Nature Communications 11, Article number: 4058 (2020)
The impact of transposable elements on tomato diversity
Marisol Domínguez, Elise Dugas, Médine Benchouaia, Basile Leduque, José M Jiménez-Gómez, Vincent Colot & Leandro Quadrana

Tomatoes come in a multitude of shapes and flavors despite a narrow genetic pool. Here, we leverage whole-genome resequencing data available for 602 cultivated and wild accessions to determine the contribution of transposable elements (TEs) to tomato diversity. We identify 6,906 TE insertions polymorphisms (TIPs), which result from the mobilization of 337 distinct TE families. Most TIPs are low frequency variants and TIPs are disproportionately located within or adjacent to genes involved in environmental responses. In addition, genic TE insertions tend to have strong transcriptional effects and they can notably lead to the generation of multiple transcript isoforms. Using genome-wide association studies (GWAS), we identify at least 40 TIPs robustly associated with extreme variation in major agronomic traits or secondary metabolites and in most cases, no SNP tags the TE insertion allele. Collectively, these findings highlight the unique role of TE mobilization in tomato diversification, with important implications for breeding.

For instance, our TIP-GWAS revealed a strong association between a RIDER insertion within the gene PSY1, which encodes a fruit-specific phytoene synthase, and yellow fruit (Fig. 3e–h). Incidentally, our SNP-GWAS revealed another variant of PSY1 associated with yellow fruit (Fig. 3g). Local assembly using short reads indicated that this alternative allele, which we named rDel to distinguish it from the previously identified rTE allele, contains an ~6-kb deletion that bridges the last exon of PSY1 with the next gene (Solyc03g031870) downstream (Fig. 3i). Together, rTE and rDel account for 60% of yellow tomato accessions, and those carrying the rTE allele display lower expression levels of PSY1 and yellower fruit than accessions with the rDel allele (Fig. 3j, k). Moreover, we detected the rTE and rDel alleles in several SLC and SLL vintage accessions but in none of the wild tomatoes (S. pimpinellifolium) and wild relatives (Fig. 3l), which suggests that rTE and rDel arose after domestication. Also, while the RIDER insertion affected a common haplotype of PSY1 shared among early domesticated and improved tomatoes, the ~6-kb deletion affected a rare haplotype containing numerous SP-derived sequences (Supplementary Fig. 4). Together, these results suggest that the first tomato cultivar introduced in Europe during the sixteenth century, which was reported to be yellow42, harbored the rTE allele.

CybeRose note: The association of transposons with genes related to fruit color and shape may account for some so-called "vegetative hybrids", and Burdick's (1951) odd results with doubled haploids.