Reconstructing the Evolutionary History of Powdery Mildew Lineages (Blumeria graminis) at Different Evolutionary Time Scales with NGS Data

Abstract

Blumeria graminis (Ascomycota) includes fungal pathogens that infect numerous grasses and cereals. Despite its economic impact on agriculture and its scientific importance in plant–pathogen interaction studies, the evolution of different lineages with different host ranges is poorly understood. Moreover, the taxonomy of grass powdery mildew is rather exceptional: there is only one described species (B. graminis) subdivided in different formae speciales (ff.spp.), which are defined by their host range. In this study we applied phylogenomic and population genomic methods to whole genome sequence data of 31 isolates of B. graminis belonging to different ff.spp. and reconstructed the evolutionary relationships between different lineages. The results of the phylogenomic analysis support a pattern of co-evolution between some of the ff.spp. and their host plant. In addition, we identified exceptions to this pattern, namely host jump events and the recent radiation of a clade less than 280,000 years ago. Furthermore, we found a high level of gene tree incongruence localized in the youngest clade. To distinguish between incomplete lineage sorting and lateral gene flow, we applied a coalescent-based method of demographic inference and found evidence of horizontal gene flow between recently diverged lineages. Overall we found that different processes shaped the diversification of B. graminis, co-evolution with the host species, host jump and fast radiation. Our study is an example of how genomic data can resolve complex evolutionary histories of cryptic lineages at different time scales, dealing with incomplete lineage sorting and lateral gene flow.

Evolution within the fungal genus Verticillium is characterized by chromosomal rearrangement and gene loss

“…It was observed that different processes shaped the diversification of B. graminis, including co-evolution with the host species for some of the ff. spp., host jumps, host range expansions, lateral gene flow and fast radiation (Menardo et al, 2017). Arguably, as highly adapted and obligate biotrophic pathogens, powdery mildews underwent many host species-specific adaptations, which are perhaps not or less required for saprophytes and facultative and broad host range pathogens such as Verticillium species.…”

Evolution within the fungal genusVerticilliumis characterized by chromosomal rearrangement and gene loss

“…was reconstructed. It was observed that different processes shaped the diversification of B. graminis , including co-evolution with the host species for some of the ff.spp ., host jumps, host range expansions, lateral gene flow and fast radiation (Menardo et al, 2017). Arguably, as highly adapted and obligate biotrophic pathogens, powdery mildews underwent many host species–specific adaptations, which are perhaps not or less required for saprophytes and facultative and broad host range pathogens such as Verticillium species.…”

Comparative genome analyses reveal sequence features reflecting distinct modes of host-adaptation between dicot and monocot powdery mildew

“…fungi have co-evolved with their hosts, leading to host specialization. Yet, there are exceptions where possible host jumps or host range expansions might have occurred [ 17 ]. Additionally, while the majority of grass PM fungi are monophylogenetic, there may be exceptions; for example, there are different B. graminis isolates affecting Dactylis glomerata , and therefore B. g. f.sp.…”