Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis

eLife

Volumn 2013, Issue 2, 2013, Pages

  Chang, Katherine Noelani ^a   Zhong, Shan ^b   Weirauch, Matthew T ^c   Hon, Gary ^d   Pelizzola, Mattia ^a,g   Li, Hai ^a   Carol Huang, Shao Shan ^a,e   Schmitz, Robert J ^a   Urich, Mark A ^a   Kuo, Dwight ^d   Nery, Joseph R ^a   Qiao, Hong ^a   Yang, Ally ^c   Jamali, Abdullah ^a   Chen, Huaming ^a   Ideker, Trey ^d   Ren, Bing ^d,f   Bar Joseph, Ziv ^a,b   Hughes, Timothy R ^c   Ecker, Joseph R ^a,e  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b Carnegie Mellon University   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLENE; GROWTH HORMONE; MESSENGER RNA; ETHYLENE DERIVATIVE; PHYTOHORMONE;

ARABIDOPSIS; ARTICLE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA MICROARRAY; GENETIC TRANSCRIPTION; LOSS OF FUNCTION MUTATION; NONHUMAN; PLANT DEVELOPMENT; PLANT GROWTH; POLYMERASE CHAIN REACTION; PROTEIN BINDING; RNA EXTRACTION; SEEDLING; SIGNAL TRANSDUCTION; GENETICS; METABOLISM;

ARABIDOPSIS; CHROMATIN IMMUNOPRECIPITATION; ETHYLENES; PLANT GROWTH REGULATORS; TRANSCRIPTION, GENETIC;

EID: 84879951956     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00675     Document Type: Article

