Distribution of runs of homozygosity in Lactuca species and its implications for plant breeding and evolutionary conservation.

Abstract

Runs of homozygosity (ROH) have been extensively investigated to uncover the genomic inbred regions that reflect past population and breeding histories. In this study, we have explored the distribution and number of ROH in different Lactuca species including the cultivated lettuce varieties and their wild relatives. Next generation sequencing (NGS) technology provides the unique opportunity to study the genomes with resolution up to per-base-pair and we could compute ROH in the highest accuracy using NGS data. Our study reveals that Lactuca sativa has the longest average ROH length and fewest number of ROHs, while wild species show shorter, more numerous ROHs as expected. We found that these cultivated varieties exhibit relatively stable number of ROH and ROH lengths, with the largest median ROH count observed in Oilseed and the largest average ROH length in Crisphead. There is a significant proportion of medium-length ROHs (100 kb-1 Mb) enriched in L. sativa and L. serriola, with the highest number observed in L. serriola, while L. saligna has more short ROHs (< 10 KB), and the highest number of ROHs in the 10 KB-100 KB range were observed in Butterhead, with Stalk and Oilseed showing fewer and shorter ROHs overall. It suggests that Stalk and Oilseed were still in a process of breeding. The comparison between PLINK computation and our developed in-house algorithm shows that PLINK tends to detect longer ROH, whereas our algorithm adopts a more conservative approach, resulting in fewer and shorter ROH segments detected with higher precision more suitable for NGS data. We further analyze the distribution of ROH hotspots with a higher frequency occurred across cultivated species genomes, which has identified key genes such as DREB2B, NHL12, RPV1, and EIX2, which play crucial roles in plant stress tolerance and immune responses, enhancing adaptability to extreme environments and providing resistance to various diseases. These findings provide fresh scientific insights into lettuce breeding, germplasm conservation, and sustainable production, highlighting the importance of understanding and managing genetic diversity in global agricultural practices.