Hidden DNA mutations in tomatoes revealed in genetic study of 100 varieties


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After centuries of breeding, tomatoes now come in all shapes and sizes, from cherries to large heirloom fruits. Scientists are trying to determine at the gene level how and why these physical changes occur. Credit: Lippman Lab / CSHL / HHMI

Human appetites transformed the tomato – DNA and all. After centuries of breeding, what was once a South American berry roughly the size of a pea now comes in all shapes and sizes, from cherries to large, ancient fruit.

Today, scientists are discovering how these physical changes manifest at the level of genes – work that could guide modern efforts to refine the tomato, says Zachary Lippman, a researcher at Howard Hughes Medical Institute.

He and his colleagues have now identified hidden mutations long hidden in the genomes of 100 types of tomatoes, including a wild, orange-berry plant from the Galapagos Islands and varieties typically made into ketchup and sauce.

Their analysis, described on June 17, 2020, in the journal Cell, is the most comprehensive assessment of these mutations – which alter long sections of DNA – for any plant. The research could lead to the creation of new tomato varieties and the improvement of existing varieties, Lippman says. A handful of the mutations his team identified alter key characteristics, such as flavor and weight, the researchers showed.

Previous studies have long shown that these mutations exist in plant genomes, says Lippman, a plant geneticist at the Cold Spring Harbor Laboratory. “But until now, we haven’t had an effective way to find them and study their impact,” he says.

A window on the genome

Mutations or changes in the four types of DNA letters carried in an organism’s cells can alter its physical characteristics. Scientists who study plants have typically focused on a small type of treatable mutation, in which one letter of DNA is swapped for another.

The mutations studied by Lippman’s team are much larger – they alter the structure of DNA by copying, deleting, inserting, or moving long sections of DNA elsewhere in the genome. These mutations, also called structural variations, occur in everyone living. Studies in humans, for example, have linked these variations to disorders such as schizophrenia and autism.

Tomato size

Researchers have shown that structural variation – in this case the copy number of a gene – can alter fruit. Plants with three gene copies (left) produced fruit 30 percent larger than those with one (right). Credit: M. Alonge et al./Cell 2020

Scientists can identify mutations by reading the letters in DNA using a technique known as genetic sequencing. However, the limitations of this technology have made it difficult to decode long sections of DNA, Lippman explains. The researchers were therefore not able to capture a full picture of structural mutations in the genome.

Even so, plant breeders have suspected that these mutations contribute significantly to the characteristics of the plants, says Michael Purugganan, who studies rice and date palms in New York University and was not involved in the new study. “This is why this article is so fascinating,” he says. Lippman’s team not only found these mutations in the tomato and its wild relatives, but also determined how they work in plants, he says.

A guide to future tomatoes

The new study, a collaboration with Michael Schatz of Johns Hopkins University and others, has identified more than 200,000 structural mutations in tomatoes using a technique called long-read sequencing. Lippman likens it to looking through a panoramic window of large sections of the genome. By comparison, more conventional sequencing only offered a peephole, he says.

The majority of the mutations they found do not alter the genes that encode the traits. But what is clear, says Lippman, is that many of these mutations alter the mechanisms controlling gene activity. Such a gene, for example, controls the size of tomato fruits. By altering the structure of DNA – in this case, the copy number of the gene – Lippman’s team were able to alter fruit production. Plants lacking the gene never produced fruit, while plants with three copies of the gene produced fruit about 30 percent larger than those with a single copy.

Lippman’s team also demonstrated how DNA structure can influence traits in an example he calls “remarkably complex.” They showed that four structural mutations were needed to replicate a major harvest trait in modern tomatoes.

These types of information could help explain the diversity of traits in other crops and allow breeders to improve varieties, Lippman says. For example, maybe adding an extra copy of the size gene to tiny ground cherries, a close relative of the tomato, could increase their appeal by making them larger, he says.

“One of the holy grails of agriculture is being able to say, ‘If I mutate this gene, I know what the result will be,’” he says. “The estate is taking important steps towards this predictable type of breeding.”

Reference: “Major impacts of generalized structural variation on gene expression and crop improvement in tomato” by Michael Alonge, Xingang Wang, Matthias Benoit, Sebastian Soyk, Lara Pereira, Lei Zhang, Hamsini Suresh, Srividya Ramakrishnan , Florian Maumus, Danielle Ciren, Yuval Levy, Tom Hai Harel, Gili Shalev-Schlosser, Ziva Amsellem, Hamid Razifard, Ana L. Caicedo, Denise M. Tieman, Harry Klee, Melanie Kirsche, Sergey Aganezov, T. Rhyker Ranallo-Benavidez , Zachary H. Lemmon, Jennifer Kim, Gina Robitaille, Melissa Kramer, Sara Goodwin, W. Richard McCombie, Samuel Hutton, Joyce Van Eck, Jesse Gillis, Yuval Eshed, Fritz J. Sedlazeck, Esther van der Knaap, Michael C. Schatz and Zachary B. Lippman, June 17, 2020, Cell.
DOI: 10.1016 / j.cell.2020.05.021

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