Signatures of balancing selection are maintained at disease resistance loci following mating system evolution and a population bottleneck in the genus Capsella

Abstract

BackgroundPopulation bottlenecks can lead to a loss of variation at disease resistance loci, which could have important consequences for the ability of populations to adapt to pathogen pressure. Alternatively, current or past balancing selection could maintain high diversity, creating a strong heterogeneity in the retention of polymorphism across the genome of bottlenecked populations. We sequenced part of the LRR region of 9 NBS-LRR disease resistance genes in the outcrossing Capsella grandiflora and the recently derived, bottlenecked selfing species Capsella rubella, and compared levels and patterns of nucleotide diversity and divergence with genome-wide reference loci.ResultsIn strong contrast with reference loci, average diversity at resistance loci was comparable between C. rubella and C. grandiflora, primarily due to two loci with highly elevated diversity indicative of past or present balancing selection. Average between-species differentiation was also reduced at the set of R-genes compared with reference loci, which is consistent with the maintenance of ancestral polymorphism.ConclusionsHistorical or ongoing balancing selection on plant disease resistance genes is a likely contributor to the retention of ancestral polymorphism in some regions of the bottlenecked Capella rubella genome.

Plant adaptation and speciation studied by population genomic approaches

“…In A. thaliana , population genetic studies have revealed multiple modes of selection that shape the nucleotide variations of R‐genes, such as balancing or directional selection (Bakker et al., ; Bergelson, Kreitman, Stahl, & Tian, ; Mauricio et al., ; Rose et al., ; Stahl, Dwyer, Mauricio, Kreitman, & Bergelson, ). Similar patterns have also been reported from other species, including Capsella rubella (Gos, Slotte, & Wright, ), Lactuca sativa (Kuang, Woo, Meyers, Nevo, & Michelmore, ), Lycopersicon (Rose, Michelmore, & Langley, ), and Solanum peruvianum (Horger et al., ).…”

Genome‐wide scans of selection highlight the impact of biotic and abiotic constraints in natural populations of the model grass Brachypodium distachyon

“…On the other hand, we also found additional R‐genes and genes involved in phosphorylation, a process especially important for immune signaling response in plants (for review, see Park et al ., ), to be under balancing selection. Our results are thus consistent with the two classical models of host–pathogens coevolution (Mondragón‐palomino et al ., ; Mchale et al ., ; Gos et al ., ; Mace et al ., ; Zhong et al ., ; Wu et al ., ). Overall, and as shown in other organisms (Fumagalli et al ., ; Karasov et al ., ; Krattinger and Keller, ,b; Bourgeois et al ., ), our genome‐wide approach suggests that pathogens may constitute an important driving force of population and genome evolution in B. distachyon .…”

Genomic variability as a driver of plant–pathogen coevolution?

“…Several of the balanced resistance polymorphisms studied to date appear to be millions of years old, even persisting as trans-species polymorphisms [36,43,47–49]. The long-term maintenance of these polymorphisms indicates the ubiquity and stability of the dynamics that generated them.…”