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PMID: 28507144 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 114 ·No. 22 ·2017-00-30 ·Pages E4511-E4519

Lang Z, Wang Y, Tang K, Tang D, Datsenka T, Cheng J, Zhang Y, Handa AK, Zhu JK

Abstract

DNA methylation is a conserved epigenetic mark important for genome integrity, development, and environmental responses in plants and mammals. Active DNA demethylation in plants is initiated by a family of 5-mC DNA glycosylases/lyases (i.e., DNA demethylases). Recent reports suggested a role of active DNA demethylation in fruit ripening in tomato. In this study, we generated loss-of-function mutant alleles of a tomato gene, SlDML2, which is a close homolog of the Arabidopsis DNA demethylase gene ROS1 In the fruits of the tomato mutants, increased DNA methylation was found in thousands of genes. These genes included not only hundreds of ripening-induced genes but also many ripening-repressed genes. Our results show that SlDML2 is critical for tomato fruit ripening and suggest that active DNA demethylation is required for both the activation of ripening-induced genes and the inhibition of ripening-repressed genes.

Keywords
5-mC DNA glycosylase DNA demethylase DNA methylation epigenetic regulation gene silencing
MeSH Terms
DNA Demethylation DNA Glycosylases/genetics,metabolism Epigenesis, Genetic/genetics Fruit/genetics,physiology Gene Expression Regulation, Plant/genetics Gene Silencing Histone Demethylases/genetics,metabolism Lycopersicon esculentum/genetics,physiology Nuclear Proteins/genetics,metabolism Plant Proteins/genetics,physiology
Chemicals
Nuclear Proteins Plant Proteins Histone Demethylases DNA Glycosylases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Lang Zhaobo
Shanghai Center for Plant Stress Biology and Center of Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China; jkzhu@purdue.edu zblang@sibs.ac.cn. | Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.
Wang Yihai
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.
Tang Kai
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.
Tang Dengguo
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.
Datsenka Tatsiana
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.
Cheng Jingfei
Shanghai Institute of Plant Physiology and Ecology and Center of Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
Zhang Yijing
Shanghai Institute of Plant Physiology and Ecology and Center of Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
Handa Avtar K
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.
Zhu Jian-Kang ORCID
Shanghai Center for Plant Stress Biology and Center of Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China; jkzhu@purdue.edu zblang@sibs.ac.cn. | Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.
Conflict of Interest

The authors declare no conflict of interest.

