CUHK Passions and Pursuits

51 The Fruit Cracker Zhong Silin decodes fruition in nature S cientists have long wanted to fathom the mechanism which regulates the ripening of fleshy fruits. Like the gestation of a human foetus followed by labour, nature seems to have encoded when and under what conditions a fruit should ripen. Prof. Zhong Silin leads an international team of scientists in the fruitENCODE project which aims to provide a comprehensive annotation of the functional elements in fleshy fruits in order to crack the mysterious process of fruit ripening. The fruitENCODE team studied the genetic and epigenetic bases of the evolution of 11 fruits— apple, pear, melon, peach, papaya, banana, watermelon, grape, strawberry, tomato and cucumber. By means of large-scale profiling of gene expression data and DNA methylation, and mapping of histone modifications and accessible chromatin regions, the team was able to identify three types of positive feedback loop that govern their fruit ripening processes. Their findings were published in Nature Plants . Apple, pear and tomato experienced recent whole genome duplication (doubling or even tripling their genome size) at the end of the Cretaceous period (145–66 million years ago). They evolved their fruits by using those duplicated floral organ identity genes (genes that specify the identity of the different organs of a flower) of their ancestors. In these fruits, a certain transcription factor (protein that controls if and when a gene gets activated) directly binds to genes that signal the production of ethylene, a kind of fruit hormone which facilitates ripening. The result further triggers other transcription factors which come full circle to bind with the original transcription factor and so on, thereby starting a positive feedback loop that enables and sustains ethylene synthesis. Melon, peach and papaya did not have the luxury of whole genome duplication during the late Cretaceous, and therefore have not inherited the first group’s ethylene- production kit. They instead synthesize ethylene by converting their existing gene controlling senescence (aging of the plant) to form a different positive feedback loop for the sustenance of ethylene synthesis. The most eclectic of the bunch, banana, reaches ripening by a combination of the two: using both the floral organ identity and the senescence genes. The other fruits in the study—watermelon, cucumber, grape and strawberry— have developed their own system of ripening independent of ethylene. What the team also found is that the epigenetic mark H3K27me3, which represses key developmental genes in animals, plays an important regulatory role in the ripening process of fruits, too. It acts as a braking device that targets key ripening genes in plants to prevent premature ripening which may be undesirable in terms of the survival of the seeds. Marks similar to H3K27me3 are found in the ripening genes of the ancestral plant species, suggesting that in their evolution, fruits like tomato, peach and banana have not just inherited the type of positive feedback loop from their ancestors but also their epigenetic marks to regulate ripening. By elucidating the genetic and epigenetic mechanism of fruit ripening, the team’s findings could pave the way for a healthier and steadier food source in future. It is also possible to manipulate and engineer the regulatory components in gene expressions to enhance the fruits’ nutritional value, consumer appeal and shelf life. This is good news to fruit-lovers across the globe.