The hidden molecular mechanism of tomato: Green → yellow → red!

Hirokazu Kobayashi

CEO, Green Insight Japan, Inc.

Professor Emeritus and Visiting Professor, University of Shizuoka

Is a tomato a fruit or a vegetable? This question, which sparked the Nix-Hedden Trial in 1893, has significantly shaped our perception of tomatoes. The United States imposed tariffs on imported vegetables, but fruits were exempt. The United States Supreme Court ruled that the tomato was a "vegetable." This historical context is crucial to understanding the journey of tomatoes. When I was a child in the 1960s, tomatoes were a summer staple in Japan during its rapid economic growth. Many children disliked them due to their tomato-like smell, and tomatoes were unpopular among consumers because of their unappealing appearance. Since then, tomatoes have improved in these characteristics and, through ingenious cultivation methods, have become a vegetable not limited to one season. Tomatoes have been the world's most extensive vegetable by production since the 1990s, with about 200 million tons produced annually, representing 14 trillion yen (equivalent to US$93 billion). Native to the Andean plateau of South America, tomatoes were introduced to Spain from Mexico by Hernán Cortés (1485-1547) in 1519. Initially, it was an ornamental plant, but later, it was also used for food.

Tomatoes grow large as green fruits, then turn yellow, and then red. In the late 1980s, I started working on this research question to understand what happens during this process. Several events co-occur during the green-to-red transformation of the tomato fruit. First, the green fruit undergoes "photosynthesis," which uses solar energy to fix carbon dioxide in the air and synthesize sugars. The fruit grows, including the result of photosynthesis, but this activity stops as the fruit turns red. Second, the green pigment chlorophylls, responsible for receiving solar energy in photosynthesis, are degraded. Third, the red component called lycopene, which has cancer-preventing properties, begins to be synthesized and accumulated.

The instructions for photosynthesis, the breakdown of chlorophylls, and lycopene synthesis are encoded in the genetic information of DNA, which consists of four different nucleotide combinations: A, C, G, and T. Of these, the chemical structure of C is of particular interest. C can have a methyl group at position 5 of its chemical structure. Using four techniques, we concluded that "photosynthetic genes in chloroplasts are methylated during the reddening process of tomato fruit, resulting in the loss of expression of these genes and the eventual cessation of photosynthetic function." We published this in 1990 in the European "EMBO Journal," which is on par with the "Proceedings of the National Academy of Sciences of the United States of America (PNAS)." The results attracted the interest of other researchers, and considerable studies were conducted on DNA methylation and gene expression in tomatoes and other plants. For the next 30 years, I worked on different research projects. During this time, comprehensive literature databases have been developed, making it easy to identify which of our publications have been cited in subsequent research papers. A thorough analysis of methylated DNA (methylome) has become available recently. A paper on the chloroplast DNA methylation analysis during rice ripening strongly supports our observation of tomato fruits turning red (supplementary academic comments are shown separately).

The stay-green (sgr) gene was reported in soybeans about 100 years ago, in 1921, for degrading the green pigment chlorophylls. Now, the entity of the SGR protein and its regulatory mechanism have been clarified. On the other hand, lycopene, a red component of carotenoids, was first reported in 1873. Subsequently, the chemical structure was determined in the 1950s, and the biosynthetic pathway was elucidated through the 1960s. Today, it is possible to increase lycopene levels through genome editing. I have here presented the elucidation of the molecular mechanism behind the ripening process of tomatoes, which is the world's largest producer of tomatoes as a vegetable. I want to convey that this kind of research will contribute to improving tomatoes.