You say tomato, these scientists say evolutionary mystery

Biologists at the University of Massachusetts Amherst have found evidence for evolutionary "syndromes" -- sets of traits that occur together -- that help to explain how tomatoes first evolved their distinctive blend of color, sweetness, acidity and aroma. The research, represented by a pair of papers recently published in Plants People Planet and The American Journal of Botany, not only shines a light on how fruits evolve in the wild, but will also be valuable 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?" asks Jacob Barnett, graduate student in organismic and evolutionary biology at UMass Amherst and the papers' lead author. It turns out that the juicy, red tomatoes with their unique flavor have a long and circuitous evolutionary history.

Barnett and his co-authors, including Ana Caicedo, professor of biology at UMass Amherst, turned to the relatives of our modern tomatoes, a group of several wild species growing in the western coast of South America, from Chile to Ecuador, to explore this question. And 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?

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. But evidence of evolutionary syndromes in wild tomatoes has been hard to gather, because no previous researchers had grown all the species of wild tomatoes together at the same time.

"These two studies are the first to look at fruit traits across all species in the entire tomato group," says Caicedo. "We have been able to tell a comprehensive story of how wild tomatoes compare to each other and to our modern, cultivated varieties."

Part of that story involves the collecting efforts of Charles Rick, from the University of California Davis, who 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 seeds from multiple variants within each species, and then grew them at the UMass Crop and Animal Research and Education Farm in South Deerfield, Massachusetts.

When mature, the plants were "wild and scraggly," says 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 and analyzed the DNA in the leaf samples. With the help of co-author Denise Tieman, research assistant professor at the University of Florida, Barnett measured and classified each sample's volatile organic compounds -- the chemicals responsible for tomatoes' smell.

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

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Being in nature: Good for mind, body and nutrition

In late 2020, Canadian doctors made headlines for "prescribing nature," or recommended time outdoors based on research that suggests people who spent two or more hours in nature per week improved their health and wellbeing. Knowing this, transdisciplinary researchers from Drexel University investigated how nature relatedness -- simply feeling connected with the natural world -- benefits dietary diversity and fruit and vegetable intake, in a study recently published the American Journal of Health Promotion.

"Nature relatedness has been associated with better cognitive, psychological and physical health and greater levels of environmental stewardship. Our findings extend this list of benefits to include dietary intake," said Brandy-Joe Milliron, PhD, an associate professor in Drexel's College of Nursing and Health Professions and lead author of the publication. "We found people with higher nature relatedness were more likely to report healthful dietary intake, including greater dietary variety and higher fruit and vegetable consumption."

The research team surveyed over 300 adults in Philadelphia to measure their self-reported connection to nature, including their experience with and perspective of nature, and the foods and beverages they had consumed the previous day to assess their dietary diversity and estimate their daily fruit and vegetable consumption. Survey participants mirrored demographic characteristics (gender, income, education and race) of Philadelphia, as of the 2010 census. The data were collected between May and August 2017. The results of the survey showed that participants with a stronger connection to nature reported a more varied diet and ate more fruits and vegetables.

"This work can impact health promotion practices in two ways," said Milliron. "First, nature-based health promotion interventions may increase nature relatedness across the lifespan and potentially improve dietary intake. And second, augmenting dietary interventions with nature-based activities may lead to greater improvements in dietary quality."

The research team added that these findings highlight the potential for leveraging nature-based experiences or interventions such as incorporating green spaces or urban greening into city planning, integrating nature- and park-prescription programs into healthcare practices (similar to the Canadian model) and promoting nature-based experiences in the classroom settings, among many others.

But, the researchers noted, while improving dietary intake through nature-based interventions may be valuable, it is also complex.

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‘Battle of the sexes’ begins in womb as father and mother’s genes tussle over nutrition

Cambridge scientists have identified a key signal that the fetus uses to control its supply of nutrients from the placenta, revealing a tug-of-war between genes inherited from the father and from the mother. The study, carried out in mice, could help explain why some babies grow poorly in the womb.

As the fetus grows, it needs to communicate its increasing needs for food to the mother. It receives its nourishment via blood vessels in the placenta, a specialised organ that contains cells from both baby and mother.

Between 10% and 15% of babies grow poorly in the womb, often showing reduced growth of blood vessels in the placenta. In humans, these blood vessels expand dramatically between mid and late gestation, reaching a total length of approximately 320 kilometres at term.

In a study published today in Developmental Cell, a team led by scientists at the University of Cambridge used genetically engineered mice to show how the fetus produces a signal to encourage growth of blood vessels within the placenta. This signal also causes modifications to other cells of the placenta to allow for more nutrients from the mother to go through to the fetus.

Dr Ionel Sandovici, the paper's first author, said: "As it grows in the womb, the fetus needs food from its mum, and healthy blood vessels in the placenta are essential to help it get the correct amount of nutrients it needs.

"We've identified one way that the fetus uses to communicate with the placenta to prompt the correct expansion of these blood vessels. When this communication breaks down, the blood vessels don't develop properly and the baby will struggle to get all the food it needs."

The team found that the fetus sends a signal known as IGF2 that reaches the placenta through the umbilical cord. In humans, levels of IGF2 in the umbilical cord progressively increase between 29 weeks of gestation and term: too much IGF2 is associated with too much growth, while not enough IGF2 is associated with too little growth. Babies that are too large or too small are more likely to suffer or even die at birth, and have a higher risk to develop diabetes and heart problems as adults.

Dr Sandovici added: "We've known for some time that IGF2 promotes the growth of the organs where it is produced. In this study, we've shown that IGF2 also acts like a classical hormone -- it's produced by the fetus, goes into the fetal blood, through the umbilical cord and to the placenta, where it acts."

Particularly interesting is what their findings reveal about the tussle taking place in the womb.

In mice, the response to IGF2 in the blood vessels of the placenta is mediated by another protein, called IGF2R. The two genes that produce IGF2 and IGF2R are 'imprinted' -- a process by which molecular switches on the genes identify their parental origin and can turn the genes on or off. In this case, only the copy of the igf2 gene inherited from the father is active, while only the copy of igf2r inherited from the mother is active.

Lead author Dr Miguel Constância, said: "One theory about imprinted genes is that paternally-expressed genes are greedy and selfish. They want to extract the most resources as possible from the mother. But maternally-expressed genes act as countermeasures to balance these demands."

"In our study, the father's gene drives the fetus's demands for larger blood vessels and more nutrients, while the mother's gene in the placenta tries to control how much nourishment she provides. There's a tug-of-war taking place, a battle of the sexes at the level of the genome."

The team say their findings will allow a better understanding of how the fetus, placenta and mother communicate with each other during pregnancy. This in turn could lead to ways of measuring levels of IGF2 in the fetus and finding ways to use medication to normalise these levels or promote normal development of placental vasculature.

The researchers used mice, as it is possible to manipulate their genes to mimic different developmental conditions. This enables them to study in detail the different mechanisms taking place. The physiology and biology of mice have many similarities with those of humans, allowing researchers to model human pregnancy, in order to understand it better.

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