Effects of Introgression and Recombination on Haplotype Structure and Linkage Disequilibrium Surrounding a Locus EncodingBymovirusResistance in Barley

Abstract

We present a detailed analysis of linkage disequilibrium (LD) in the physical and genetic context of the barley gene Hv-eIF4E, which confers resistance to the barley yellow mosaic virus (BYMV) complex. Eightythree SNPs distributed over 132 kb of Hv-eIF4E and six additional fragments genetically mapped to its flanking region were used to derive haplotypes from 131 accessions. Three haplogroups were recognized, discriminating between the alleles rym4 and rym5, which each encode for a spectrum of resistance to BYMV. With increasing map distance, haplotypes of susceptible genotypes displayed diverse patterns driven mainly by recombination, whereas haplotype diversity within the subgroups of resistant genotypes was limited. We conclude that the breakdown of LD within 1 cM of the resistance gene was generated mainly by susceptible genotypes. Despite the LD decay, a significant association between haplotype and resistance to BYMV was detected up to a distance of 5.5 cM from the resistance gene. The LD pattern and the haplotype structure of the target chromosomal region are the result of interplay between low recombination and recent breeding history.T HE ever-increasing availability of nucleotide sequence, and the concomitant improvement that this brings to our understanding of the organization of complex crop plant genomes, has created the opportunity to identify trait-related genes and to analyze their allelic diversity. The association between phenotype and genotype in diverse populations represents a powerful approach, but the applicability and design of such analyses depend critically on the extent and pattern of linkage disequilibrium (LD) present in the study population. Cultivated barley (Hordeum vulgare ssp. vulgare) has many of the hallmarks known to be associated with a high level of LD. Its effective recombination rate is dramatically reduced by its predominantly inbreeding habit, with an estimated outcrossing rate of 5% in winter barley and ,0.5% in spring barley (Giles et al. 1974;Doll 1987;Abdel-Ghani et al. 2005). Domestication and intensive selection have introduced major bottlenecks in genetic variation, and these are thought to be largely responsible for the perceived narrowness of the modern gene pool (Badr et al. 2000;Russell et al. 2000;Matus and Hayes 2002). LD in modern spring barley, as estimated from a whole-genome survey, extends over distances of at least 10 cM, indicative of an extensive conservation of the genetic identity of barley chromosomes (Kraakman et al. 2004). However, estimates of genomewide LD conceal localized variation, which, as has been shown for a number of species, can be substantial and independent of the mating system (Gupta et al. 2005). In the self-pollinating species Arabidopsis thaliana LD varies from ,10 kb in global (Tian et al. 2002) to 50-250 kb in local populations (Nordborg et al. , 2005Aranzana et al. 2005). Within a given set of maize (an outbreeding species) accessions, the extent of LD has been documented to vary widely around different genes and chr...

Association mapping reveals gene action and interactions in the determination of flowering time in barley

“…Population structure, the target genomic region, and the number of polymorphic sites can all have a major impact on the pattern of LD and consequently, on the outcome of association studies (Akey et al 2003;Ke et al 2004;Pritchard et al 2000b). The population structure of the barley collection is largely consistent with the phenotype-based grouping into two-and six-rowed ear types, as has been noted in other sets of spring (Brantestam et al 2007;Hayes and Szucs 2006) and winter cultivars (Matus and Hayes 2002;Stracke et al 2007;Thiel et al 2003). Ear type is encoded by a single major gene v, located on chromosome 2H (Komatsuda et al 2007), which cannot account for the existence of genetically distinct subpopulations.…”

Sequence diversification in recessive alleles of two host factor genes suggests adaptive selection for bymovirus resistance in cultivated barley from East Asia

“…The EIF4E protein is of crucial importance in organisms, as it is a component of the conserved eukaryotic translation initiation complex that interacts with the cap-structure of the host mRNAs and enables initiation of the translation of cellular proteins (Browning 1996; Kawaguchi and Bailey-Serres 2002). In previous EcoTILLING (a method for the discovery of natural nucleotide diversity) studies, no haplotypes carrying loss-of-function mutations in EIF4E were found in broad collections of accessions of a number of different crops and related wild plant species (Charron et al 2008; Hofinger et al2009, 2011; Ibiza et al 2010; Konecna et al 2014; Nieto et al 2007; Rubio et al 2009; Stein et al 2005; Stracke et al 2007). In the coding sequence of HvEIF4E , only non-synonymous mutations were previously identified in an Ethyl Methane Sulfonate (EMS) induced barley population (Gottwald et al 2009).…”

Sequence variation in the barley genes encoding sucrose synthase I and sucrose phosphate synthase II, and its association with variation in grain traits and malting quality

“…Its value in barley has been demonstrated for various candidate genes and phenotypic traits (Haseneyer et al 2010;Matthies et al 2009a, b;Stracke et al 2007Stracke et al , 2009Malysheva-Otto et al 2006;Kraakman et al 2004Kraakman et al , 2006. Here, we report the sequence diversity present in barley SSI and SPSII, and use this variation to determine their influence over grain and malting quality.…”

“…As all SNP markers are found to be in complete linkage disequilibrium (LD) in the SSI gene, the resulting three main haplotypes were considered here for the association analysis (Table 1). High LD in barley is an important prerequisite for association mapping in candidate genes (Caldwell et al 2006;Rostoks et al 2006;Stracke et al 2007). A high LD was found between all eleven SNPs of SSI in the total set of 190 varieties and in the subpopulation of 96 winter barleys.…”