Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening

Authors: LIU, PEITAO - The Chinese University Of Hong Kong (CUHK); YU, SHENG - The Chinese University Of Hong Kong (CUHK); CHEN, YUN-RU - The Chinese University Of Hong Kong (CUHK); ZHOU, BIYAN - The Chinese University Of Hong Kong (CUHK); TZENG, DAVID - The Chinese University Of Hong Kong (CUHK); GRIERSON, DONALD - University Of Nottingham; XIANG, JENNY - Cornell University; FEI, ZHANGJUN - Boyce Thompson Institute; Giovannoni, James; ZHONG, SILIN - The Chinese University Of Hong Kong (CUHK)

Submitted to: Nature Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/9/2018
Publication Date: 9/24/2018
Citation: Liu, P., Yu, S., Chen, Y., Zhou, B., Tzeng, D., Grierson, D., Xiang, J., Fei, Z., Giovannoni, J.J., Zhong, S. 2018. Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening. Nature Plants. https://doi.org.10.1038/s41477-018-0249-z
DOI: https://doi.org/10.1038/s41477-018-0249-z

Interpretive Summary: The development of fleshy fruits enabled angiosperms to interact with coevolving animals (frugivores), which consumed the fruits and dispersed the seeds to different locations, thus enhancing distribution, minimizing parental competition and increasing plant reproductive success. Fleshy fruit ripening is a developmental process unique to flowering plants, in which the chemical and physiological properties such as color, aroma, flavor, texture and nutritional contents of the seed-bearing organ are dramatically altered to attract frugivore seed dispersers. As vital to human and animal diets, understanding fruit ripening is increasingly important for global food and nutritional security. Here we explore the genome sequences, expression and DNA binding of ripe and unripe fruits of eleven species. We reveal that epigenetic control of two transcription factors regulating ethylene hormone synthesis is a reoccurring theme in evolution of fleshy fruit ripening. These findings point to breeding and engineering targets for manipulation of ripening for crop shelf-life and nutritional quality.

Technical Abstract: Fleshy fruits using ethylene to regulate ripening have developed multiple times in the history of angiosperms, presenting a clear case of convergent evolution whose molecular basis remains largely unknown. Analysis of the fruitENCODE data consisting of 361 transcriptome, 71 accessible chromatin, 147 histone and 45 DNA methylation profiles reveals three types of transcriptional feedback circuits controlling ethylene-dependent fruit ripening. These circuits are evolved from senescence or floral organ identity pathways in the ancestral angiosperms either by neofunctionalisation or repurposing pre-existing genes. The epigenome, H3K27me3 in particular, has played a conserved role in restricting ripening genes and their orthologues in dry and ethylene-independent fleshy fruits. Our findings suggest that evolution of ripening is constrained by limited hormone molecules and genetic and epigenetic materials, and whole-genome duplications have provided opportunities for plants to successfully circumvent these limitations.