Abstract
BackgroundExamining allelic variation of R-genes in closely related perennial species of Arabidopsis thaliana is critical to understanding how population structure and ecology interact with selection to shape the evolution of innate immunity in plants. We finely sampled natural populations of Arabidopsis lyrata from the Great Lakes region of North America (A. l. lyrata) and broadly sampled six European countries (A. l. petraea) to investigate allelic variation of two R-genes (RPM1 and WRR4) and neutral genetic markers (Restriction Associated DNA sequences and microsatellites) in relation to mating system, phylogeographic structure and subspecies divergence.ResultsFine-scale sampling of populations revealed strong effects of mating system and population structure on patterns of polymorphism for both neutral loci and R-genes, with no strong evidence for selection. Broad geographic sampling revealed evidence of balancing selection maintaining polymorphism in R-genes, with elevated heterozygosity and diversity compared to neutral expectations and sharing of alleles among diverged subspecies. Codon-based tests detected both positive and purifying selection for both R-genes, as commonly found for animal immune genes.ConclusionsOur results highlight that combining fine and broad-scale sampling strategies can reveal the multiple factors influencing polymorphism and divergence at potentially adaptive genes such as R-genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0665-5) contains supplementary material, which is available to authorized users.
Highlights
Examining allelic variation of R-genes in closely related perennial species of Arabidopsis thaliana is critical to understanding how population structure and ecology interact with selection to shape the evolution of innate immunity in plants
We focused on two nucleotide-binding site (NBS)-leucine-rich repeat (LRR) proteins that confer resistance in A. thaliana to common biotrophic pathogens of the Brassicaceae: RPM1 (Resistance to Pseudomonas maculicola) [33] and WRR4 (White Rust Resistance) [34]
We addressed two questions: 1) At a fine spatial scale, how does population structure, mating system variation and selection shape patterns of polymorphism within and among A. l. lyrata populations around the Great Lakes region? we predicted that if the R-genes are under balancing selection this would result in higher heterozygosity and diversity, but reduced genetic structure among populations, relative to that observed at neutral microsatellites and RAD loci
Summary
Examining allelic variation of R-genes in closely related perennial species of Arabidopsis thaliana is critical to understanding how population structure and ecology interact with selection to shape the evolution of innate immunity in plants. We finely sampled natural populations of Arabidopsis lyrata from the Great Lakes region of North America Natural variation in disease resistance conferred by pathogen specific R-genes has been essential for the evolution of innate immunity in plants [1,2,3]. Signatures of balancing selection were only detected in seven out of 27 loci in a comprehensive study of R-genes in Arabidopsis thaliana [4], suggesting that other types of selection or neutral demographic processes could affect allelic variation of plant R-genes. Past demographic history and mating system variation could substantially impact genetic variation at both neutral
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