References (75)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, et al. 2003a. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653-7. doi: 10.1126/science.1086391.
2. Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel FM, et al. 2003b. Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci USA 100:2992-7. doi: 10.1073/pnas.0438070100.
3. Amit I, Citri A, Shay T, Lu Y, Katz M, Zhang F, et al. 2007. A module of negative feedback regulators defines growth factor signaling. Nat Genet 39:503-12. doi: 10.1038/ng1987.
4. Arabidopsis Interactome Mapping Consortium. 2011. Evidence for network evolution in an Arabidopsis interactome map. Science 333:601-7. doi: 10.1126/science.1203877.
5. Avraham R, Yarden Y. 2011. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat Rev Mol Cell Biol 12:104-17. doi: 10.1038/nrm3048.
6. Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR, Jaeger SA, et al. 2009. Diversity and complexity in DNA recognition by transcription factors. Science 324:1720-3. doi: 10.1126/science.1162327.
7. Berger MF, Bulyk ML. 2009. Universal protein-binding microarrays for the comprehensive characterization of the DNA-binding specificities of transcription factors. Nat Protoc 4:393-411. doi: 10.1038/nprot.2008.195.
8. Berger MF, Badis G, Gehrke AR, Talukder S, Philippakis AA, Peña-Castillo L, et al. 2008. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133:1266-76. doi: 10.1016/j.cell.2008.05.024.
9. Berger MF, Philippakis AA, Qureshi AM, He FS, Estep PW, Bulyk ML. 2006. Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat Biotechnol 24:1429-35. doi: 10.1038/nbt1246.
10. Binder BM, Mortimore LA, Stepanova AN, Ecker JR, Bleecker AB. 2004a. Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent. Plant Physiol 136:2921-7. doi: 10.1104/pp.104.050393.
11. Binder BM, O'Malley RC, Wang W, Moore JM, Parks BM, Spalding EP, et al. 2004b. Arabidopsis seedling growth response and recovery to ethylene. A kinetic analysis. Plant Physiol 136:2913-20. doi: 10.1104/pp.104.050369.
12. Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, et al. 2010. Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107:14502-7. doi: 10.1073/pnas.1003347107.
13. Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR. 1997. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133-44. doi: 10.1016/S0092-8674(00)80300-1.
14. Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, et al. 2009. ETHYLENE INSENSITIVE3 and ethylene INSENSITIVE3-LIKE1 repress salicylic acid induction DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21:2527-40. doi: 10.1105/tpc.108.065193.
15. Chen Y-F, Shakeel SN, Bowers J, Zhao X-C, Etheridge N, Schaller GE. 2007. Ligand-induced degradation of the ethylene receptor ETR2 through a proteasome-dependent pathway in Arabidopsis. J Biol Chem 282:24752-8. doi: 10.1074/jbc.M704419200.
16. Chenna R. 2003. Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 31:3497-500. doi: 10.1093/nar/gkg500.
17. de Grauwe L, Vandenbussche F, Tietz O, Palme K, van der Straeten D. 2005. Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant Cell Physiol 46:827-36. doi: 10.1093/pcp/pci111.
18. Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES. 2011. FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci USA 108:6680-5. doi: 10.1073/pnas.1103175108.
19. Eddy SR. 2009. A new generation of homology search tools based on probabilistic inference. Genome Inform 23:205-11. doi: 10.1142/9781848165632_0019.
20. Ernst J, Vainas O, Harbison CT, Simon I, Bar-Joseph Z. 2007. Reconstructing dynamic regulatory maps. Mol Syst Biol 3:74. doi: 10.1038/msb4100115.
21. Fang X, Yoon J-G, Li L, Yu W, Shao J, Hua D, et al. 2011. The SOX2 response program in glioblastoma multiforme: an integrated ChIP-seq, expression microarray, and microRNA analysis. BMC Genomics 12:11. doi: 10.1186/1471-2164-12-11.
22. Feng Z, Lin M, Wu R. 2011. The regulation of aging and longevity: a new and complex role of p53. Genes Cancer 2:443-52. doi: 10.1177/1947601911410223.
23. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, et al. 2009. The Pfam protein families database. Nucleic Acids Res 38:D211-22. doi: 10.1093/nar/gkp985.
24. Foat BC, Morozov AV, Bussemaker HJ. 2006. Statistical mechanical modeling of genome-wide transcription factor occupancy data by MatrixREDUCE. Bioinformatics 22:e141-9. doi: 10.1093/bioinformatics/btl223.
25. Gao Z, Chen Y-F, Randlett MD, Zhao X-C, Findell JL, Kieber JJ, et al. 2003. Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes. J Biol Chem 278:34725-32. doi: 10.1074/jbc.M305548200.
