Chloroplast and nuclear phylogenomics reveals concordant phylogenetic structure in wild tomatoes (Solanum sect. Lycopersicon, Solanaceae)

Tomato (Solanum lycopersicon) is one of the most important crops worldwide with 177 million tonnes produced over 4.7 million ha. Compared to many other crops plant used in commercial production show very little genetic variation due to selection for a limited set of traits during its domestication. This group consisting of 13 inter-crossable diploid (2n = 2x = 24) species under extensive taxonomic studies, is an important source of traits and genes for tomato improvement. Tomato is the most intensively studied solanaceous species both in terms of its genetics and genomics. In addition to marker, sequence, and bioinformatic resources, various molecular genetic tools for functional analyses have been developed extensively. It is surprizing that these large-scale genome-sequencing initiatives generated quasi-complete plastid sequences, which were later discarded as non-target contamination without further analysis. They provide an untapped treasure trove of plastid genomic in raw read archives and other repositories for tomatoes. Chloroplast DNA is organized in compact gene-rich genomes, which are present in high copy number within plant cells. In Solanaceae plastid gene content and synteny are highly conserved, which is also preserved to some level in the intergenic spacer regions (IGS & ITS). In the present study, we utilized high-throughput sequencing data to gather a transcriptome based nuclear matrix and to assemble complete plastid genome sequences for all species of the core tomato clade (Solanum sect. Lycopersicon). We compare the genome organization, structure and phylogenetic relationships based on these data and investigate incongruences found between nuclear and plastid genomic trees. Our study allowed us to construct the first interspecific analysis including all species of wild tomatoes based on entire plastid sequences and compare genomic rearrangements with congeneric taxa. We found that plastome based trees provide strong support for two major groups in the tomato clade with S. pennellii and S. habrochaites in two distinct groups with the rest of the species. On the other hand, these two species form a clade in a basal position as compared with other tomato species in the phylogenetic analyses based on nuclear genes. This topological incongruence observed might be caused by the chloroplast capture event. In this process, a new combination of nuclear and chloroplast genomes were formed through inter-species hybridization and subsequent backcrosses with S. pennellii and S. habrochaites. Cross-species transfer of the chloroplast from one species to another has been reported among hybridizing plant groups, but it has not been hypothesised previously in Solanaceae.