Tomatoes: From the ancient wilds to the modern table

Israelis have voted tomatoes as their favorite type of produce, and are willing to try any size, shape, or color – even though crop losses during heatwaves have often made them very expensive.

Now, biologists at the University of Massachusetts at Amherst have found evidence for evolutionary “syndromes” – sets of traits that occur together – that help explain how tomatoes first evolved their distinctive blend of color, sweetness, acidity, and aroma.

While the layman generally regards the tomato as a vegetable, scientists classify it as a fruit because it is the fleshy part of the plant surrounding its seeds, and because it grows from the flower of the plant.

The research, published in The American Journal of Botany under the title “Variation in ripe fruit volatiles across the tomato clade: An evolutionary framework for studying fruit scent diversity in a crop wild relative,” not only explains how fruits and vegetables evolve in the wild, but will also contribute to crop-improvement efforts aimed at breeding more nutritious and appealing varieties of fruits.

“Have you ever held a fresh tomato in your hand and wondered why it looks good, smells good, and tastes delicious?” asked Jacob Barnett, a graduate student in organismic and evolutionary biology at the university and the paper’s lead author. “It turns out that the juicy, red tomatoes with their unique flavor have a long and circuitous evolutionary history.”

For fleshy-fruited plants, the scents of volatile organic compounds (VOCs) in ripe fruits are generally thought to help attract seed dispersers by making mature fruits noticeable and appealing to animal consumers, while also aiding in defense against pathogens and seed predators.

To explore this, Barnett and his co-authors, including biology Prof. Ana Caicedo, studied relatives of our modern tomatoes – a group of several wild species growing in the western coast of South America, from Chile to Ecuador. They discovered that those wild species are nothing like what you’d find in your sandwich or salad today.

“For one thing, they’re tiny,” says Barnett, “about the size of a blueberry. And most of them are green when ripe. Many smell like apples, melons, or even cucumbers, and a number of them taste terrible.” So how did we get from a tiny, green, terrible-tasting, melon-smelling fruit to the sublime blend of color, sweetness, acidity, and umami that makes tomatoes so beloved in pasta sauces, salads, and pizzas?

Traits develop together, stay together

It turns out that fruits in the wild tend to have sets of traits that occur together, which biologists call syndromes. For example, many fruits are small, brightly colored, and high in sugar. However, evidence of evolutionary syndromes in wild tomatoes has been hard to collect because no previous researchers had grown all the species of wild tomatoes together at the same time.

“The study is the first to look at fruit traits across all species in the entire tomato group,” claimed Caicedo. “We have been able to tell a comprehensive story of how wild tomatoes compare to each other and to our modern, cultivated varieties.”

Charles Rick of the University of California at Davis traveled through South America in the 1950s and 1960s collecting seeds from wild species and bringing them back to what would become the C.M. Rick Tomato Genetics Resource Center. Barnett and Caicedo acquired seeds from 13 species of wild tomato, as well as some from multiple variants within each species, and then grew them at the University of Massachusetts’ Mass Crop and Animal Research and Education Farm.

When mature, the plants were “wild and scraggly,” recalled Caicedo, and at one point Barnett had to hack his way through them with a machete on his way to gathering their fruits and leaves. Back in the lab, the team scanned the fruits for color and shape, measured sugar and acid content, analyzed the DNA in the leaf samples, and classified each sample’s volatile organic compounds – the chemicals responsible for the tomatoes’ smell.

Not only did the team discover that smell, flavor, and color are syndromatic but also that there is what Barnett calls an “honest signal” – a match between the outside appearance of the tomato and the nutritional content inside. This match supports a controversial hypothesis that animal preferences shaped the evolution of fruit, because animals will choose some fruits over others if they learn to associate the fruit’s looks with its unique nutrient reward.

The small, green, melon-smelling fruit may be preferred by small mammals, while the sweet, colored tomatoes are likely the favorites of birds. How humans wound up preferring tomatoes loved by birds is a mystery yet to be unraveled. Indeed, as the authors point out, we need more in-the-field studies to confirm which animals are eating which fruits: “There is currently no systematic data on which animals eat wild tomato fruits.”