Academic journal article Genetics

High-Diversity Genes in the Arabidopsis Genome

Academic journal article Genetics

High-Diversity Genes in the Arabidopsis Genome

Article excerpt

ABSTRACT

High-diversity genes represent an important class of loci in organismal genomes. Since elevated levels of nucleotide variation are a key component of the molecular signature for balancing selection or local adaptation, high-diversity genes may represent loci whose alleles are selectively maintained as balanced polymorphisms. Comparison of 4300 random shotgun sequence fragments of the Arabidopsis thaliana L er ecotype genome with the whole genomic sequence of the Col-0 ecotype identified 60 genes with putatively high levels of intraspecific variability. Eleven of these genes were sequenced in multiple A. thaliana accessions, 3 of which were found to display elevated levels of nucleotide polymorphism. These genes encode the wyb-like transcription factor MYB103, a putative soluble starch synthase I, and a homeodomain-leucine zipper transcription factor. Analysis of these genes and 4-7 flanking genes in 14-20 A. thaliana ecotypes revealed that two of these loci show other characteristics of balanced polymorphisms, including broad peaks of nucleotide diversity spanning multiple linked genes and an excess of intermediate-frequency polymorphisms. Scanning genomes for high-diversity genomic regions may be useful in approaches to adaptive trait locus mapping for uncovering candidate balanced polymorphisms.

UNCOVERING the genetic basis of adaptation has been a central goal of evolutionary genetics for nearly a century (ORR and COYNE 1992), and recent advances in genetic analysis have permitted the identification and isolation of loci responsible for speciation (GREENBERG et al 2003; BARBASH et al. 2004), species differences (DOEBLEY et al. 1997; GOMPEL and CARROLL 2003), and adaptive intraspecific variation QOHANSON et al. 2000; KROYMANN et al. 2003). Several approaches based on patterns of molecular evolution have been proposed to scan genomes for genes associated with adaptation (NiELSEN2001; SWANSON et ai 2001a,b; SCHLOTTERER 2002; BAMSHAD and WOODING 2003; BARRIER et al. 2003). These methods provide opportunities to analyze evolutionary diversification at both molecular genetic and phenotypic levels.

Approaches for mapping adaptive trait loci are based on detecting regions of the genome in which intraspecific sequence variation and/or interspecific divergence deviate either from predictions of a neutral-equilibrium model (NIELSEN 2001) or from the norm of a genomewide distribution (Ïôôï 2000; LUIKART et al. 2003). Evolutionary expressed sequence tag (EST) (SwANSON et al. 2001a,b; BARRIER et al. 2003) and comparative genomic approaches (CLARK et al. 2003), for example, use interspecifie patterns of nonsynonymous/synonynmous substitution ratios (K21/Ks) to identify candidate adaptive genes on the basis of accelerated rates of protein evolution (K3/Ks> 1). Genes and genomic regions associated with directional selection have also been identified by scanning dense sets of genome-wide molecular markers for reduced levels of variation (HARR et al. 2002; PAYSEUR et al. 2002; SCHLOTTERER 2002; VIGOUROUX et al. 2002; WOOTTON et al 2002; STORZ et al 2004). The latter approach, referred to as hitchhiking mapping, is based on the premise that a beneficial mutation that rapidly spreads in a population will also reduce nucleotide variation at linked neutral loci. Hitchhiking mapping has successfully identified several genomic regions containing putative adaptive trait loci that were thought to contribute to the worldwide colonization of Drosophila melanogasterout of Africa ^10,0OO years ago (HARR et al. 2002). Although genome scanning for putative adaptive trait loci on the basis of levels of molecular diversity has focused largely on identifying genes associated with directional selection, this approach could also be employed in identifying genes and/or genomic regions that harbor balanced polymorphisms. This could complement other genome-scanning approaches, such as screens for elevated F^1 estimates in marker loci between two populations (ÁêÅÕ et al. …

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