Abstract
BackgroundHybridization 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.ResultsGenomic 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.ConclusionThe 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.
Highlights
Hybridization is a central mechanism in evolution, producing new species or introducing important genetic variation into existing species
From 50 S. latifolia plants that were inoculated with its endemic pathogen Microbotryum lychnidis-dioiceae (MSL), a proportion of 0.79 became diseased, while none of the 50 plants inoculated with M. silenes-acaulis (MSA) exhibited disease symptoms (Fig. 2)
Infection experiments on the host species S. latifolia supported a high degree of specialization of these two pathogens, since none of these host plants became infected by M. silenes-acaulis, while M. lychnidis-dioicae successfully infected the host at high rates
Summary
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. Central to the ecology of pathogenic fungi is their adaptation to exploit the host environment, and there is broad variation in host specialization and adaptation among pathogens [5]. In plant-pathogenic fungi, host specificity is often characteristic of the biotrophic lifestyle, where the fungi colonize and exploit living host tissues [8]. These biotrophic fungi often produce ‘effector’ proteins. Genome and secretome (i.e. all secreted proteins) analyses of fungal species with different lifestyles revealed a great repertoire of effector proteins that are common in fungi to promote virulence and interact with the host. The function of such effector proteins or their role in specialization is often unclear [5, 11]
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