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Tomato Structural Variations Linked to Gene Expression, Traits

NEW YORK – Structural variants may influence a variety of tomato traits, such as whether a tomato is small or large, or has a smoky flavor, according to a new study.

A team led by researchers at Johns Hopkins University and Cold Spring Harbor Laboratory analyzed the genomes of 100 different tomato varieties using long-read nanopore sequencing to dig into the structural variants they contain. Tomatoes are a key fruit crop and represent a $190 billion global industry, and structural variants appear to underpin many of the variations — shape, color, and taste — observed in tomatoes.

As they reported Wednesday in the journal Cell, the researchers uncovered more than 230,000 structural variants, some of which appear to influence tomato gene expression and, in turn, tomato traits, including ones sought by farmers. 

"There was a whole massive amount of natural genetic variation that we were blind to. And the only way to get at it was through this new technology," Cold Spring Harbor's Zachary Lippman said in a statement. "[Structural variation] was probably being grossly underestimated in terms of its importance. So we really just needed to walk through that door. And the only way to do it was to do it at scale with a hundred different genomes."  

Using Oxford Nanopore long-read sequencing, the researchers generated a minimum 40X coverage for 100 tomato accessions. These varieties represented a wide swath of tomato diversity and included the closest relatives of wild tomatoes as well as early domesticated and modern domesticated tomatoes. The researchers were able to sequence the 100 tomato genomes in 100 days, as Johns Hopkins' Michael Schatz noted in a 2019 Plant and Animal Genomes conference presentation of early findings from the analysis.

They aligned the reads to the Heinz 1706 tomato reference genome and called structural variations using the algorithm Sniffles to uncover a total 238,490 SVs. Most accessions had between 1,928 and 45,840 SVs. 

Previous studies have implicated structural variants in crop traits, and the researchers reported that about half the SVs they uncovered overlap with genes or gene regulatory sequences. In the more than 21,000 SV-gene pairs they analyzed, they uncovered hundreds of significant changes to expression. 

In particular, the researchers examined SVs affecting genes associated with fruit weight, an increase in which was a key part of tomato domestication. Using CRISPR-based tools, they found that duplications of the KLUH gene led tomatoes to increase in fruit size by about 30 percent.

Previously, mutations in the NSGT1 and NSGT2 genes — short for non-smoky glycosyltransferase — and the candidate gene E8 have been linked to the accumulation of guaiacol and tomato taste. Within their dataset, the researchers uncovered five haplotypes affecting these genes — including ones affected by duplications and deletions in addition to coding sequence alterations — suggesting multiple mutations can affect guaiacol accumulation and the smoky flavor of tomatoes.

Additionally, the researchers uncovered a complex interaction of four structural variants that affect three transcription factors that influence the ease of tomato harvesting and affect tomato productivity. 

By identifying the SVs involved in these traits, tomato breeders could use them as guides for engineering future tomatoes.

The work lays the foundation for similar studies in other crops, Lippman added. "All crops are based on mutations. Everything that we eat is based on mutations and up until now it's been [a] pretty slow process to identify and evaluate the importance of those mutations," he said. 

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