26. Guo H, Ecker JR. 2003. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115:667-77. doi: 10.1016/S0092-8674(03)00969-3.
27. Hertz GZ, Stormo GD. 1999. Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 15:563-77. doi: 10.1093/bioinformatics/15.7.563.
28. Hiroi H. 2004. Temporal and spatial changes in transcription factor binding and histone modifications at the steroidogenic acute regulatory protein (stAR) locus associated with stAR transcription. Mol Endocrinol 18:791-806. doi: 10.1210/me.2003-0305.
29. Hou Y, Von Arnim AG, Deng XW. 1993. A new class of Arabidopsis constitutive photomorphogenic genes involved in regulating cotyledon development. Plant Cell 5:329-39. doi: 10.1105/tpc.5.3.329.
30. Immink RG, Posé D, Ferrario S, Ott F, Kaufmann K, Valentim FL, et al. 2012. Characterization of SOC1's central role in flowering by the identification of its upstream and downstream regulators. Plant Physiol 160:433-49. doi: 10.1104/pp.112.202614.
31. Iyer-Pascuzzi AS, Jackson T, Cui H, Petricka JJ, Busch W, Tsukagoshi H, et al. 2011. Cell identity regulators link development and stress responses in the Arabidopsis root. Dev Cell 21:770-82. doi: 10.1016/j.devcel.2011.09.009.
32. Kaufmann K, Muiño JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, et al. 2009. Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLOS Biol 7:e90. doi: 10.1371/journal.pbio.1000090.
33. Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar V, et al. 2010. Orchestration of floral initiation by APETALA1. Science 328:85-9. doi: 10.1126/science.1185244.
34. Kendrick M, Chang C. 2008. Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 11:479-85. doi: 10.1016/j.pbi.2008.06.011.
35. Kharchenko PV, Tolstorukov MY, Park PJ. 2008. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat Biotechnol 26:1351-9. doi: 10.1038/nbt.1508.
36. Konishi M, Yanagisawa S. 2008. Ethylene signaling in Arabidopsis involves feedback regulation via the elaborate control of EBF2 expression by EIN3. Plant J 5:821-31. doi: 10.1111/j.1365-313X.2008.03551.x.
37. Kosugi S, Ohashi Y. 2000. Cloning and DNA-binding properties of a tobacco ethylene-insensitive3 (EIN3) homolog. Nucleic Acids Res 28:960-7. doi: 10.1093/nar/28.4.960.
38. Lam KN, van Bakel H, Cote AG, van der Ven A, Hughes TR. 2011. Sequence specificity is obtained from the majority of modular C2H2 zinc-finger arrays. Nucleic Acids Res 39:4680-90. doi: 10.1093/nar/gkq1303.
39. Lehman A, Black R, Ecker JR. 1996. HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183-94. doi: 10.1016/S0092-8674(00)81095-8.
40. Lewis DR, Negi S, Sukumar P, Muday GK. 2011. Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138:3485-95. doi: 10.1242/dev.065102.
41. Leyser H, Lincoln C, Timpte C, Lammer D. 1993. Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364:161-4. doi: 10.1038/364161a0.
42. Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR. 2004. Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7:193-204. doi: 10.1016/j.devcel.2004.07.002.
43. Lickwar CR, Mueller F, Hanlon SE, McNally JG, Lieb JD. 2012. Genome-wide protein-DNA binding dynamics suggest a molecular clutch for transcription factor function. Nature 484:251-5. doi: 10.1038/nature10985.
44. Lippman Z, Gendrel A, Colot V. 2005. Profiling DNA methylation patterns using genomic tiling microarrays. Nat Methods 2:219-24. doi: 10.1038/nmeth0305-219.
45. Lister R, Omalley R, Tontifilippini J, Gregory B, Berry C, Millar A, et al. 2008. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523-36. doi: 10.1016/j.cell.2008.03.029.
46. Lumba S, Tsuchiya Y, Delmas F, Hezky J, Provart NJ, Lu QS, et al. 2012. The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis. BMC Biol 10:8. doi: 10.1186/1741-7007-10-8.
47. Macquarrie KL, Fong AP, Morse RH, Tapscott SJ. 2011. Genome-wide transcription factor binding: beyond direct target regulation. Trends Genet 27:141-8. doi: 10.1016/j.tig.2011.01.001.
48. Maere S. 2005. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448-9. doi: 10.1093/bioinformatics/bti551.
49. Mahony S, Benos PV. 2007. STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res 35:W253-8. doi: 10.1093/nar/gkm272.
50. Mahony S, Golden A, Smith TJ, Benos PV. 2005. Improved detection of DNA motifs using a self-organized clustering of familial binding profiles. Bioinformatics 21(suppl 1):i283-91. doi: 10.1093/bioinformatics/bti1025.
