Tomato’s evolution took several turns

Researchers discover more to the vegetable’s development than the previously believed two-step evolutionary process

For decades it was thought that tomatoes became domesticated in a two-step process.

This oversimplified view involved the transition of the small, wild blueberry-sized tomato Solanum pimpinellifolium L to an intermediate fruit and then to the fully domesticated, cultivated tomato. But there were missing links.

Tomatoes are one of the world’s most consumed, highest valued and most widely grown vegetable crop making it an important model for studying fruit and vegetable development.

According to the Food and Agriculture Organization (FAO), world production of tomatoes in 2017 was nearly 183 million tonnes. The largest producer was China accounting for nearly 33 percent of global production. However, Mexico was the world’s largest exporter of tomatoes, exporting a dollar value of $2.3 billion in 2018.

Understanding the evolution of the tomato has been a mystery. Now, researchers at the University of Massachusetts Amherst have identified those missing links in the tomato’s evolution showing in the study that there were a number of intermediate variants between the fully wild and the fully domesticated plant.

The study indicates that the modern tomato is most closely related to a weed-like tomato still found in Mexico rather than the semi-domesticated, intermediate types found in South America.

In Mexico, the tomato weed grows in milpas, which are fields where farmers plant many different crops in the same area. The wild tomato is not bred by local farmers although they can be used as local, casual food source.

“We started the study with the idea that we had a more thorough sampling of the intermediate stage in tomato (Solanum lycopersicum var. cerasiforme or SLC) domestication than had previously been examined, and that this was going to allow us to more precisely trace the tomato’s domestication path,” said Ana Caicedo, associate professor in the university’s biology department.

“However, once we started examining the traits of these SLC, we were startled to discover large differences between SLC found in Mesoamerica and SLC found in South America. Specifically, Mesoamerican SLC had more wild-like phenotypes even though they are the closest relatives to the fully domesticated tomato. This was unexpected and was the basis for the discovery that tomato’s domestication had not involved a linear and steady growth in size as had been previously portrayed.”

She said that the ancestors of today’s cultivated tomatoes originated in Peru-Ecuador some 80,000 years ago where it eventually, and naturally, gave rise to an intermediate form.

Much later, when people populated the region, the tomato became a food source and they likely came to depend on it, in the process selecting it for certain traits similar to the desired traits in modern medium-size tomatoes. Over time, people moved northward, taking some of these intermediate subgroups of tomatoes with them into Central America and Mexico, likely as a weedy companion to other crops. Some 7,000 years ago, further human selection on these tomatoes in Mesoamerica gave rise to modern tomatoes.

“Our genetic data cannot tell us how they spread from South America to Mesomerica,” she said. “Given that wild tomatoes existed in South America for a long time and no fully wild species has spread north, as well as the fact that most SLC in Mesoamerica are currently found in areas that have been disturbed by humans, we believe it is likely that humans spread them. Our data suggests that SLC arose about 80,000 years ago, which implies it was a natural event and involved natural selection. But we cannot be sure what the traits of those first SLC looked like. The descendants of those SLC that are currently found in Ecuador and Peru have traits that are consistent with the domestication syndrome and this is likely due to human selection.”

According to a news release, researchers used whole-genome sequencing of wild, intermediate and domesticated varieties, as well as population genomic analyses to reconstruct tomato domestication. They focused on evolutionary changes especially in the intermediate stages and generated new whole-genome sequences for 166 samples. They paid special attention to the intermediate variants from their native ranges and cultivated tomatoes from Mexico.

The researchers said that exploring intermediate stages of tomato domestication has direct implications for crop improvement.

“We think this is possible,” said Caicedo. “These northern SLC groups, for example, have higher levels of sugar, which could be mined for crop improvement of modern cultivated tomato. We believe that there are likely to be other traits of value in these populations. Both drought and disease resistance would be of great interest, although in this study we only evaluated (existing) traits.”

But in the complexity of all the intermediate stages of the tomato’s natural evolution, valuable genetics could have been lost.

“Any time there is a domestication event there is a narrowing of the genetic pool,” she said. “Thus, all ancestral and intermediate stages can be valuable resources for traits that did not make it into the modern domesticated tomato gene pool. This is why it is so crucial to conserve the wild and semi-wild relatives of cultivated species.”

The research was published in an advanced access edition of Molecular Biology and Evolution.

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