Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development

Genome Biology

Volumn 15, Issue 3, 2014, Pages

  Pajoro, Alice ^a   Madrigal, Pedro ^b   Muiño, Jose M ^c   Matus, José T ^d   Jin, Jian ^d   Mecchia, Martin A ^e   Debernardi, Juan M ^e   Palatnik, Javier F ^e   Balazadeh, Salma ^f   Arif, Muhammad ^f   Ó'Maoiléidigh, Diarmuid S ^g   Wellmer, Frank ^g   Krajewski, Pawel ^b   Riechmann, José Luis ^d,h   Angenent, Gerco C ^a   Kaufmann, Kerstin ^a,f  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b INSTITUTE OF PLANT GENETICS   (Poland)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d CENTRE FOR RESEARCH IN AGRICULTURAL GENOMICS CRAG   (Spain)

^e UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^f UNIVERSITY OF POTSDAM   (Germany)

^g TRINITY COLLEGE DUBLIN   (Ireland)

^h INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MADS DOMAIN TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; AP1 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; CHROMATIN; HOMEODOMAIN PROTEIN; MADS DOMAIN PROTEIN; PROTEIN BINDING; SEP3 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

APETALA1 GENE; ARABIDOPSIS; ARTICLE; BINDING SITE; CHROMATIN; CONTROLLED STUDY; FLOWER DEVELOPMENT; GENE CONTROL; GENE EXPRESSION; GENE REGULATORY NETWORK; NONHUMAN; PROTEIN DNA BINDING; SEPALLATA3 GENE; CHROMATIN ASSEMBLY AND DISASSEMBLY; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; MADS DOMAIN PROTEINS; PROTEIN BINDING; TRANSCRIPTION FACTORS;

EID: 84899047963     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-3-r41     Document Type: Article

References (68)