References (45)
45 references, click to expand
  1. Regulation of active DNA demethylation by an α-crystallin domain protein in Arabidopsis.
    Mol Cell. 2014 Aug 7;55(3):361-71 PMID: 25002145
  2. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity.
    Nat Rev Genet. 2014 Jun;15(6):394-408 PMID: 24805120
  3. BRAT-BW: efficient and accurate mapping of bisulfite-treated reads.
    Bioinformatics. 2012 Jul 1;28(13):1795-6 PMID: 22563065
  4. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase.
    Cell. 2002 Dec 13;111(6):803-14 PMID: 12526807
  5. An AP endonuclease functions in active DNA demethylation and gene imprinting in Arabidopsis [corrected].
    PLoS Genet. 2015 Jan 08;11(1):e1004905 PMID: 25569774
  6. Local DNA hypomethylation activates genes in rice endosperm.
    Proc Natl Acad Sci U S A. 2010 Oct 26;107(43):18729-34 PMID: 20937895
  7. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.
    Bioinformatics. 2010 Jan 1;26(1):139-40 PMID: 19910308
  8. Genome-wide identification of cytosine-5 DNA methyltransferases and demethylases in Solanum lycopersicum.
    Gene. 2014 Oct 25;550(2):230-7 PMID: 25149677
  9. Regulation and function of DNA methylation in plants and animals.
    Cell Res. 2011 Mar;21(3):442-65 PMID: 21321601
  10. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.
    Genome Biol. 2013 Apr 25;14(4):R36 PMID: 23618408
  11. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening.
    Nat Biotechnol. 2013 Feb;31(2):154-9 PMID: 23354102
  12. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation.
    Cell. 2006 Feb 10;124(3):495-506 PMID: 16469697
  13. A DEMETER-like DNA demethylase governs tomato fruit ripening.
    Proc Natl Acad Sci U S A. 2015 Aug 25;112(34):10804-9 PMID: 26261318
  14. Establishing, maintaining and modifying DNA methylation patterns in plants and animals.
    Nat Rev Genet. 2010 Mar;11(3):204-20 PMID: 20142834
  15. Genetics and control of tomato fruit ripening and quality attributes.
    Annu Rev Genet. 2011;45:41-59 PMID: 22060040
  16. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin.
    Cell. 2013 Mar 28;153(1):193-205 PMID: 23540698
  17. Regulatory link between DNA methylation and active demethylation in Arabidopsis.
    Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):3553-7 PMID: 25733903
  18. A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening.
    Plant Cell. 2013 Feb;25(2):371-86 PMID: 23386264
  19. Application of the CRISPR-Cas system for efficient genome engineering in plants.
    Mol Plant. 2013 Nov;6(6):2008-11 PMID: 23963532
  20. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner.
    Plant Physiol. 2011 Nov;157(3):1568-79 PMID: 21941001
  21. A histone acetyltransferase regulates active DNA demethylation in Arabidopsis.
    Science. 2012 Jun 15;336(6087):1445-8 PMID: 22700931
  22. The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis.
    Curr Biol. 2007 Jan 9;17(1):54-9 PMID: 17208187
  23. DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis.
    Genome Biol. 2014 Sep 17;15(9):458 PMID: 25228471
  24. Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation.
    Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11796-801 PMID: 16864782
  25. The DNA demethylase ROS1 targets genomic regions with distinct chromatin modifications.
    Nat Plants. 2016 Oct 31;2(11):16169 PMID: 27797352
  26. A DNA 3' phosphatase functions in active DNA demethylation in Arabidopsis.
    Mol Cell. 2012 Feb 10;45(3):357-70 PMID: 22325353
  27. DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases.
    Proc Natl Acad Sci U S A. 2006 May 2;103(18):6853-8 PMID: 16624880
  28. A potential role for CHH DNA methylation in cotton fiber growth patterns.
    PLoS One. 2013 Apr 12;8(4):e60547 PMID: 23593241
  29. The tomato genome sequence provides insights into fleshy fruit evolution.
    Nature. 2012 May 30;485(7400):635-41 PMID: 22660326
  30. A pair of transposon-derived proteins function in a histone acetyltransferase complex for active DNA demethylation.
    Cell Res. 2017 Feb;27(2):226-240 PMID: 27934869
  31. Overproduction of stomatal lineage cells in Arabidopsis mutants defective in active DNA demethylation.
    Nat Commun. 2014 Jun 05;5:4062 PMID: 24898766
  32. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening.
    Nat Genet. 2006 Aug;38(8):948-52 PMID: 16832354
  33. Active DNA demethylation in plants and animals.
    Cold Spring Harb Symp Quant Biol. 2012;77:161-73 PMID: 23197304
  34. Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation.
    Proc Natl Acad Sci U S A. 2016 Nov 1;113(44):12580-12585 PMID: 27791156
  35. The methyl-CpG-binding protein MBD7 facilitates active DNA demethylation to limit DNA hyper-methylation and transcriptional gene silencing.
    Mol Cell. 2015 Mar 19;57(6):971-83 PMID: 25684209
  36. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features.
    Bioinformatics. 2014 Apr 1;30(7):923-30 PMID: 24227677
  37. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus.
    Science. 2002 Apr 12;296(5566):343-6 PMID: 11951045
  38. Methyl-CpG-binding domain protein MBD7 is required for active DNA demethylation in Arabidopsis.
    Plant Physiol. 2015 Mar;167(3):905-14 PMID: 25593350
  39. DNA Methylation Signatures of the Plant Chromomethyltransferases.
    PLoS Genet. 2016 Dec 20;12 (12 ):e1006526 PMID: 27997534
  40. Matrix2png: a utility for visualizing matrix data.
    Bioinformatics. 2003 Jan 22;19(2):295-6 PMID: 12538257
  41. Active DNA demethylation mediated by DNA glycosylases.
    Annu Rev Genet. 2009;43:143-66 PMID: 19659441
  42. Fruit ripening mutants yield insights into ripening control.
    Curr Opin Plant Biol. 2007 Jun;10(3):283-9 PMID: 17442612
  43. A DNA ligase required for active DNA demethylation and genomic imprinting in Arabidopsis.
    Cell Res. 2015 Jun;25(6):757-60 PMID: 25906993
  44. A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics.
    Plant Cell Physiol. 2006 Mar;47(3):426-31 PMID: 16381658
  45. Increasing tomato fruit quality by enhancing fruit chloroplast function. A double-edged sword?
    J Exp Bot. 2014 Aug;65(16):4589-98 PMID: 24723405
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
DOI
10.1073/pnas.1705233114
Email
jkzhu@purdue.edu
zblang@sibs.ac.cn
Published
2017-00-30
Epub
2017-00-15
Pages
E4511-E4519
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC5465898
Subset
IM
Grants
NIGMS NIH HHS · R01 GM059138 · United States
NIGMS NIH HHS · R01 GM070795 · United States
External Links
PubMed source DOI: 10.1073/pnas.1705233114 PMC Full Text View journal details
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