Determinate growth habit is an agronomically important trait associated with domestication in soya bean. Previous studies have demonstrated that the emergence of determinacy is correlated with artificial selection on four nonsynonymous mutations in the Dt1 gene. To better understand the signatures of the soft sweeps across the Dt1 locus and track the origins of the determinate alleles, we examined patterns of nucleotide variation in Dt1 and the surrounding genomic region of approximately 800 kb. Four local, asymmetrical hard sweeps on four determinate alleles, sized approximately 660, 120, 220 and 150 kb, were identified, which constitute the soft sweeps for the adaptation. These variable-sized sweeps substantially reflected the strength and timing of selection and indicated that the selection on the alleles had been completed rapidly within half a century. Statistics of EHH, iHS, H12 and H2/H1 based on haplotype data had the power to detect the soft sweeps, revealing distinct signatures of extensive long-range LD and haplotype homozygosity, and multiple frequent adaptive haplotypes. A haplotype network constructed for Dt1 and a phylogenetic tree based on its extended haplotype block implied independent sources of the adaptive alleles through de novo mutations or rare standing variation in quick succession during the selective phase, strongly supporting multiple origins of the determinacy. We propose that the adaptation of soya bean determinacy is guided by a model of soft sweeps and that this model might be indispensable during crop domestication or evolution.
Genome scans for selection can provide an efficient way to dissect the genetic basis of domestication traits and understand mechanisms of adaptation during crop evolution. Selection involving soft sweeps (simultaneous selection for multiple alleles) is probably common in plant genomes but is under‐studied, and few if any studies have systematically scanned for soft sweeps in the context of crop domestication. Using genome resequencing data from 302 wild and domesticated soybean accessions, we conducted selection scans using five widely employed statistics to identify selection candidates under classical (hard) and soft sweeps. Across the genome, inferred hard sweeps are predominant in domesticated soybean landraces and improved varieties, whereas soft sweeps are more prevalent in a representative subpopulation of the wild ancestor. Six domestication‐related genes, representing both hard and soft sweeps and different stages of domestication, were used as positive controls to assess the detectability of domestication‐associated sweeps. Performance of various test statistics suggests that differentiation‐based (FST) methods are robust for detecting complete hard sweeps, and that LD‐based strategies perform well for identifying recent/ongoing sweeps; however, none of the test statistics detected a known soft sweep we previously documented at the domestication gene Dt1. Genome scans yielded a set of 66 candidate loci that were identified by both differentiation‐based and LD‐based (iHH) methods; notably, this shared set overlaps with many previously identified QTLs for soybean domestication/improvement traits. Collectively, our results will help to advance genetic characterizations of soybean domestication traits and shed light on selection modes involved in adaptation in domesticated plant species.
Background DNA mutations of diverse types provide the raw material required for phenotypic variation and evolution. In the case of crop species, previous research aimed to elucidate the changing patterns of repetitive sequences, single-nucleotide polymorphisms (SNPs), and small InDels during domestication to explain morphological evolution and adaptation to different environments. Additionally, structural variations (SVs) encompassing larger stretches of DNA are more likely to alter gene expression levels leading to phenotypic variation affecting plant phenotypes and stress resistance. Previous studies on SVs in rice were hampered by reliance on short-read sequencing limiting the quantity and quality of SV identification, while SV data are currently only available for cultivated rice, with wild rice largely uncharacterized. Here, we generated two genome assemblies for O. rufipogon using long-read sequencing and provide insights on the evolutionary pattern and effect of SVs on morphological traits during rice domestication. Results In this study, we identified 318,589 SVs in cultivated and wild rice populations through a comprehensive analysis of 13 high-quality rice genomes and found that wild rice genomes contain 49% of unique SVs and an average of 1.76% of genes were lost during rice domestication. These SVs were further genotyped for 649 rice accessions, their evolutionary pattern during rice domestication and potential association with the diversity of important agronomic traits were examined. Genome-wide association studies between these SVs and nine agronomic traits identified 413 candidate causal variants, which together affect 361 genes. An 824-bp deletion in japonica rice, which encodes a serine carboxypeptidase family protein, is shown to be associated with grain length. Conclusions We provide relatively accurate and complete SV datasets for cultivated and wild rice accessions, especially in TE-rich regions, by comparing long-read sequencing data for 13 representative varieties. The integrated rice SV map and the identified candidate genes and variants represent valuable resources for future genomic research and breeding in rice.
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