Transcription factor PpNAC1 and DNA demethylase PpDML1 synergistically regulate peach fruit ripening
- 22 November 2023
- journal article
- research article
- Published by Oxford University Press (OUP) in Plant Physiology
- Vol. 194 (4) , 2049-2068
Abstract
Fruit ripening is accompanied by dramatic changes in color, texture, and flavor and is regulated by transcription factors (TFs) and epigenetic factors. However, the detailed regulatory mechanism remains unclear. Gene expression patterns suggest that PpNAC1 (NAM/ATAF1/2/CUC) TF plays a major role in peach (Prunus persica) fruit ripening. DNA affinity purification (DAP)-seq combined with transactivation tests demonstrated that PpNAC1 can directly activate the expression of multiple ripening-related genes, including ACC synthase1 (PpACS1) and ACC oxidase1 (PpACO1) involved in ethylene biosynthesis, pectinesterase1 (PpPME1), pectate lyase1 (PpPL1) and polygalacturonase1 (PpPG1) related to cell wall modification, and lipase1 (PpLIP1), fatty acid desaturase (PpFAD3-1) and alcohol acyltransferase1 (PpAAT1) involved in volatiles synthesis. Overexpression of PpNAC1 in the tomato (Solanum lycopersicum) nor (non-ripening) mutant restored fruit ripening, and its transient overexpression in peach fruit induced target gene expression, supporting a positive role of PpNAC1 in fruit ripening. The enhanced transcript levels of PpNAC1 and its target genes were associated with decreases in their promoter mCG methylation during ripening. Declining DNA methylation was negatively associated with increased transcripts of DNA demethylase1 (PpDML1), whose promoter is recognized and activated by PpNAC1. We propose that decreased methylation of the promoter region of PpNAC1 leads to a subsequent decrease in DNA methylation levels and enhanced transcription of ripening-related genes. These results indicate that positive feedback between PpNAC1 and PpDML1 plays an important role in directly regulating expression of multiple genes required for peach ripening and quality formation.Keywords
Funding Information
- National Key R&D Program of China (2022YFD2100101)
- National Natural Science Foundation of China (32102445)
- National Natural Science Foundation of Zhejiang Province (LD22C150001)
- 111 Project (B17039)
- Foundational Research Funds for the Central Universities (226-2023-00078)
This publication has 85 references indexed in Scilit:
- Increased levels of IAA are required for system 2 ethylene synthesis causing fruit softening in peach (Prunus persica L. Batsch)Journal of Experimental Botany, 2013
- Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripeningNature Biotechnology, 2013
- Molecular characterization of banana NAC transcription factors and their interactions with ethylene signalling component EIL during fruit ripeningJournal of Experimental Botany, 2012
- Fast gapped-read alignment with Bowtie 2Nature Methods, 2012
- Metabolic Profiling during Peach Fruit Development and Ripening Reveals the Metabolic Networks That Underpin Each Developmental StagePlant Physiology, 2011
- MEME-ChIP: motif analysis of large DNA datasetsBioinformatics, 2011
- Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell IdentitiesMolecular Cell, 2010
- Expression of Genes Associated with Aroma Formation Derived from the Fatty Acid Pathway during Peach Fruit RipeningJournal of Agricultural and Food Chemistry, 2010
- Model-based Analysis of ChIP-Seq (MACS)Genome Biology, 2008
- Tomato (Lycopersicum esculentum)2006