Nov 14, 2013
OSU clones gene that regulates tomato size

There is a good reason tomatoes can grow to be large and plump. Ohio State University crop scientists are pointing to a gene that took hold thousands of years ago, when farmers in South America began domesticating the popular fruit.

Esther van der Knaap, a geneticist with the university’s College of Food, Agricultural, and Environmental Sciences, led an international research team that discovered and cloned a gene that regulates fruit size in tomato. This is only the second domestication gene involved in size ever cloned in any vegetable or fruit crop.

She said the researchers recently determined that commercial lines of tomatoes already have the large version of the gene.

“This means that fruit size cannot be improved in most modern tomatoes,” van der Knaap said. “However, the story is different for grape and cherry tomatoes. In that case, the fruit weight gene could be replaced by another fruit weight gene, because we don’t want to select giant grape tomatoes (we prefer them small).

“For this fruit weight gene, ripening is delayed, which could be a negative aspect. In addition, the architecture of the plant is impacted as well. Breeders now have a choice to get larger fruit or a more branched plant that ripens earlier. This information could all be implemented immediately.”

The gene discovery was reported Sept. 30 in the Proceedings of the National Academy of Sciences.

“This work represents an important improvement in the understanding of the regulation of fruit size and how domestication played a role in the selection of this gene,” said van der Knaap, who is based on the Wooster campus of the Ohio Agricultural Research and Development Center (OARDC), the research arm of the college.

“We identified a gene that controls fruit size in tomato and possibly pepper,” van der Knaap confirmed. “The findings revealed that the allele (version of a gene) that makes larger fruit arose early during the domestication of tomato and became gradually fixed in modern tomatoes.”

The researcher said that, from publications by a few of the co-authors of this work, it is now believed that the tomato was domesticated in two waves: in South America, mainly in northern Peru and Ecuador, and in Central America.

“This knowledge is based on extensive genetic characterizations of tomato and its closest wild relatives,” she said. “Once you know where each tomato accession is from and how each fits within its evolutionary history, you can ask where a certain mutation occurred, in which subsample of the tomatoes. This information provides a trajectory of where the mutation arose and how it spread through the germplasm. It also gives us confirmation of the direction of domestication as we assume that, over time, larger tomato fruit were selected.”

Domestication of crop plants some 10,000 years ago had a significant effect on the development of humans and their societies. However, even today, van der Knaap acknowledged, scientists know little about the molecular mechanisms involved in changes in fruit appearance – size, shape and other factors – as a result of domestication and selection by early farmers.

“Despite the importance of fruit mass in the evolution of fruit and vegetable plants, cloning of domestication genes of fruit and vegetable crops has lagged behind that of cereal crops,” van der Knaap said. “For that reason, insights into the molecular mechanisms that led to the transition of the fruit from small to large remain mostly unknown.

“Fruit size is a trait that is controlled by many genes,” she said. “It is a so-called ‘quantitative trait.’ That means if you are interested in following up on one gene at the time, you have to make sure that the other genes don’t interfere. This means you have to develop lines by genetics and further selections before you can go after the chosen gene. This takes about two years, and then you can start the actual cloning effort.

“In general, funding for vegetable and fruit research is quite limited, especially when compared to soy, corn and rice research,” van der Knaap said. “Without funding, these projects cannot be undertaken. We are fortunate that we have gotten funding from the National Science Foundation for the broad scope of our tomato fruit shape and size research. That means that this project is a part of a larger funded project.”

Van der Knaap said the cloned gene, known as SlKLUH, impacts fruit size by increasing cell layers and delaying ripening. This gene promotes extra cell divisions during the process of fruit development, immediately after fertilization. These extra cell divisions lead to enlarged fruit, while the delay in ripening is likely the result of an extension of the cell division stage.

“After flower opening and fertilization of the ovules (those will become seeds), the developing fruit will undergo a stage of cell division, followed by a stage of cell size increase,” she said. “The increase in cell sizes ceases right before ripening of the fruit starts. We identified a gene that controls the number of cell layers. We assume that this means the gene impacts cell division (two extra divisions).

“We now hypothesize that if cell division is extended, fruit ripening is delayed. Basically, the fruit is not ready for ripening until the cell divisions and enlargements have been completed.”

She said larger fruit size could have a significant impact on the marketability and profitability of produce in the future.

“For beefsteaks, the consumers want the largest tomato fruits,” she said. “For processing tomatoes, the producers want larger fruit. It is clear that slightly larger tomato fruit is desired for nearly all market classes. Our discovery does not immediately impact this issue, but it is a step in the direction of going after those genes that have not been found yet and those that would lead to crop improvement.”

The research team also identified a potential regulatory element in the promoter of SlKLUH, which is hypothesized to control gene expression. The promoter is a region of DNA that is responsible for initiating the transcription of a gene.

The cloning of SlKLUH is expected to increase scientists’ understanding of fruit development processes, not only in tomato but in other crop species as well.

“We show in this paper that the same gene may have been selected during domestication of chili pepper, leading to increased fruit size in this vegetable crop as well,” van der Knaap said.

A majority of the research was conducted by Ohio State postdoctoral researcher Manohar Chakrabarti and Ph.D. student Na Zhang, working in van der Knaap’s lab. Other scientists in the United States, France and Spain collaborated as well.

Gary Pullano

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