A genome-wide chronological study of gene expression and two histone modifications, H3K4me3 and H3K9ac, during developmental leaf senescence

Plant Physiology

Volumn 168, Issue 4, 2015, Pages 1246-1261

  Brusslan, Judy A ^a   Bonora, Giancarlo ^b   Rus Canterbury, Ana M ^a   Tariq, Fayha ^a   Jaroszewicz, Artur ^b   Pellegrini, Matteo ^b  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

HISTONE; PLANT RNA;

ARABIDOPSIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTONE CODE; METABOLISM; METHYLATION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT GENOME; PLANT LEAF; SEQUENCE ANALYSIS; TIME FACTOR; UPREGULATION;

ARABIDOPSIS; BASE SEQUENCE; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; HISTONE CODE; HISTONES; METHYLATION; MOLECULAR SEQUENCE DATA; PLANT LEAVES; RNA, PLANT; SEQUENCE ANALYSIS, RNA; TIME FACTORS; UP-REGULATION;

EID: 84939153785     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.252999     Document Type: Article

References (72)

1. Adrian J, Farrona S, Reimer JJ, Albani MC, Coupland G, Turck F (2010) cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22: 1425-1440
2. Alvarez-Venegas R, Abdallat AA, Guo M, Alfano JR, Avramova Z (2007) Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2: 106-113
3. Anders S, Pyl PT, Huber W (2015) HTSeq: a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169
4. Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Müllner AE, Luschnig C (2010) Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proc Natl Acad Sci USA 107: 10308-10313
5. Ay N, Irmler K, Fischer A, Uhlemann R, Reuter G, Humbeck K (2009) Epigenetic programming via histone methylation at WRKY53 controls leaf senescence in Arabidopsis thaliana. Plant J 58: 333-346
6. Benayoun BA, Pollina EA, Ucar D, Mahmoudi S, Karra K, Wong ED, Devarajan K, Daugherty AC, Kundaje AB, Mancini E, et al (2014) H3K4me3 breadth is linked to cell identity and transcriptional consistency. Cell 158: 673-688
7. Besseau S, Li J, Palva ET (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J Exp Bot 63: 2667-2679
8. Bradbury CA, Khanim FL, Hayden R, Bunce CM, White DA, Drayson MT, Craddock C, Turner BM (2005) Histone deacetylases in acute myeloid leukaemia show a distinctive pattern of expression that changes selectively in response to deacetylase inhibitors. Leukemia 19: 1751-1759
9. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, et al (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23: 873-894
10. Brusslan JA, Rus Alvarez-Canterbury AM, Nair NU, Rice JC, Hitchler MJ, Pellegrini M (2012) Genome-wide evaluation of histone methylation changes associated with leaf senescence in Arabidopsis. PLoS ONE 7: e33151
11. Chambers J, Cleveland W, Kleiner B, Tukey P (1983) Graphical Methods for Data Analysis. Wadsworth International Group, Belmont, CA
12. Charron JBF, He H, Elling AA, Deng XW (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21: 3732-3748
13. De Cecco M, Criscione SW, Peterson AL, Naeretti N, Sedivy JM, Kreiling JA (2013) Transposable elements become active and mobile in the genomes of aging mammalian somatic tissues. Aging 5: 867-883
14. Ding Y, Ndamukong I, Xu Z, Lapko H, Fromm M, Avramova Z (2012) ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes. PLoS Genet 8: e1003111
15. Guan Q, Yue X, Zeng H, Zhu J (2014) The protein phosphatase RCF2 and its interacting partner NAC019 are critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis. Plant Cell 26: 438- 453
16. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10: 453-460
17. Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27: 521-549
18. Guo Y, Gan SS (2012) Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ 35: 644-655
19. Higashi K, Ishiga Y, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2008) Modulation of defense signal transduction by flagellin-induced WRKY41 transcription factor in Arabidopsis thaliana. Mol Genet Genomics 279: 303-312
20. Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213: 469-473
