Requirement of CHROMOMETHYLASE3 for somatic inheritance of the spontaneous tomato epimutation Colourless non-ripening

Chen, Weiwei; Kong, Junhua; Qin, Cheng; Yu, Sheng; Tan, Jinjuan; Chen, Yun-ru; Wu, Chaoqun; Wang, Hui; Shi, Yan; Li, Chunyang; Li, Bin; Zhang, Pengcheng; Wang, Ying; Lai, Tongfei; Yu, Zhiming; Zhang, Xian; Shi, Nongnong; Wang, Huizhong; Osman, Toba; Liu, Yule; Manning, Kenneth; Jackson, Stephen; Rolin, Dominique; Zhong, Silin; Seymour, Graham B.; Gallusci, Philippe; Hong, Yiguo

Abstract

Naturally-occurring epimutants are rare and have mainly been described in plants. However how these mutants maintain their epigenetic marks and how they are inherited remain unknown. Here we report that CHROMOMETHYLASE3 (SlCMT3) and other methyltransferases are required for maintenance of a spontaneous epimutation and its cognate Colourless non-ripening (Cnr) phenotype in tomato. We screened a series of DNA methylation-related genes that could rescue the hypermethylated Cnr mutant. Silencing of the developmentally-regulated SlCMT3 gene results in increased expression of LeSPL-CNR, the gene encodes the SBP-box transcription factor residing at the Cnr locus and triggers Cnr fruits to ripen normally. Expression of other key ripening-genes was also up-regulated. Targeted and whole-genome bisulfite sequencing showed that the induced ripening of Cnr fruits is associated with reduction of methylation at CHG sites in a 286-bp region of the LeSPL-CNR promoter, and a decrease of DNA methylation in differentially-methylated regions associated with the LeMADS-RIN binding sites. Our results indicate that there is likely a concerted effect of different ethyltransferases at the Cnr locus and the plant-specific SlCMT3 is essential for sustaining Cnr epi-allele. Maintenance of DNA methylation dynamics is critical for the somatic stability of Cnr epimutation and for the inheritance of tomato non-ripening phenotype.

Citation

Chen, W., Kong, J., Qin, C., Yu, S., Tan, J., Chen, Y.-R., …Hong, Y. (2015). Requirement of CHROMOMETHYLASE3 for somatic inheritance of the spontaneous tomato epimutation Colourless non-ripening. Scientific Reports, 5, Article 9192. https://doi.org/10.1038/srep09192

• Journal Article Type: Article
• Acceptance Date: Feb 23, 2015
• Online Publication Date: Mar 17, 2015
• Publication Date: Mar 17, 2015
• Deposit Date: Mar 20, 2015
• Publicly Available Date: Mar 20, 2015
• Journal: Scientific Reports
• Electronic ISSN: 2045-2322
• Publisher: Nature Publishing Group
• Peer Reviewed: Peer Reviewed
• Volume: 5
• Article Number: 9192
• DOI: https://doi.org/10.1038/srep09192
• Public URL: https://nottingham-repository.worktribe.com/output/987950
• Publisher URL: http://www.nature.com/srep/2015/150317/srep09192/full/srep09192.html
• Contract Date: Mar 20, 2015