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Study Examines Influence of Tomato Domestication, Improvement on its Genome

NEW YORK (GenomeWeb) – An analysis of the genomes of some 360 accessions of tomato has given researchers a glimpse into tomato domestication and improvement.

Researchers from the Chinese Academy of Agricultural Sciences and elsewhere reported in Nature Genetics yesterday that tomato domestication involved two different sets of quantitative trait loci that resulted in the domesticated tomato being some hundred times larger than its wild forbearers. Additionally, they uncovered a genomic signal identifying modern tomatoes bred for processing as well as the variant that underlies pink tomatoes, which are popular in Japan and China.

"The genomic foundation for modern tomato breeding was shaped by human-involved selection, as illustrated in [our] study," Chinese Academy of Agricultural Sciences' Sanwen Huang and his colleagues wrote in their paper. "Despite their historical contribution to desirable phenotypic traits, these human-induced processes also resulted in the near fixation of a large proportion of the tomato genome."

Tomatoes, Solanum lycopersicum, are a leading crop, the researchers noted, with a global yield in 2012 of 162 million tons valued at more than $55 billion.

They and their wild relatives originated in the Andean region of South America where they were likely domesticated before spreading throughout the world.

To reconstruct the genomic history of tomato breeding, Huang and his colleagues analyzed the genomes of 360 different tomato accessions, including 33 accessions from the red-fruited clade, 10 wild species, and 17 modern commercial hybrids.

Resequencing these accessions using the Illumina HiSeq 2000 to a median depth of 5.7x and aligning them to the tomato reference genome yielded 11.6 million SNPs and 1.3 small indels. The researchers also noted more than 207,000 nonsynonymous SNPs in nearly 31,000 genes, including nonsense SNPs in 7,680 genes that lead to codon changes. This set of SNPs, Huang and colleagues said, could be a resource for future tomato breeding work.

Using a neighbor-joining approach, the researchers developed a phylogenetic tree to examine relationships among the various accessions. The tree, they noted, clustered the red-fruited accessions together, as expected. They further divided that cluster into three groups based on morphological characteristics like fruit weight — PIM, CER, and BIG.

Additional model-based clustering analysis divvied the CER cluster in two, with one group of accessions from South America showing evidence of admixture while the other group of non-South American accessions was homogenous with the BIG group. The BIG group itself included a cluster of processing tomatoes.

Through these analyses and an examination of linkage disequilibrium decay between the three groups, Huang and his colleagues determined that the PIM group was the ancestor of the red-fruited clade and the CER group, and the CER group was an intermediary between the PIM and BIG groups. They also estimated that tomatoes had an effective population size of about 300 when they were domesticated.

To search for QTLs linked to domestication and fruit size — a trait for which humans commonly select — Huang and his colleagues searched for genomic regions of reduced nucleotide diversity in the CER lines as compared to the smaller PIMs and between the CERs and the larger BIGs. From this, they found 186 domestication sweeps and 133 improvement sweeps.

Five QTLs, the researchers reported, linked to fruit mass were part of the domestication sweep and likely influenced the increased size of CERs as compared to PIMs. Meanwhile, the researchers found more than a dozen other QTLs within the improvement sweeps that likely affected the change in size between the CER and BIG accessions.

One of the genes implicated in this enlargement during the improvement of the tomato crops was fw2.2, which, the researchers noted, controls carpel cell number.

Additionally, by sequencing two bulk populations of extreme tomato size, the result of crosses between CER and BIG lines, they identified four genomic regions linked to fruit size, all of which overlapped with the previously identified improvement sweeps.

"[W]e propose a two-step evolution of fruit mass that involved two different sets of loci, which jointly gave rise to modern tomatoes about 100 times larger in fruit size than their wild ancestor," the researchers said.

While most tomatoes were bred for eating fresh, some were destined for processing into tomato paste. These processing tomatoes, the researchers said, harbor a specific set of QTLs on chromosome 5 linked to higher soluble solid content and fruit firmness. The selection of these QTLs, they noted, appears to have also led to the hitchhiking of most of chromosome 5, which they said was a signature of the modern processing tomato.

Huang and his colleagues also examined the genetic source of pink-fruited tomatoes. Previous studies, they noted, implicated SIMYB12 on chromosome 1, which controls the accumulation of yellow-colored flavonoids in tomato skins, but not the causative variant.

Here, they found a strong signal more than 8,000 base pairs upstream of the SIMYB12 start codon — most, though not all, of the pink-fruited tomatoes had a 603 base-pair deletion there. The four pink-fruited accessions lacking the deletion had other mutations in the region.

"We hypothesize that the deletion might impair the transcription of SlMYB12, whose expression is silenced in pink fruits," Huang and his colleagues said.

Recent improvements to tomato crops that drew on wild introgressions have also left their mark on the tomato genomes. For instance, Huang and his colleagues reported finding a large chromosome 9 fragment that carries the resistance gene to the tomato mosaic virus and two introgression spots on chromosome 6 carrying root knot nematode and tomato yellow leaf curl virus resistance genes.

Though a preponderance of the tomato genome has been affected — some 25 percent by the researchers' calculations — by domestication and improvements sweeps and introgressions, they said that their map could enable further improvement of tomato crops by uncoupling genes for favorable traits from the sweeps and linkage drags in which they are embedded.

"These efforts should enable a redesign of the genomic foundation for future tomato breeding," the researchers added.

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