21. Hou K, Wu W, Gan SS (2013) SAUR36, a SMALL AUXIN UP RNA gene, is involved in the promotion of leaf senescence in Arabidopsis. Plant Physiol 161: 1002-1009
22. Humbeck K (2013) Epigenetic and small RNA regulation of senescence. Plant Mol Biol 82: 529-537
23. Jaskiewicz M, Conrath U, Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12: 50-55
24. Jiang Y, Liang G, Yang S, Yu D (2014) Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell 26: 230-245
25. Johnson NL, Kotz S, Kemp AW (1992) Univariate Discrete Distributions. Wiley, New York
26. Katari MS, Nowicki SD, Aceituno FF, Nero D, Kelfer J, Thompson LP, Cabello JM, Davidson RS, Goldberg AP, Shasha DE, et al (2010) VirtualPlant: a software platform to support systems biology research. Plant Physiol 152: 500-515
27. Kim DH, Doyle MR, Sung S, Amasino RM (2009a) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25: 277- 299
28. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009b) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323: 1053-1057
29. KimJM, To TK, Ishida J, Matsui A, Kimura H, SekiM(2012) Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol 53: 847-856
30. Kim JM, To TK, Ishida J, Morosawa T, KawashimaM,Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008) Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49: 1580-1588
31. Kim JM, To TK, Nishioka T, Seki M (2010) Chromatin regulation functions in plant abiotic stress responses. Plant Cell Environ 33: 604-611
32. Kim YS, Sakuraba Y, Han SH, Yoo SC, Paek NC (2013) Mutation of the Arabidopsis NAC016 transcription factor delays leaf senescence. Plant Cell Physiol 54: 1660-1672
33. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast andmemoryefficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25
34. Lauberth SM, Nakayama T, Wu X, Ferris AL, Tang Z, Hughes SH, Roeder RG (2013) H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 152: 1021-1036
35. Li W, Prazak L, Chatterjee N, Gruninger S, Krug L, Theodorou D, Dubnau J (2013a) Activation of transposable elements during aging and neuronal decline in Drosophila. Nat Neurosci 16: 529-531
36. Li Z, Peng J, Wen X, Guo H (2012) Gene network analysis and functional studies of senescence-associated genes reveal novel regulators of Arabidopsis leaf senescence. J Integr Plant Biol 54: 526-539
37. Li Z, Peng J, Wen X, Guo H (2013b) Ethylene-insensitive3 is a senescenceassociated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 25: 3311-3328
38. Lim PO, Kim HJ, Nam HG (2007a) Leaf senescence. Annu Rev Plant Biol 58: 115-136
39. Lim PO, Kim Y, Breeze E, Koo JC, Woo HR, Ryu JS, Park DH, Beynon J, Tabrett A, Buchanan-Wollaston V, et al (2007b) Overexpression of a chromatin architecture-controlling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. Plant J 52: 1140-1153
40. Liu X, Li Z, Jiang Z, Zhao Y, Peng J, Jin J, Guo H, Luo J (2011) LSD: a leaf senescence database. Nucleic Acids Res 39: D1103-D1107
41. López-González L, Mouriz A, Narro-Diego L, Bustos R, Martínez-Zapater M, Jarillo JA, Piñeiro M (2014) Chromatin-Dependent Repression of the Arabidopsis Floral Integrator Genes Involves Plant Specific PHD-Containing Proteins. Plant Cell 26: 3922-3938
42. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol 15: 550
43. Malapeira J, Khaitova LC, Mas P (2012) Ordered changes in histone modifications at the core of the Arabidopsis circadian clock. Proc Natl Acad Sci USA 109: 21540-21545
44. Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, et al (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci USA 108: 18512-18517
45. Matallana-Ramirez LP, Rauf M, Farage-Barhom S, Dortay H, Xue GP, Dröge-Laser W, Lers A, Balazadeh S, Mueller-Roeber B (2013) NAC transcription factor ORE1 and senescence-induced BIFUNCTIONAL NUCLEASE1 (BFN1) constitute a regulatory cascade in Arabidopsis. Mol Plant 6: 1438-1452
46. Miao Y, Jiang J, Ren Y, Zhao Z (2013) The single-stranded DNA-binding protein WHIRLY1 represses WRKY53 expression and delays leaf senescence in a developmental stage-dependent manner in Arabidopsis. Plant Physiol 163: 746-756
47. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55: 853-867
48. Miao Y, Zentgraf U (2010) A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J 63: 179-188
49. Molitor AM, Bu Z, Yu Y, Shen WH (2014) Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet 10: e1004091
50. Nightingale KP, Gendreizig S, White DA, Bradbury C, Hollfelder F, Turner BM (2007) Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J Biol Chem 282: 4408-4416
51. Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 12: 527-535
52. Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43: 29-46
53. Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogenindependent induction of defense-related genes. Plant Mol Biol 40: 267- 278
54. Roudier F, Ahmed I, Bérard C, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D, Caillieux E, Duvernois-Berthet E, Al-Shikhley L, et al (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30: 1928-1938
55. Schenke D, Cai D, Scheel D (2014) Suppression of UV-B stress responses by flg22 is regulated at the chromatin level via histone modification. Plant Cell Environ 37: 1716-1721
56. Sequeira-Mendes J, Aragüez I, Peiró R, Mendez-Giraldez R, Zhang X, Jacobsen SE, Bastolla U, Gutierrez C (2014) The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell 26: 2351-2366
57. Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inzé D, Peer WA, Murphy AS, Overvoorde PJ, Gray WM (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J 70: 978-990
58. Spartz AK, Ren H, Park MY, Grandt KN, Lee SH, Murphy AS, Sussman MR, Overvoorde PJ, Gray WM (2014) SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell explansion in Arabidopsis. Plant Cell 26: 2129-2142
59. Stepanova AN, Yun J, Robles LM, Novak O, He W, Guo H, Ljung K, Alonso JM (2011) The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23: 3961-3973
60. Taverna SD, Ueberheide BM, Liu Y, Tackett AJ, Diaz RL, Shabanowitz J, Chait BT, Hunt DF, Allis CD (2007) Long-distance combinatorial linkage between methylation and acetylation on histone H3 N termini. Proc Natl Acad Sci USA 104: 2086-2091
61. Thatcher SR, Burd S, Wright C, Lers A, Green PJ (2015) Differential expression of miRNAs and their target genes in senescing leaves and siliques: insights from deep sequencing of small RNAs and cleaved target RNAs. Plant Cell Environ 33: 188-200
62. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111 van der
63. Graaff E, Schwacke R, Schneider A, Desimone M, Flügge UI, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141: 776-792
64. van Dijk K, Ding Y, Malkaram S, Riethoven JJ, Liu R, Yang J, Laczko P, Chen H, Xia Y, Ladunga I, et al (2010) Dynamic changes in genomewide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol 10: 238
65. Wang Y, Bouwmeester K, van de Mortel JE, Shan W, Govers F (2013) A novel Arabidopsis-oomycete pathosystem: differential interactions with Phytophthora capsici reveal a role for camalexin, indole glucosinolates and salicylic acid in defence. Plant Cell Environ 36: 1192-1203
66. Won C, Shen X,Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci USA 108: 18518-18523
67. Wu K, Zhang L, Zhou C, Yu CW, Chaikam V (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59: 225-234
68. Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10: R62
69. Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE (2007) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5: e129
70. Zheng MS, Takahashi H, Miyazaki A, Hamamoto H, Shah J, Yamaguchi I, Kusano T (2004) Up-regulation of Arabidopsis thaliana NHL10 in the hypersensitive response to Cucumber mosaic virus infection and in senescing leaves is controlled by signalling pathways that differ in salicylate involvement. Planta 218: 740-750
71. Zhou J, Wang X, He K, Charron JBF, Elling AA, Deng XW (2010) Genomewide profiling of histone H3 lysine 9 acetylation and dimethylation in Arabidopsis reveals correlation between multiple histone marks and gene expression. Plant Mol Biol 72: 585-595
72. Zong W, Zhong X, You J, Xiong L (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol Biol 81: 175-188