Conditional neutrality at two adjacent NBS‐LRR disease resistance loci in natural populations of Arabidopsis lyrata

Abstract

We examined patterns of nucleotide diversity at a genomic region containing two linked candidate disease resistance (NBS-LRR) genes in seven populations of the outcrossing plant Arabidopsis lyrata. In comparison with two adjacent control genes and neutral reference genes across the genome, the NBS-LRR genes exhibited elevated nonsynonymous variation and a large number of major-effect polymorphisms causing early stop codons and/or frameshift mutations. In contrast, analysis of synonymous diversity provided no evidence that the region was subject to long-term balancing selection or recent selective sweeps in any of the seven populations surveyed. Also in contrast with earlier surveys of one of these R genes, there was no evidence that the resistance genes or the major-effect mutations were subject to elevated differentiation between populations. We suggest that conditional neutrality in the absence of the corresponding pathogen, rather than long-term balancing selection or local adaptation, may in some circumstances be a significant cause of elevated functional polymorphism at R genes. In contrast with the R genes, analysis of diversity and differentiation at the flanking FERONIA locus showed high population divergence, suggesting local adaptation on this locus controlling male-female signalling during fertilization.

Presence–Absence Variation in A. thaliana Is Primarily Associated with Genomic Signatures Consistent with Relaxed Selective Constraints

“…This would be consistent with the increase in nucleotide diversity, but this scenario cannot be distinguished from alternative neutral models. Conditional neutrality at PAV loci, where the functional gene has ceased to be adaptive in some but not all environments, cannot be ruled out (e.g., in the case of resistance genes where the corresponding pathogen is absent [Gos and Wright 2008]). In this case, the absent allele would have no selective advantage at any point but rather result from relaxed constraints associated with PAV genes in some Arabidopsis populations.…”

Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula

“…By contrast, the nodule-specific cysteine rich gene family, which is found only in the galegoid lineage of legumes, contains members with direct antimicrobial properties as well as members involved in controlling the terminal differentiation of the nitrogen-fixing rhizobial bacteroids inside of nodules (41). High average diversity of the members of large, defense-related gene families, which has also been found in genome-wide surveys of A. thaliana (11,42), likely reflects both frequency-dependent selection favoring rare alleles (43) as well as relaxed selective constraint acting on nonfunctional gene copies (44).…”

Molecular evolution of a family of resistance gene analogs of nucleotide-binding site sequences in Solanum lycopersicum

“…These newly evolved NBS sequences might have played roles in the resistance to pathogens attacking tomato, and may be selectively advantageous. Rare allelic variants of subclades A1-A3 may rapidly increase in frequency in order to enhance the fitness when stresses are strong and later become selectively neutral due to pathogen counter-adaptation or a lower frequency of attack (Tiffin and Gaut 2001;Gos and Wright 2008). This evolutionary process is similar to the hypothesis of the birth-and-death cycle in response to the evolution of (Van der Hoorn et al 2002;Couch et al 2006).…”

“…These ancestral polymorphisms provide genetic constituents for avirulence against pathogens (McDowell and Simon 2006). Moreover, a recent study suggested the conditional neutral evolution of NBS-LRR RGAs in the absence of corresponding pathogens (Gos and Wright 2008).…”