Diversity and redundancy of the ripening regulatory networks revealed by the fruitENCODE and the new CRISPR/Cas9 CNR and NOR mutants. Issue 1 (11th February 2019)

• Record Type: Journal Article
• Authors: Gao, Ying; Zhu, Ning; Zhu, Xiaofang; Wu, Meng; Jiang, Cai-Zhong; Grierson, Donald; Luo, Yunbo; Shen, Wei; Zhong, Silin; Fu, Da-Qi; Qu, Guiqin
• Is Part Of: Horticulture research. Volume 6:Issue 1(2019)
• Publication Date: 2019-02-11
• Subjects: Fruiting -- Molecular ecology -- Transcription factor -- Gene editing; Horticulture -- Research -- Periodicals; 635.072
• DOI: 10.1038/s41438-019-0122-x
• Languages: English
• ISSNs: 2052-7276

Abstract

Abstract: Tomato is considered as the genetic model for climacteric fruits, in which three major players control the fruit ripening process: ethylene, ripening transcription factors, and DNA methylation. The fruitENCODE project has now shown that there are multiple transcriptional circuits regulating fruit ripening in different species, and H3K27me3, instead of DNA methylation, plays a conserved role in restricting these ripening pathways. In addition, the function of the core tomato ripening transcription factors is now being questioned. We have employed CRISPR/Cas9 genome editing to mutate the SBP - CNR and NAC - NOR transcription factors, both of which are considered as master regulators in the current tomato ripening model. These plants only displayed delayed or partial non-ripening phenotypes, distinct from the original mutant plants, which categorically failed to ripen, suggesting that they might be gain-of-function mutants. Besides increased DNA methylation genome-wide, the original mutants also have hyper-H3K27me3 in ripening gene loci such as ACS2, RIN, and TDR4 . It is most likely that multiple genetic and epigenetic factors have contributed to their strong non-ripening phenotypes. Hence, we propose that the field should move beyond these linear and two-dimensional models and embrace the fact that important biological processes such as ripening are often regulated by highly redundant network with inputs from multiple levels. Fruit ripening: Multiple backup plans: The regulatory circuits that govern the expression of genes required for ripening in tomato plants are highly redundant. Fleshy fruits that use the hormone ethylene to regulate ripening have developed independently multiple times in the history of the angiosperms. Guiqin Qu at China Agricultural University in Beijing and colleagues working on the fruitENCODE project are exploring the genetic and epigenetic basis of this convergent evolution. In tomatoes, three transcription factors have been shown to control ethylene production and regulate ripening. However, when gene editing techniques were used to introduce mutations that interfere with the function of these transcription factors, partial ripening or a delay in ripening was observed. The fact that ripening was not abolished indicates that the ripening process is more robust and complex than previously thought.