1. Honma T, Goto K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 2001, 409:525-529. 10.1038/35054083, 11206550.
2. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 1992, 360:273-277. 10.1038/360273a0, 1359429.
3. Coen ES, Meyerowitz EM. The war of the whorls: genetic interactions controlling flower development. Nature 1991, 353:31-37. 10.1038/353031a0, 1715520.
4. Theissen G. Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 2001, 4:75-85. 10.1016/S1369-5266(00)00139-4, 11163172.
5. Smaczniak C, Immink RG, Muino JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S, Parcy F, Xu L, Carles CC, Angenent GC, Kaufmann K. Characterization of MADS-domain transcription factor complexes in arabidopsis flower development. Proc Natl Acad Sci U S A 2012, 109:1560-1565. 10.1073/pnas.1112871109, 3277181, 22238427.
6. Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 1935-1940, 2004:14.
7. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 2000, 405:200-203. 10.1038/35012103, 10821278.
8. Kaufmann K, Pajoro A, Angenent GC. Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 2010, 11:830-842. 10.1038/nrg2885, 21063441.
9. Smaczniak C, Immink RG, Angenent GC, Kaufmann K. Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 2012, 139:3081-3098. 10.1242/dev.074674, 22872082.
10. Sridhar VV, Surendrarao A, Liu Z. APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 2006, 133:3159-3166. 10.1242/dev.02498, 16854969.
11. Zhang W, Zhang T, Wu Y, Jiang J. Genome-wide identification of regulatory DNA elements and protein-binding footprints using signatures of open chromatin in Arabidopsis. Plant Cell 2012, 24:2719-2731. 10.1105/tpc.112.098061, 3426110, 22773751.
12. Liu C, Xi W, Shen L, Tan C, Yu H. Regulation of floral patterning by flowering time genes. Dev Cell 2009, 16:711-722. 10.1016/j.devcel.2009.03.011, 19460347.
13. Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in arabidopsis. Plant Cell 1990, 2:755-767. 159928, 2152125.
14. Song L, Crawford GE. DNase-seq: a high-resolution technique for mapping active gene regulatory elements across the genome from mammalian cells. Cold Spring Harb Protoc 2010, 2:pdb.prot5384.
15. Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar V, Serrano-Mislata A, Madueño F, Krajewski P, Meyerowitz EM, Angenent GC, Riechmann JL. Orchestration of floral initiation by APETALA1. Science 2010, 328:85-89. 10.1126/science.1185244, 20360106.
16. Segal E, Widom J. From DNA sequence to transcriptional behaviour: a quantitative approach. Nat Rev Genet 2009, 10:443-456. 2719885, 19506578.
17. Bardet AF, He Q, Zeitlinger J, Stark A. A computational pipeline for comparative ChIP-seq analyses. Nat Protoc 2012, 7:45-61.
18. He Q, Bardet AF, Patton B, Purvis J, Johnston J, Paulson A, Gogol M, Stark A, Zeitlinger J. High conservation of transcription factor binding and evidence for combinatorial regulation across six drosophila species. Nat Genet 2011, 43:414-420. 10.1038/ng.808, 21478888.
19. Byzova MV, Franken J, Aarts MG, de Almeida-Engler J, Engler G, Mariani C, van Lookeren Campagne MM, Angenent GC. Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development. Genes Dev 1999, 13:1002-1014. 10.1101/gad.13.8.1002, 316639, 10215627.
20. Sawa S, Watanabe K, Goto K, Liu YG, Shibata D, Kanaya E, Morita EH, Okada K. FILAMENTOUS FLOWER, a meristem and organ identity gene of arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev 1999, 13:1079-1088. 10.1101/gad.13.9.1079, 316944, 10323860.
21. Xu L, Xu Y, Dong A, Sun Y, Pi L, Huang H. Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 2003, 130:4097-4107. 10.1242/dev.00622, 12874130.
22. Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF. Control of cell proliferation in arabidopsis thaliana by microRNA miR396. Development 2010, 137:103-112. 10.1242/dev.043067, 2796936, 20023165.
23. Jones-Rhoades MW, Bartel DP. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 2004, 14:787-799. 10.1016/j.molcel.2004.05.027, 15200956.
24. Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR. Control of Flower Development in Arabidopsis-Thaliana by Apetala1 and Interacting Genes. Development 1993, 119:721-743.
25. Wuest SE, O'Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K, Lohan AJ, Loftus B, Graciet E, Wellmer F. Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc Natl Acad Sci U S A 2012, 109:13452-13457. 10.1073/pnas.1207075109, 3421202, 22847437.
26. MacArthur S, Li XY, Li J, Brown JB, Chu HC, Zeng L, Grondona BP, Hechmer A, Simirenko L, Keranen SV, Knowles DW, Stapleton M, Bickel P, Biggin MD, Eisen MB. Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol 2009, 10:R80. 10.1186/gb-2009-10-7-r80, 2728534, 19627575.
27. Shi JX, Malitsky S, De Oliveira S, Branigan C, Franke RB, Schreiber L, Aharoni A. SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLoS Genet 2011, 7:e1001388. 10.1371/journal.pgen.1001388, 3102738, 21637781.
28. Bowman JL, Smyth DR. CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 1999, 126:2387-2396.
29. Murmu J, Bush MJ, DeLong C, Li S, Xu M, Khan M, Malcolmson C, Fobert PR, Zachgo S, Hepworth SR. Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol 2010, 154:1492-1504. 10.1104/pp.110.159111, 2971623, 20805327.
30. Wu C. The 5′ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature 1980, 286:854-860. 10.1038/286854a0, 6774262.
31. Natarajan A, Yardimci GG, Sheffield NC, Crawford GE, Ohler U. Predicting cell-type-specific gene expression from regions of open chromatin. Genome Res 2012, 22:1711-1722. 10.1101/gr.135129.111, 3431488, 22955983.
32. Long JA, Moan EI, Medford JI, Barton MK. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 1996, 379:66-69. 10.1038/379066a0, 8538741.
33. Nole-Wilson S, Tranby TL, Krizek BA. AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol 2005, 57:613-628. 10.1007/s11103-005-0955-6, 15988559.
34. Kempin SA, Savidge B, Yanofsky MF. Molecular basis of the cauliflower phenotype in Arabidopsis. Science 1995, 267:522-525. 10.1126/science.7824951, 7824951.
35. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E, Vernot B, Thurman RE, John S, Sandstrom R, Johnson AK, Maurano MT, Humbert R, Rynes E, Wang H, Vong S, Lee K, Bates D, Diegel M, Roach V, Dunn D, Neri J, Schafer A, Hansen RS, Kutyavin T, Giste E, Weaver M, Canfield T, Sabo P, Zhang M, Balasundaram G, et al. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 2012, 489:83-90. 10.1038/nature11212, 3736582, 22955618.
36. Kaufmann K, Muino JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC. Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 2009, 7:e1000090. 2671559, 19385720.
37. Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES. FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci U S A 2011, 108:6680-6685. 10.1073/pnas.1103175108, 3081018, 21464308.
38. Monfared MM, Simon MK, Meister RJ, Roig-Villanova I, Kooiker M, Colombo L, Fletcher JC, Gasser CS. Overlapping and antagonistic activities of BASIC PENTACYSTEINE genes affect a range of developmental processes in Arabidopsis. Plant J 2011, 66:1020-1031. 10.1111/j.1365-313X.2011.04562.x, 21435046.
39. Simonini S, Roig-Villanova I, Gregis V, Colombo B, Colombo L, Kater MM. Basic pentacysteine proteins mediate MADS domain complex binding to the DNA for tissue-specific expression of target genes in Arabidopsis. Plant Cell 2012, 24:4163-4172. 10.1105/tpc.112.103952, 3517243, 23054472.
40. Zaret KS, Carroll JS. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 2011, 25:2227-2241. 10.1101/gad.176826.111, 3219227, 22056668.
41. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 2000, 288:1613-1616. 10.1126/science.288.5471.1613, 10834834.
42. Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM. Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet 2006, 2:e117. 10.1371/journal.pgen.0020117, 1523247, 16789830.
43. Soufi A, Donahue G, Zaret KS. Facilitators and impediments of the pluripotency reprogramming factors'initial engagement with the genome. Cell 2012, 151:994-1004. 10.1016/j.cell.2012.09.045, 3508134, 23159369.
44. Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 2007, 5:e129. 10.1371/journal.pbio.0050129, 1852588, 17439305.
45. Hesselberth JR, Chen X, Zhang Z, Sabo PJ, Sandstrom R, Reynolds AP, Thurman RE, Neph S, Kuehn MS, Noble WS, Fields S, Stamatoyannopoulos JA. Global mapping of protein-DNA interactions in vivo by digital genomic footprinting. Nat Methods 2009, 6:283-289. 10.1038/nmeth.1313, 2668528, 19305407.
46. Kaufmann K, Muino JM, Osteras M, Farinelli L, Krajewski P, Angenent GC. Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP). Nat Protoc 2010, 5:457-472. 10.1038/nprot.2009.244, 20203663.
47. Huala E, Dickerman AW, Garcia-Hernandez M, Weems D, Reiser L, LaFond F, Hanley D, Kiphart D, Zhuang M, Huang W, Mueller L, Bhattacharyya D, Bhaya D, Sobral B, Beavis B, Somerville C, Rhee SY. The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res 2001, 29:102-105. 10.1093/nar/29.1.102, 29827, 11125061.
48. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
49. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Li W, Liu XS. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9:R137. 10.1186/gb-2008-9-9-r137, 2592715, 18798982.
50. Muino JM, Kaufmann K, van Ham RC, Angenent GC, Krajewski P. ChIP-seq Analysis in R (CSAR): an R package for the statistical detection of protein-bound genomic regions. Plant Methods 2011, 7:11. 10.1186/1746-4811-7-11, 3114017, 21554688.
51. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
52. Payne RW, Murray DA, Harding SA, VSN I GenStat for Windows 2012, Hemel Hempstead: VSN International, 15, VSN I.
53. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842. 10.1093/bioinformatics/btq033, 2832824, 20110278.
54. Machanick P, Bailey TL. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 2011, 27:1696-1697. 10.1093/bioinformatics/btr189, 3106185, 21486936.
55. Smit AFA, Hubley R, Green P. RepeatMasker Open-3.0. 1996-2010. [http://www.repeatmasker.org].
56. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics 2011, 27:1017-1018. 10.1093/bioinformatics/btr064, 3065696, 21330290.
57. Pique-Regi R, Degner JF, Pai AA, Gaffney DJ, Gilad Y, Pritchard JK. Accurate inference of transcription factor binding from DNA sequence and chromatin accessibility data. Genome Res 2011, 21:447-455. 10.1101/gr.112623.110, 3044858, 21106904.
58. Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B. PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 2010, 38:D822-827. 10.1093/nar/gkp805, 2808933, 19858103.
59. Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005, 21:3448-3449. 10.1093/bioinformatics/bti551, 15972284.
60. Agilent technologies eArray. [https://earray.chem.agilent.com/earray/].
61. Weng L, Dai H, Zhan Y, He Y, Stepaniants SB, Bassett DE. Rosetta error model for gene expression analysis. Bioinformatics 2006, 22:1111-1121. 10.1093/bioinformatics/btl045, 16522673.
62. Pollard SK, Gilbert HN, Ge Y, Taylor S, Dudoit S. multtest: resampling-based multiple hypothesis testing. R package version 2.10.0. [http://www.bioconductor.org/packages/release/bioc/html/multtest.html].
63. Caldana C, Scheible WR, Mueller-Roeber B, Ruzicic S. A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 2007, 3:7. 10.1186/1746-4811-3-7, 1914063, 17559651.
64. Balazadeh S, Riano-Pachon DM, Mueller-Roeber B. Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol (Stuttg) 2008, 10:63-75.
65. Jarvis P, Chen LJ, Li H, Peto CA, Fankhauser C, Chory J. An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 1998, 282:100-103.
66. Wang JW, Schwab R, Czech B, Mica E, Weigel D. Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 2008, 20:1231-1243. 10.1105/tpc.108.058180, 2438454, 18492871.
67. Curtis MD, Grossniklaus U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 2003, 133:462-469. 10.1104/pp.103.027979, 523872, 14555774.
68. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998, 16:735-743. 10.1046/j.1365-313x.1998.00343.x, 10069079.