Genetic Control of Fruit Ripening in Tomato
The tomato is one of many plants that have evolved an “edible fruit” strategy for seed dispersal. Mature seed is encased in a fruit designed to be attractive for consumption by fruit-eating animals. Seed dispersal occurs when the consumed seed passes safely through the digestive tract and is deposited with feces on the soil some distance from the mother plant. In tomatoes, the fruit-ripening process involves several steps designed to enhance attractiveness for consumption: an increase in fruit sugars, acids, and flavor-enhancing aromatic compounds that greatly improve tastiness of the fruit; fruit softening to a more edible texture; and obvious fruit pigmentation designed to signal to passing animals that the fruit is fully ripe and ready to eat. However, from an evolutionary standpoint, it would be disadvantageous if fruit were consumed prior to seed ripening—so the ripening process is closely coordinated with seed maturity. These features were preserved during the domestication of the tomato and the more recent development of the tomato as one of the world’s most important fruit/vegetable crops.
Tomato Fruit Development (from Alba et al., 2005)
The Ripening Process
Tomatoes are a climacteric fruit, which means that the plant hormone ethylene is required for fruit ripening. Tomato seed is mature at the mature green (MG) stage. Ethylene is rapidly produced in tomato fruit at the breaker (BK) stage, which drives a series of reactions that together define the fruit-ripening process. During normal ripening, there are simultaneous and independent processes that lead to 1) accumulation of sugars, organic acids, and volatile organic compounds influencing flavor; 2) conversion of chloroplasts to chromoplasts and the synthesis and accumulation of carotenoid pigments; and 3) softening of the fruit.
The tomato has become the “model system” for the study of ripening in climacteric fruit, and in the last several years, much has been learned about genetic control of fruit ripening in tomato. A summary of this is outlined below:
The genes RIN and NOR are master regulatory genes that control the various genetic pathways associated with tomato fruit ripening. Both genes are transcription factors that activate (or repress) expression of target genes, thus regulating expression of virtually all key genes associated with fruit ripening. The wild-type alleles of both genes allow for initiation of ethylene production and downstream ethylene-mediated ripening processes, such as carotenoid biosynthesis (i.e., fruit pigmentation), sugar accumulation, and fruit softening. A relatively recent research paper 1 showed that although tomato fruit ripening is triggered by ethylene, its effect is restricted by an unknown developmental signal to fruit containing viable seeds. They further demonstrated that epigenetic gene silencing prevented expression of key ripening genes prior to the MG stage, and this was caused by methylation of promoter sequences of these genes that prevented RIN binding and gene activation. In wild-type plants, demethylation of these ripening genes is triggered when viable seed is formed in MG fruit, and ripening proceeds under the control of RIN and NOR, mediated by ethylene.
There are mutant alleles of both RIN (rin) and NOR (nor) that have incomplete dominance. For both rin and nor alleles, plants that are homozygous for either mutant allele (i.e., rin/rin or nor/nor) produce fruit that do not ripen normally. In most cases, the fruit stays firm and crisp, and there is minimal development of carotenoid pigments and fruit sugars. Fruit from plants heterozygous +/rin or +/nor, with a single copy of the mutant allele, shows delayed ripening and extended shelf life of ripened fruit. The rin mutant was recently shown to be a complex mutation that turned the RIN transcription factor from an activator to a repressor of expression of key ripening genes 2. There are at least three mutant alleles of nor, each with subtle differences in phenotype—a current area of active research. Most current extended shelf life hybrids are either +/rin or +/nor; these represent a significant portion of the vine-ripened/protected culture fresh market tomato sector.
Fruit at BK +7 Stage (Seven Days after Breaker Stage in the WT)
Wild Type rin/rin nor/nor
Photo by Martel, 2010
- Zhong et al., 2013
- Ito et al., 2017