title: A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening.
abstract: The fruit ripening developmental program is specific to plants bearing fleshy fruits and dramatically changes fruit characteristics, including color, aroma, and texture. The tomato (Solanum lycopersicum) MADS box transcription factor RIPENING INHIBITOR (RIN), one of the earliest acting ripening regulators, is required for both ethylene-dependent and -independent ripening regulatory pathways. Recent studies have identified two dozen direct RIN targets, but many more RIN targets remain to be identified. Here, we report the large-scale identification of direct RIN targets by chromatin immunoprecipitation coupled with DNA microarray analysis (ChIP-chip) targeting the predicted promoters of tomato genes. Our combined ChIP-chip and transcriptome analysis identified 241 direct RIN target genes that contain a RIN binding site and exhibit RIN-dependent positive or negative regulation during fruit ripening, suggesting that RIN has both activator and repressor roles. Examination of the predicted functions of RIN targets revealed that RIN participates in the regulation of lycopene accumulation, ethylene production, chlorophyll degradation, and many other physiological processes. Analysis of the effect of ethylene using 1-methylcyclopropene revealed that the positively regulated subset of RIN targets includes ethylene-sensitive and -insensitive transcription factors. Intriguingly, ethylene is involved in the upregulation of RIN expression during ripening. These results suggest that tomato fruit ripening is regulated by the interaction between RIN and ethylene signaling.
authors: National Food Research Institute, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8642, Japan.
authors: Masaki
authors: M
authors: Fujisawa
authors: Toshitsugu
authors: T
authors: Nakano
authors: Yoko
authors: Y
authors: Shima
authors: Yasuhiro
authors: Y
authors: Ito
mesh_terms: D001665:Binding Sites; D002338:Carotenoids / Q000378:metabolism; D002734:Chlorophyll / Q000378:metabolism; D047369:Chromatin Immunoprecipitation; D003521:Cyclopropanes / Q000494:pharmacology; D005030:Ethylenes / Q000378:metabolism; D005638:Fruit / Q000235:genetics / Q000254:growth & development*; D018506:Gene Expression Regulation, Plant; D000077276:Lycopene; D018551:Solanum lycopersicum / Q000187:drug effects / Q000254:growth & development* / Q000502:physiology; D026161:MADS Domain Proteins / Q000235:genetics / Q000378:metabolism*; D008969:Molecular Sequence Data; D020411:Oligonucleotide Array Sequence Analysis; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D011401:Promoter Regions, Genetic; D015398:Signal Transduction; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D003521:Cyclopropanes; D005030:Ethylenes; D026161:MADS Domain Proteins; D010940:Plant Proteins; D014157:Transcription Factors; D002734:Chlorophyll; D002338:Carotenoids; C036216:ethylene; C412563:1-methylcyclopropene; D000077276:Lycopene
references: Plant Mol Biol. 1993 Jul;22(4):589-602
references: 8343597
references: BMC Bioinformatics. 2003 Jun 23;4:25
references: 12820902
references: Plant Cell. 2009 Sep;21(9):2563-77
references: 19767455
references: Sci Rep. 2012;2:836
references: 23150786
references: BMC Plant Biol. 2012 Feb 13;12:19
references: 22330838
references: Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1560-5
references: 22238427
references: J Exp Bot. 2009;60(12):3433-42
references: 19605457
references: Nat Genet. 2006 Aug;38(8):948-52
references: 16832354
references: Int J Dev Biol. 2009;53(8-10):1635-48
references: 19876848
references: BMC Plant Biol. 2011 Jan 30;11:26
references: 21276270
references: PLoS Biol. 2009 Apr 21;7(4):e1000090
references: 19385720
references: Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):1035-40
references: 9023378
references: Plant Cell. 2012 Nov;24(11):4437-51
references: 23136376
references: Science. 2002 Apr 12;296(5566):343-6
references: 11951045
references: Nucleic Acids Res. 2004 Oct 14;32(18):5539-45
references: 15486203
references: Plant Cell. 2011 Mar;23(3):923-41
references: 21398570
references: Plant Physiol. 1999 Jan;119(1):41-8
references: 9880344
references: Plant Physiol. 1999 Jun;120(2):383-90
references: 10364389
references: Plant Physiol. 2004 Dec;136(4):4184-97
references: 15563627
references: Trends Genet. 2000 Jun;16(6):276-7
references: 10827456
references: Plant Cell. 2000 Mar;12(3):393-404
references: 10715325
references: Plant Cell. 2005 Nov;17(11):2954-65
references: 16243903
references: Plant J. 2009 Dec;60(6):1081-95
references: 19891701
references: Plant J. 2008 Jul;55(2):301-10
references: 18397374
references: Plant J. 2012 Apr;70(2):243-55
references: 22098335
references: BMC Plant Biol. 2008 Dec 22;8:131
references: 19102748
references: J Exp Bot. 2010 Jun;61(6):1795-806
references: 20335407
references: Plant Cell. 2004;16 Suppl:S170-80
references: 15010516
references: Plant Cell. 2002 Feb;14(2):333-42
references: 11884678
references: Plant Physiol. 2008 May;147(1):179-87
references: 18359841
references: Planta. 2012 Jun;235(6):1107-22
references: 22160566
references: Plant J. 2010 Dec;64(6):936-47
references: 21143675
references: Plant Cell. 2009 Feb;21(2):403-19
references: 19244139
references: Curr Opin Plant Biol. 2000 Jun;3(3):217-23
references: 10837265
references: Curr Opin Plant Biol. 2007 Jun;10(3):283-9
references: 17442612
references: Plant Cell. 2007 Mar;19(3):731-49
references: 17337630
references: Plant Cell. 2007 May;19(5):1649-64
references: 17513504
references: Genome Res. 2004 Jun;14(6):1188-90
references: 15173120
references: Biochemistry. 2002 Apr 2;41(13):4202-8
references: 11914065
references: Genome Res. 2008 Mar;18(3):393-403
references: 18258921
references: Plant J. 2012 Apr;70(2):191-204
references: 22111515
references: Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):1092-7
references: 11805345
references: Plant Physiol. 2011 Sep;157(1):405-25
references: 21795583
references: Plant J. 2012 May;70(4):549-61
references: 22268548
references: Nature. 2012 May 30;485(7400):635-41
references: 22660326
references: Plant J. 2008 Jul;55(2):212-23
references: 18363783
references: Nucleic Acids Res. 1990 Oct 25;18(20):6097-100
references: 2172928
references: PLoS One. 2010 Dec 23;5(12):e14427
references: 21203447
references: Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
references: 9254694
references: Methods. 2001 Dec;25(4):402-8
references: 11846609
references: Plant Cell. 2009 Oct;21(10):3041-62
references: 19880793
references: Plant Physiol. 2011 Nov;157(3):1568-79
references: 21941001