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

Jason Argyris, Silin Zhong, James Giovannoni, Zhangjun Fei, Jenny Xiang, Donald Grierson, Jianhua Zhang, Nenghui Ye, Jordi Garcia-Mas, Peitao Lü, Joao Paulo Fabi, David Tzeng, Yu Pan, Biyan Zhou, Yun-Ru Chen, Ning Zhu, Sheng Yu

Journal: Nature plants 2019;4(10):784-791

PMID: 30250279

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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.

Address: State Key Laboratory of Agrobiotechnology, School of Life Sciences, Chinese University of Hong Kong, Hong Kong, China.; College of Horticulture, South China Agricultural University, Guangzhou, China.; College of Horticulture and Landscape Architecture, Southwest University, Chongqing, China.; Department of Food Science and Experimental Nutrition, FCF, University of Sao Paulo, Sao Paulo, Brazil.; IRTA, Centre for Research in Agricultural Genomics, Barcelona, Spain.; Department of Biology, Hong Kong Baptist University, Hong Kong, China.; School of Crop Sciences, University of Nottingham, Nottingham, UK.; Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Hangzhou, China.; Weill Medical College, Cornell University, New York, NY, USA.; US Department of Agriculture-Agricultural Research Service and Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY, USA.; State Key Laboratory of Agrobiotechnology, School of Life Sciences, Chinese University of Hong Kong, Hong Kong, China. [email protected].

DOI: 10.1038/s41477-018-0249-z

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MeSH Terms: Biological Evolution, Chromatin, DNA Methylation, Ethylenes, Fruit, Gene Expression Profiling, Genome, Plant, Histones, Solanum lycopersicum, MADS Domain Proteins, Malus, Plant Growth Regulators, Pyrus