Copy number variation shapes structural genomic diversity associated with ecological adaptation in the wild tomato Solanum chilense

Abstract

Copy Number Variation (CNV) is a prevalent type of variation affecting large genomic regions which contributes to both genetic diversity and ecological adaptation in plants. The target genes involved in adaptation through CNV in tomato and its wild relatives remain unexplored at the population level. Therefore, we characterized the CNV landscape of Solanum chilense, a wild tomato species adapted to dry habitats, using whole-genome short-read data of 35 individuals from seven populations. We identified 212,207 CNVs, including 160,926 deletions and 51,281 duplications. We found a higher number of CNVs in diverging populations occupying stressful habitats. CNVs and single nucleotide polymorphisms analyses concordantly revealed the known species population structure, underscoring the impact of historical demographic and recent colonization events shaping genome-wide CNVs. Furthermore, we identified 3,539 candidate genes with highly divergent CNV profiles across populations. Interestingly, these genes are functionally associated with response to abiotic stress and linked to multiple pathways of flowering time regulation. Gene CNVs in S. chilense exhibit two evolutionary trends: gene loss in ancestral lineages distributed in central and southern coast populations and gene gain in the most recent diverged lineage from the southern highland region. Environmental association of the CNVs ultimately linked the dynamics of gene copy number to six climatic variables. It suggests that natural selection has likely shaped CNV patterns in stress-response genes promoting the colonization of contrasting habitats. Our findings provide insights into the role of CNV underlying adaptation during recent range expansion.