Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing

TL;DR

This study used whole-genome sequencing of 84 tomato accessions and wild relatives to analyze genetic diversity, identify specific polymorphisms, and resolve phylogenetic relationships, revealing low diversity in cultivated tomatoes and highlighting the importance of multiple reference genomes.

Contribution

It provides new reference genomes and comprehensive comparative analyses, demonstrating the extent of genetic erosion in cultivated tomatoes and the utility of whole-genome SNP data for phylogenetics.

Findings

Genetic diversity in crop tomatoes is extremely low compared to wild species.

Whole-genome SNP data effectively resolves phylogenetic relationships within the Lycopersicon clade.

Identified group- and species-specific polymorphisms linked to fruit traits and growth habits.

Abstract

Genetic variation in the tomato clade was explored by sequencing a selection of 84 tomato accessions and related wild species representative for the Lycopersicon, Arcanum, Eriopersicon, and Neolycopersicon groups. We present a reconstruction of three new reference genomes in support of our comparative genome analyses. Sequence diversity in commercial breeding lines appears extremely low, indicating the dramatic genetic erosion of crop tomatoes. This is reflected by the SNP count in wild species which can exceed 10 million i.e. 20 fold higher than in crop accessions. Comparative sequence alignment reveals group, species, and accession specific polymorphisms, which explain characteristic fruit traits and growth habits in tomato accessions. Using gene models from the annotated Heinz reference genome, we observe a bias in dN/dS ratio in fruit and growth diversification genes compared to a random set of genes, which probably is the result of a positive selection. We detected highly divergent segments in wild S. lycopersicum species, and footprints of introgressions in crop accessions originating from a common donor accession. Phylogenetic relationships of fruit diversification and growth specific genes from crop accessions show incomplete resolution and are dependent on the introgression donor. In contrast, whole genome SNP information has sufficient power to resolve the phylogenetic placement of each accession in the four main groups in the Lycopersicon clade using Maximum Likelihood analyses. Phylogenetic relationships appear correlated with habitat and mating type and point to the occurrence of geographical races within these groups and thus are of practical importance for introgressive hybridization breeding. Our study illustrates the need for multiple reference genomes in support of tomato comparative genomics and Solanum genome evolution studies.