51. Mathieu O, Jasencakova Z, Vaillant I, Gendrel A-V, Colot V, Schubert I, et al. 2003. Changes in 5S rDNA chromatin organization and transcription during heterochromatin establishment in Arabidopsis. Plant Cell 15:2929-39. doi: 10.1105/tpc.017467.
52. Menet JS, Rodriguez J, Abruzzi KC, Rosbash M. 2012. Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. eLife 1:e00011. doi: 10.7554/eLife.00011.026.
53. Nemhauser JL, Hong F, Chory J. 2006. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467-75. doi: 10.1016/j.cell.2006.05.050.
54. Ni L, Bruce C, Hart C, Leigh-Bell J, Gelperin D, Umansky L, et al. 2009. Dynamic and complex transcription factor binding during an inducible response in yeast. Genes Dev 23:1351-63. doi: 10.1101/gad.1781909.
55. Ohto M-A, Hayashi S, Sawa S, Hashimoto-Ohta A, Nakamura K. 2006. Involvement of HLS1 in sugar and auxin signaling in Arabidopsis leaves. Plant Cell Physiol 47:1603-11. doi: 10.1093/pcp/pcl027.
56. Peng Z-Y, Zhou X, Li L, Yu X, Li H, Jiang Z, et al. 2008. Arabidopsis hormone database: a comprehensive genetic and phenotypic information database for plant hormone research in Arabidopsis. Nucleic Acids Res 37:D975-82. doi: 10.1093/nar/gkn873.
57. Rosenfeld N, Elowitz MB, Alon U. 2002. Negative autoregulation speeds the response times of transcription networks. J Mol Biol 323:785-93. doi: 10.1016/S0022-2836(02)00994-4.
58. Rozowsky J, Euskirchen G, Auerbach RK, Zhang ZD, Gibson T, Bjornson R, et al. 2009. PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nat Biotechnol 27:66-75. doi: 10.1038/nbt.1518.
59. Sessions RA, Zambryski PC. 1995. Arabidopsis gynoecium structure in the wild and in ettin mutants. Development 121:1519-32. http://dev.biologists.org/content/121/5/1519.long.
60. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13:2498-504. doi: 10.1101/gr.1239303.
61. Solano R, Stepanova A, Chao Q, Ecker JR. 1998. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12:3703-14. doi: 10.1101/gad.12.23.3703.
62. Sun Y, Fan X-Y, Cao D-M, Tang W, He K, Zhu J-Y, et al. 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:765-77. doi: 10.1016/j.devcel.2010.10.010.
63. Thibaud-Nissen F, Wu H, Richmond T, Redman JC, Johnson C, Green R, et al. 2006. Development of Arabidopsis whole-genome microarrays and their application to the discovery of binding sites for the TGA2 transcription factor in salicylic acid-treated plants. Plant J 47:152-62. doi: 10.1111/j.1365-313X.2006.02770.x.
64. Tsang J, Zhu J, van Oudenaarden A. 2007. MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26:753-67. doi: 10.1016/j.molcel.2007.05.018.
65. Vandenbussche F, Vaseva I, Vissenberg K, van der Straeten D. 2012. Ethylene in vegetative development: a tale with a riddle. New Phytol 194:895-909. doi: 10.1111/j.1469-8137.2012.04100.x.
66. Winter CM, Austin RS, Blanvillain-Baufumé S, Reback MA, Monniaux M, Wu MF, et al. 2011. LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev Cell 20:430-43. doi: 10.1016/j.devcel.2011.03.019.
67. Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, et al. 2010. Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETELA2. Plant Cell 22:2156-70. doi: 10.1105/tpc.110.075606.
68. Yilmaz A, Mejia-Guerra MK, Kurz K, Liang X, Welch L, Grotewold E. 2010. AGRIS: the Arabidopsis gene regulatory information server, an update. Nucleic Acids Res 39:D1118-22. doi: 10.1093/nar/gkq1120.
69. Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, et al. 2011. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65:634-46. doi: 10.1111/j.1365-313X.2010.04449.x.
70. Yosef N, Regev A. 2011. Impulse control: temporal dynamics in gene transcription. Cell 144:886-96. doi: 10.1016/j.cell.2011.02.015.
71. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. 2008. Model-based analysis of chip-seq (MACS). Genome Biol 9:R137. doi: 10.1186/gb-2008-9-9-r137.
72. Zhao Y, Stormo GD. 2011. Quantitative analysis demonstrates most transcription factors require only simple models of specificity. Nat Biotechnol 29:480-3. doi: 10.1038/nbt.1893.
73. Zhong S, Zhao M, Shi T, Shi H, An F, Zhao Q, et al. 2009. EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proc Natl Acad Sci USA 106:21431-6. doi: 10.1073/pnas.0907670106.
74. Zhu Z, An F, Feng Y, Li P, Xue L, Mu A, et al. 2011. Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108:12539-44. doi: 10.1073/pnas.1103959108.
75. Zinzen RP, Girardot C, Gagneur J, Braun M, Furlong EEM. 2009. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 461:65-70. doi: 10.1038/nature08531.