Genomic patterns of structural variation among diverse genotypes of Sorghum bicolor and a potential role for deletions in local adaptation

Abstract

Genomic structural mutations, especially deletions, are an important source of variation in many species and can play key roles in phenotypic diversification and evolution. Previous work in many plant species has identified multiple instances of structural variations (SVs) occurring in or near genes related to stress response and disease resistance, suggesting a possible role for SVs in local adaptation. Sorghum (Sorghum bicolor (L.) Moench) is one of the most widely grown cereal crops in the world. It has been adapted to an array of different climates as well as bred for multiple purposes, resulting in a striking phenotypic diversity. In this study, we identified genome-wide SVs in the Biomass Association Panel, a collection of 347 diverse sorghum genotypes collected from multiple countries and continents. Using Illumina-based, short-read whole genome resequencing data from every genotype, we found a total of 24,648 SVs, including 22,359 deletions. The global site frequency spectrum of deletions and other types of SVs fit a model of neutral evolution, suggesting that the majority of these mutations were not under any types of selection. Clustering results based on single nucleotide polymorphisms separated the genotypes into eight clusters which largely corresponded with geographic origins, with many of the large deletions we uncovered being unique to a single cluster. Even though most deletions appeared to be neutral, a handful of cluster-specific deletions were found in genes related to biotic and abiotic stress responses, supporting the possibility that at least some of these deletions contribute to local adaptation in sorghum.

Sorghum Association Panel whole‐genome sequencing establishes cornerstone resource for dissecting genomic diversity

“…So, while it is possible that the BTx623 reference may have abnormally high copy numbers, the likely explanation for such high prevalence of deletions over insertions is that the variant callers can more easily identify deletions due to the loss of coverage associated with deletions. Not only did the distribution of CNV types show a preponderance of deletions over insertions (Figure 2c), these variant types were also more densely distributed around telomeric regions (Figure 2a), which is consistent with previous observations in sorghum (Songsomboon et al, 2021).…”

“…We identified nearly seven times more CNVs compared to a previous study in sorghum (Songsomboon et al., 2021) likely due to the variant callers used as Songsomboon et al. (Songsomboon et al., 2021) only used LUMPY, but we used LUMPY and three other variant callers within Hecaton. The identification of indels is relative to the reference genome used.…”

“…Larger CNVs identified using Hecaton, ranging from 49 bp to 1 Mb, were retained for analyses, whereas all CNVs over 1 Mb in length were deemed false positives due to the limitations of short-read data (Wijfjes et al, 2019). We identified nearly seven times more CNVs compared to a previous study in sorghum (Songsomboon et al, 2021) likely due to the variant callers used as Songsomboon et al (Songsomboon et al, 2021) only used LUMPY, but we used LUMPY and three other variant callers within Hecaton. The identification of indels is relative to the reference genome used.…”

“…Yet, their value for identifying genome‐wide associations has been overlooked due to limitations in both production cost and scalability (Say, 2017). Few studies in sorghum have examined indels and CNVs at scale (Ruperao et al., 2021; Songsomboon et al., 2021; Tao et al., 2021; Zhang et al., 2014; Zheng et al., 2011), and none of these demonstrated the comparative value of all three variant types for GWAS. In fact, comparisons across all three variant types are limited to human studies where funds and scalability are less limiting, but even human studies lack a comprehensive review of the topic (Dai et al., 2020; Say, 2017).…”

Ten new high-quality genome assemblies for diverse bioenergy sorghum genotypes

“…Furthermore, a genome-wide association study (GWAS) exploring the genetic architecture of bioenergy-related traits found that a large deletion in a sorghum-specific iron transporter was linked to stalk sugar accumulation (Brenton et al, 2016(Brenton et al, , 2020. Most recently, we undertook a broad survey of genome-wide deletions in a panel of nearly 350 diverse sorghum accessions, and found large deletions in multiple genes related to biotic and abiotic stress responses that were unique to particular geographic origins, and appeared to play a role in local adaptation (Songsomboon et al, 2021). Taken together, these results suggest that unraveling complex traits in sorghum and other crops will require a comprehensive picture of both structural and single nucleotide mutations.…”