Pangenomic analyses in the cultivated grapevine confirm high genomic collinearity and extensive dispensable gene content likely involved in adaptation.

Abstract

Pangenomes have now been developed for several horticultural crops, yet the extent to which genome diversity in sequence and organization contribute to plant adaptation and major agronomic traits remains poorly understood. Here, we assembled the genomes of 9 cultivated grapevine varieties and compared the genomes of 15 cultivated grapevine varieties for variation in gene and TE content. We found that genomic collinearity is highly conserved among varieties. We still observed substantial variation across genomes. Notably, we identified across varieties 55,662 orthologous genes, of which 55.3% appears to be dispensable. Dispensable genes are enriched for functions related to adaptation to biotic and abiotic constraints, suggesting that they may play a role in adaptation. Comparing our results with a recently published study, we found substantial differences with ∼12.6% of the genes we classified as core genes being classified as dispensable genes in this other study. We then constructed a pangenome graph and used it to performed genome-wide association studies for 3 important traits in grapevine production, which allowed us to include large structural variants as markers in the analyses. We identified 32 loci that we did not detect when we used the PN40024 genome as a reference, 20 of which are newly reported associations. Overall, our results indicates that despite recent advances in characterizing plant pangenomes, current gene classification into core and dispensable gene categories should be taken with caution. They also highlight the value of incorporating structural variants into GWAS, to better characterize the genetic architecture of agronomic traits.