection and pathogenicity processes. Moreover, we detected 211 candidate genes that were retained under host-driven selection of backcrossed lines. These genes and might therefore either play a crucial role in host specialization or be linked to genes that are essential for specialization. Conclusion The combination of genome analyses with experimental selection and hybridization is a promising way to investigate host-pathogen interactions. This study manifests genetic factors of host specialization that are required for successful biotrophic infection of the post-zygotic stage, but also demonstrates the strong influence of intra-genomic conflicts or instabilities on the viability of hybrids in the haploid host-independent stage.

The evolving species concepts used for yeasts: from phenotypes and genomes to speciation networks

“…On the other hand, work on smut fungal populations shows ongoing gene flow between closely related parasite species (Petit et al 2017) and experimental work clearly indicates that even distantly related species are able to hybridize (e.g. Büker et al 2020;Kellner et al 2011). High selfing rates by fusion of meiotic products from the same teliospore, as is for instance common in Microbotryum anther smuts (Giraud et al 2005), could restrict gene flow of sympatric populations on different host species enough for reproductive barriers between species to evolve on different hosts (Giraud et al 2008).…”

“…However, pre-and postzygotic reproduction barriers in agreement with the BSC are the norm in these fungi, as even artificial mating experiments in the laboratory resulted in few viable hybrids. Still, the hybrids that survived showed rare recombination events (Büker et al 2020), which could be important for accessing new hosts and the evolution of new smut fungal species.…”

Delimiting species in Basidiomycota: a review

“…Although many population studies support clearly separated species, hybrids between closely related species are observed in nature (Petit et al 2017). Hybrids can also be producted in culture under laboratory conditions, but their infection rate is apparently markedly reduced (Büker et al 2020).…”