A genetic mutation introduced into tomatoes to make them ripen more uniformly might have inadvertently reduced some of the sugar content that makes them taste good, a team of researchers from the U.S., Spain and Argentina have found.

In traditional and heirloom tomatoes, the green colour of an unripe fruit is not uniform, with darker shades of green concentrated around the stem and lighter shades at the bottom. That means by the time they arrive on store shelves, they are equally unevenly coloured — though in shades of red, not green.

Beginning about 70 years ago, however, tomato growers, together with breeders and seed companies, tried to remedy this uneven colouring by creating varieties of tomatoes that are a uniform light green at the time of harvesting and that ripen to an evenly distributed red en route to the grocery store.

'By having a uniform colour when they're green, it's easier to look at a field of tomatoes and see how mature they are.'— Ann Powell, plant scientist

Their intentions were not entirely aesthetic and had much to do with improving harvesting techniques, said University of California Davis plant scientist Ann Powell, the lead author of the study, published online Thursday in the journal Science.

"By having a uniform colour when they're green, it's easier to look at a field of tomatoes and see how mature they are — the entire surface of the fruit is one colour, and that colour is actually a little bit lighter than the leaves. So it's a little bit easier to say, 'Oh, OK, these guys are at this stage, and we need to harvest in three days'," Powell said.

But what Powell and her colleagues found is that by manipulating the gene responsible for the intensity and pattern of the green colour in unripe tomatoes, the breeders inadvertently disabled a protein that regulates that gene and helps optimize photosynthesis.

The elimination of the protein got rid of the dark green colour around the stem that growers didn't want, but it also reduced the amount of sugars and lycopene (an antioxidant responsible for a tomato's bright-red colour and that has possible health benefits), which are produced during photosynthesis.

Chloroplasts key to tasty tomatoes

To reach their conclusions, Powell and her colleagues first narrowed down which gene was behind the uniform light green colouring of modern cultivated tomatoes by using the recently sequenced tomato genome and by crossing wild and cultivated tomato varieties.

An unripe and ripe unevenly coloured traditional tomato, left, and one that has been mutated to select for a uniform colour distribution. (Image courtesy of C. Nguyen and J. Giovannoni)

They then found that, key to the proper functioning of that gene, called SlGLK2, was a protein or transcription factor that ensures the gene produces the most optimal and robust chloroplasts in the leaves and fruit of the tomato plant.

Chloroplasts are the specialized parts of plant cells where photosynthesis takes place. They contain the chlorophyll pigment that with the help of light and water creates the green colour of unripe fruit and produces the sugars that accumulate in the tomato as it ripens and that contribute to its flavour.

"Making a chloroplast, there's lots of parts to it, so the transcription factor will make sure that everybody shows up in the right amount on the right day in the right place to get the whole chloroplast put together," Powell said.

That didn't happen when the protein was disabled in the mutated gene and, as a result, the chloroplasts in the tomato fruit were fewer in number, smaller and less effective, producing fewer sugar and lycopene molecules.

Bulk of sugar comes from leaves

Breeders who created the mutation had little reason to suspect their manipulations would affect taste, Powell said, since the bulk of sugars in the tomato are produced during photosynthesis in the leaves, not the fruit, and are only later transferred to the fruit.

"The breeders didn't deliberately set out to change the sugars," Powell said. "This was a trait that had to do with the fruit when they were green, and there was really not any good reason that it would make much difference for ripe fruit, because everybody knew that most of the sugars in the fruit come from photosynthesis in the leaves."

A basket of ripe heirloom tomatoes shows a diverse range of colour. (Image courtesy of Ann Powell)

The mutated tomatoes still get their fair share of sugars since photosynthesis is still taking place in the leaves, and since the leaves have a second copy of the colour gene that is still able to synthesize the protein.

"In the tomato leaf — just like every other leaf — there are two genes, GLK1 and GLK2, and they are redundant. So in most leaves, you can knock out one of them, and the other one picks up the slack, and everything goes along just fine," Powell said.

"What was surprising was to see in green fruit, that, in fact, only one of them was expressed so, therefore when that one was knocked out, nobody was there to pick up the slack."

No guarantee of better taste

The research suggests that by increasing the levels of the protein in the tomato fruit, breeders may be able to get chloroplast production back on track and increase the amount of sugars produced and improve taste.

But Powell warns that there are many factors other than sugar that determine the flavour of a tomato. In that sense, the researchers' findings won't automatically translate into better-tasting tomatoes at the supermarket.

"Flavour is a very complex process," she said "There are many, many compounds in tomatoes that contribute to flavour …[and] flavour is also strongly influenced by how the tomatoes are grown — if they're grown in large production settings, if they're grown with certain fertilizer regimes or watering schemes … and, in fact, that sort of environmental condition of how the tomato is grown may trump whatever genetic changes are influencing flavour, too.

"So, this is not at all going to make an instant cure for making good-flavoured tomatoes, but it probably is one of the contributors to making tomatoes more flavourful."

An ideal solution, Powel said, might be to find a way to manipulate the protein levels so that they produce a uniform dark green tomato, which would still give growers the benefit of easily spotting when fruit is ready to harvest but would also taste good.

Upping the amount of GLK protein in tomatoes might also be useful in the tomato processing industry, which requires processed tomato products to have high sugar content.

"If you start off with tomatoes that have more sugars to begin with, then these companies have to do less cooking, less handling. It's cheaper and less energy input," Powell said.