Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep

Abstract

Both yellow and white corn occurs among ancestral open pollinated varieties. More recently, breeders have selected yellow endosperm variants of maize over ancestral white phenotypes for their increased nutritional value resulting from the up-regulation of the Y1 phytoene synthase gene product in endosperm tissue. As a result, diversity within yellow maize lines at the Y1 gene is dramatically decreased as compared to white corn. We analyzed patterns of sequence diversity and linkage disequilibrium in nine low copy regions located at varying distances from the Y1 gene, including a homolog of the barley Mlo gene. Patterns consistent with a selective sweep, such as significant associations of informative single-nucleotide polymorphisms with endosperm color phenotype, linkage disequilibrium, and significantly reduced diversity within the yellow endosperm haplotypes, were observed up to 600 kb downstream of Y1, whereas the upstream region showed a more rapid recovery. The starch branching enzyme 1 (sbe1) gene is the first region downstream of Y1 that does not have a highly conserved haplotype in the yellow endosperm germplasm.S elective forces acting on allelic variants of genes have a profound effect on local levels of genetic diversity and linkage disequilibria (LD). Positive directional selection leads to reduced variability and increased LD in the respective region (1-6), and the so-called selective sweep regions provide clues to genes that have been subjects of evolutionary forces as well as selection by humans. Recently, Clark et al. (7) characterized a selective sweep in the promoter region of teosinte branched1 (tb1). The sweep extends 60-90 kb upstream of the gene and is indicative of the gene's role in the domestication of maize from teosinte between 6,000 and 10,000 years ago.The maize Y1 gene on chromosome 6 has undergone recent selection for endosperm color phenotype. A recent study (8) uncovered a dramatic reduction in diversity at this gene for the yellow endosperm maize inbred lines only, over the entire 6-kb gene region. This footprint of selection was characterized by a conserved yellow endosperm haplotype at the 5Ј end of the gene with evidence of recombination toward the 3Ј end. Strong haplotype conservation at the 5Ј end is suggestive of the location of the causal variant associated with the gain-of-function mutation to yellow endosperm and may be indicative of further extension of the selective sweep in the 5Ј direction. The presence of recombinants in the 3Ј UTR region, however, suggested that the extent of the selective sweep may be limited downstream of the coding region.The white endosperm lines did not show characteristics of a selective sweep (8), despite the fact that the white endosperm phenotype is also a target of selection due to human taste preference (9). This is because white is the predicted ancestral state of the gene (John Doebley, personal communication), and thus multiple haplotypes are associated with the white endosperm phenotype.Understanding the boundaries of the selective ...

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