Analysis of wild plant pathogen populations reveals a signal of adaptation in genes evolving for survival in agriculture in the beet rust pathogen (Uromyces beticola)

Abstract

Improvements in crop resistance to pathogens can reduce yield losses and address global malnourishment today. Gene-for-gene -type interactions can identify new sources of resistance but genetic resistance is often short lived. Ultimately an understanding of how pathogens rapidly adapt will allow us to both increase resistance gene durability and more effectively target chemical treatments. Until recently all agricultural pathogens were living on wild hosts. To understand crop pathogen evolution, we compared genetic diversity in agricultural and wild populations. Wild reservoirs may be the source of emergent pathogen lineages, but here we outline a strategy for comparison of wild and agricultural pathogen populations to highlight genes adapting to agriculture. To address this, we have selected and developed the beet rust system (Beta vulgaris, Uromyces beticola, respectively) as our wild-agricultural model. Our hypothesis is that pathogen adaptation to agricultural crops will be evident as divergence in comparisons of wild and agricultural plant pathogen populations. We sampled isolates in both the wild and agriculture, sequenced and assembled and annotated a large fungal genome and analysed genetic diversity in 42 re-sequenced rust isolates. We found population differentiation between isolates in the wild compared to a predominantly agricultural group. Fungal effector genes are co-evolving with host resistance and are important for successful colonisation. We predicted (and found) that these exhibit a greater signal of diversification and adaptation and more importantly displayed increased wild agricultural divergence. Finding a signal of adaptation in these genes highlights this as an important strategy to identify genes which are key to pathogen success, that analysis of agricultural isolates alone cannot.

Tools for pathogen genetic surveillance: Lessons from the ash dieback invasion of Europe

“…fraxineus invasion shows that recombination does operate, increasing the potential of any further introduced polymorphism [ 18 ]. Progress in our understanding of the impact of recombination in pathogen invasion may be made by studying pathogen invasions of crops from wild crop relatives (e.g., [ 14 , 25 ]).…”

Deep population structure linked to host vernalization requirement in the barley net blotch fungal pathogen

“…These introduced fungal pathogens, which now thrive on physiologically-and phenologically-homogenous hosts planted over vast areas, have reached their current distribution following the colonization of a variety of environments, with demographic histories strongly constrained by the actions of their human vectors [4,5]. As fungal pathogens established in new territories, they encountered new environmental conditions, new wild or domesticated host species, or new host varieties, potentially leading to local adaptation [6][7][8][9]. In ascomycetes, adaptation to new hosts (i.e.…”

Deep population structure linked to host vernalization requirement in the barley net blotch fungal pathogen

“…These introduced fungal pathogens, which now thrive on physiologically-and phenologically-homogenous hosts planted over vast areas, have reached their current distribution following the colonization of a variety of environments, with demographic histories strongly constrained by the actions of their human vectors [4,5]. As fungal pathogens established in new territories, they encountered new environmental conditions, new wild or domesticated host species, or new host varieties, potentially leading to local adaptation [6][7][8][9].…”