Population genetics and genome-wide association studies provide insights into the influence of selective breeding on genetic variation in lettuce

Authors: Park, Sunchung - Sun; Kumar, Pawan; SHI, AINONG - University Of Arkansas; Mou, Beiquan

Submitted to: The Plant Genome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/17/2020
Publication Date: 2/24/2021
Citation: Park, S., Kumar, P., Shi, A., Mou, B. 2021. Population genetics and genome-wide association studies provide insights into the influence of selective breeding on genetic variation in lettuce. The Plant Genome. 14(2). Article e20086. https://doi.org/10.1002/tpg2.20086.
DOI: https://doi.org/10.1002/tpg2.20086

Interpretive Summary: Knowledge about germplasm diversity and genetic relationships among lettuce breeding materials would be an invaluable aid in crop improvement strategies. Our understanding on this subject remained incomplete mostly due to the cost to explore genome-wide genetic variation. In the past, the evaluation of genetic diversity was carried out on limited number of accessions with relatively small number of genetic markers. However, the recent advance of DNA sequencing technology enables us to analyze genome-wide genetic variation. We evaluated a diverse set of 441 lettuce accessions using the genotyping-by-sequencing (GBS) method, a cost-effective, high-throughput means to identify genetic variants across the genome, resulting in 186,008 single nucleotide polymorphism (SNP) data. Population genetic analyses based on the SNP data indicated substantial genetic difference between four lettuce horticultural types (butterhead, crisphead, leaf, and romaine), with crisphead type lettuces having less genetic variation than other types of lettuce. The artificial selection for horticultural traits during lettuce breeding programs led to a reduction of genetic variation in crisphead type. This study shows that the reduced genetic variation in crisphead type lettuces can be attributed in part to the selection by breeders of delayed bolting. The genomic regions identified with low genetic variation in this study are promising targets to introgress novel alleles for further improved varieties. The information on genetic diversity of lettuce germplasm can be useful for selecting parents to breed improved lettuce cultivars.

Technical Abstract: Genetic diversity is an important resource in crop breeding to improve cultivars with desirable traits. Selective breeding can lead to a reduction of genetic diversity. However, our understanding on this subject remains limited in lettuce (Lactuca sativa L.). Genotyping-by-sequencing (GBS) can provide a reduced version of the genome as a cost-effective method to identify genetic variants across the genome. We genotyped a diverse set of 441 lettuce accessions using the GBS method. Phylogenetic and population genetic analyses indicated substantial genetic divergence among four horticultural types of lettuce: butterhead, crisphead, leaf, and romaine. Genetic-diversity estimates between and within the four types indicated that the crisphead type was the most differentiated from other types, whereas its population was the most homogenous with the slowest linkage disequilibrium (LD) decay among the four types. These results suggested that crisphead lettuces had relatively less genetic variation across the genome as well as low gene flow from other types. We identified putative selective sweep regions that showed low genetic variation in the crisphead type. Genome-wide association study (GWAS) and quantitative trait loci (QTL) analyses provided evidence that these genomic regions were, in part, associated with delayed bolting, implicating the positive selection of delayed bolting in reducing variation. Our findings enhance the current understanding of genetic diversity and the impacts of selective breeding on patterning genetic variation in lettuce.