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Tomato Transcriptomes Hint at Effects of Natural and Artificial Selection

NEW YORK (GenomeWeb News) – Both natural and artificial selection have taken their toll on tomato transcriptomes, researchers led by Julin Maloof from the University of California, Davis, reported yesterday in the Proceedings of the National Academy of Sciences.

Maloof and his colleagues performed deep sequencing on the transcriptomes of six species of tomato — one domesticated, two red-fruited wild, and three green-fruited wild species — in the hope of uncovering gene expression divergence between the domesticated and wild varieties. Additionally, the green-fruited accessions were adapted to different habitats, including high altitude or drought, and the domesticated line was marked by an increase in size.

By comparing the domesticated and wild tomatoes, the researchers uncovered potentially deleterious changes in the domestic line as well as changes in the wild lines likely linked to adaptation to different climates.

"Taken together, our results shed light on the pervasive effects artificial and natural selection have had on the transcriptomes of tomato and its wild relatives," the investigators wrote.

From their analyses, the researchers added, they were able to identify a number of sequence and expression-level polymorphisms that may be valuable for improving tomato crops.

To characterize sequence and transcript diversity in the tomato, the researchers sequenced the RNA of six species they selected — Solanum lycopersicum, S. pimpinellifolium, S. galapagense, S. habrochaites, S. chmielewskii, and S. pennellii — using the Illumina GAII or HiSeq 2000 and aligned them to the tomato reference genome, another S. lycopersicum variant. From this, they identified 1.5 million polymorphic sites.

A phylogenic tree generated for tomato, using the potato S. phureja as a root, placed red and green tomatoes in sister clades, with the domesticated tomatoes more closely related to the wild red ones. The cultivated accessions, the researchers noted, were quite similar to each other, though only a few mutations separated them from their nearest wild relative.

Indeed, both cultivated tomatoes and S. galapagense, a red-fruited wild species, exhibited signs of an increased rate of non-synonymous to synonymous substitutions, suggested that both species when through a population bottleneck, likely due to domestication and island colonization, respectively.

Further, looking at the non-synonymous to synonymous substitutions rates across the tomato species, the investigators noted that more than two dozen genes showed evidence of positive selection, though most of them have yet to be annotated.

By inspecting transcript expression in seedling tissues, Maloof and his colleagues detected more than 25,000 expressed transcripts, about 8,000 of which appeared to be differentially expressed. Through a gene ontology enrichment analysis, many of those differentially expressed genes seemed to be involved in stress response, defense response, and photosynthesis, among other processes.

"Enrichment for these categories indicates that abiotic and biotic stresses have played a major role driving transcriptional variation among these species," Maloof and his colleagues wrote.

The desert-adapted S. pennellii lineage showed the greatest number of species expression-level changes, and those changes were enriched in genes dealing with salt stress.

Other comparisons between lineages pointed toward redox and metabolic changes. For example, wild species expressed six- to nine-fold lower levels of fructose as compared to domesticated lines, and S. pennellii also showed lower levels of redox-reaction products, as compared to cultivated tomatoes.

"In summary, the pathways identified by these analyses are consistent with the expected selective pressures on each of these lineages, with strong natural selection for life in a desert environment for S. pennellii and artificial selection for palatable fruits during breeding of domesticated tomato," the researchers noted.

The researchers also zoomed in on specific plant tissues — a panel of six tissue types including root, vegetative, and floral tissues — to examine expression changes particular to those locales. From this, they identified 166 transcripts whose expression pattern across the tissues varied between the species.

From their characterizations of the various tomato lineages, the investigators noted that they found hundreds of thousands of markers that distinguish domesticated varieties from their wild cousins. Those wild lineages could be used as a source of introgression for improving tomato crop, investigators said.

"All of these species have individual attributes that could be potentially valuable for tomato crop improvement, and our study provides the raw material necessary for marker-assisted introgression of such traits," they added.