Genome organization of the tomato sun locus and characterization of the unusual retrotransposon Rider.

DNA sequences provide useful insights into genome structure and organization as well as evolution of species. We report on a detailed analysis of the locus surrounding the tomato (Solanum lycopersicum) fruit-shape gene SUN to determine the driving force and genome environment that foster the appearance of novel phenotypes. The gene density at the sun locus is similar to that described in other euchromatic portions of the tomato genome despite the relatively high number of transposable elements. Genes at the sun locus include protein-coding as well as RNA genes, are small in size, and belong to families that were duplicated at the locus an estimated 5-74 million years ago. In general, the DNA transposons at the sun locus are older than the RNA transposons, and their insertion pre-dates the speciation of S. lycopersicum and S. pimpinellifolium. Gene redundancy and large intergenic regions may explain the tolerance of the sun locus to frequent rearrangements and transpositions. The most recent transposition event at the sun locus involved Rider, a recently discovered high-copy retrotransposon. Rider probably arose early during the speciation of tomato. The element inserts into or near to genes and may still be active, which are unusual features for a high-copy element. Rider full-length and read-through transcripts past the typical transcription termination stop are detected, and the latter are required for mobilizing nearby sequences. Rider activity has resulted in an altered phenotype in three known cases, and may therefore have played an important role in tomato evolution and domestication.