Programming of plant leaf senescence with temporal and inter-organellar coordination of transcriptome in arabidopsis

Plant Physiology

Volumn 171, Issue 1, 2016, Pages 452-467

  Woo, Hye Ryun ^a   Koo, Hee Jung ^b,c   Kim, Jeongsik ^b   Jeong, Hyobin ^b   Yang, Jin Ok ^d   Lee, Il Hwan ^b,c   Jun, Ji Hyung ^c   Choi, Seung Hee ^b,c   Park, Su Jin ^b,c   Kang, Byeongsoo ^b   Kim, You Wang ^b   Phee, Bong Kwan ^b   Kim, Jin Hee ^b   Seo, Chaehwa ^e   Park, Charny ^f   Kim, Sang Cheol ^d   Park, Seongjin ^d   Lee, Byungwook ^d   Lee, Sanghyuk ^f   Hwang, Daehee ^a,b   Nam, Hong Gil ^a,b   Lim, Pyung Ok ^a   more..

^a Daegu Gyeongbuk Institute of Science and Technology   (South Korea)

^b Institute for Basic Science   (South Korea)

^c Pohang University of Science and Technology (POSTECH)   (South Korea)

^d Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^e DNA Link Inc   (South Korea)

^f Ewha Womans University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; SMALL UNTRANSLATED RNA; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ARABIDOPSIS; CELL ORGANELLE; CHLOROPLAST; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; NUCLEIC ACID PROBE; PHYSIOLOGY; PLANT LEAF; PROCEDURES; TIME FACTOR;

ANTISENSE ELEMENTS (GENETICS); ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; ORGANELLES; PLANT LEAVES; RNA, SMALL UNTRANSLATED; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84964832457     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01929     Document Type: Article

References (81)

1. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18: 758-762
2. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221
3. Andrews S (2010) FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc
4. Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Mühlenbock P, Skirycz A, Gonzalez N, Beemster GT, et al (2012) Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev Cell 22: 64-78
5. Balazadeh S, Kwasniewski M, Caldana C, Mehrnia M, Zanor MI, Xue GP, Mueller-Roeber B (2011) ORS1, an H₂O₂-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol Plant 4: 346-360
6. Beemster GT, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inzé D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138: 734-743
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. Bonnet E, He Y, Billiau K, Van de Peer Y (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26: 1566-1568
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. Brown AV, Hudson KA (2015) Developmental profiling of gene expression in soybean trifoliate leaves and cotyledons. BMC Plant Biol 15: 169
11. Brown JB, Boley N, Eisman R, May GE, Stoiber MH, Duff MO, Booth BW, Wen J, Park S, Suzuki AM, et al (2014) Diversity and dynamics of the Drosophila transcriptome. Nature 512: 393-399
12. Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48: 181-199
13. Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39: W155-159
14. Debernardi JM, Rodriguez RE, Mecchia MA, Palatnik JF (2012) Functional specialization of the plant miR396 regulatory network through distinct microRNA-target interactions. PLoS Genet 8: e1002419
15. Del Sorbo MR, Balzano W, Donato M, Draghici S (2013) Assessing co-regulation of directly linked genes in biological networks using microarray time series analysis. Biosystems 114: 149-154
16. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210
17. Efroni I, Blum E, Goldshmidt A, Eshed Y (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20: 2293-2306
18. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498
19. Fenner M (1998) The phenology of growth and reproduction in plants. Perspect Plant Ecol Evol Syst 1: 78-91
20. Finley LW, Haigis MC (2009) The coordination of nuclear and mitochondrial communication during aging and calorie restriction. Ageing Res Rev 8: 173-188
21. Folkes L, Moxon S, Woolfenden HC, Stocks MB, Szittya G, Dalmay T, Moulton V (2012) PAREsnip: a tool for rapid genome-wide discovery of small RNA/target interactions evidenced through degradome sequencing. Nucleic Acids Res 40: e103
22. German MA, Pillay M, Jeong DH, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R, et al (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26: 941-946
23. Gomes AP, Price NL, Ling AJ, Moslehi JJ, Montgomery MK, Rajman L, White JP, Teodoro JS, Wrann CD, Hubbard BP, et al (2013) Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155: 1624-1638
24. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, et al (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471: 473-479
25. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10: 453-460
26. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46: 601-612
27. Hensel LL, Grbic V, Baumgarten DA, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in arabidopsis. Plant Cell 5: 553-564
28. Hickman R, Hill C, Penfold CA, Breeze E, Bowden L, Moore JD, Zhang P, Jackson A, Cooke E, Bewicke-Copley F, et al (2013) A local regulatory network around three NAC transcription factors in stress responses and senescence in Arabidopsis leaves. Plant J 75: 26-39
29. Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43: 68-78
30. Kim HJ, Hong SH, Kim YW, Lee IH, Jun JH, Phee BK, Rupak T, Jeong H, Lee Y, Hong BS, et al (2014a) Gene regulatory cascade of senescenceassociated NAC transcription factors activated by ETHYLENEINSENSITIVE2- mediated leaf senescence signalling in Arabidopsis. J Exp Bot 65: 4023-4036
31. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323: 1053-1057
32. Kim WC, Kim JY, Ko JH, Kang H, Kim J, Han KH (2014b) AtC3H14, a plant-specific tandem CCCH zinc-finger protein, binds to its target mRNAs in a sequence-specific manner and affects cell elongation in Arabidopsis thaliana. Plant J 80: 772-784
33. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39: D152-D157
34. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639-1645
35. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, et al (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40: D1202-D1210
36. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25
37. Leinonen R, Sugawara H, Shumway M; International Nucleotide Sequence Database Collaboration (2011) The sequence read archive. Nucleic Acids Res 39: D19-D21
38. Leopold AC (1961) Senescence in plant development: the death of plants or plant parts may be of positive ecological or physiological value. Science 134: 1727-1732
39. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP; 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079
40. Li Z, Peng J, Wen X, Guo H (2013) Ethylene-insensitive3 is a senescenceassociated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 25: 3311-3328
41. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58: 115-136
42. Lim PO, Lee IC, Kim J, Kim HJ, Ryu JS, Woo HR, Nam HG (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxinmediated leaf longevity. J Exp Bot 61: 1419-1430
43. Lin M, Pang C, Fan S, Song M, Wei H, Yu S (2015) Global analysis of the Gossypium hirsutum L. Transcriptome during leaf senescence by RNASeq. BMC Plant Biol 15: 43
44. Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1- like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6: 1859-1876
45. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449
46. Martin M (2011) Cutadapt removes adapter sequences from highthroughput sequencing reads. EMB J 17: 10-12
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. Nam HG (1997) The molecular genetic analysis of leaf senescence. Curr Opin Biotechnol 8: 200-207
49. Nath U, Crawford BC, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299: 1404-1407
50. Noodén LD (1988) The phenomenon of senescence and aging. In Senescence and Aging in Plants. eds Noodén LN, Leopold AC, Academic Press, San Diego, pp 1-50
51. Oh SA, Lee SY, Chung IK, Lee CH, Nam HG (1996) A senescenceassociated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol Biol 30: 739-754
52. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425: 257-263
53. Pesaresi P, Schneider A, Kleine T, Leister D (2007) Interorganellar communication. Curr Opin Plant Biol 10: 600-606
54. Pigliucci M (1998) Developmental phenotypic plasticity: where internal programming meets the external environment. Curr Opin Plant Biol 1: 87-91
55. Qiu K, Li Z, Yang Z, Chen J, Wu S, Zhu X, Gao S, Gao J, Ren G, Kuai B, Zhou X (2015) EIN3 and ORE1 accelerate degreening during ethylenemediated leaf senescence by directly activating chlorophyll catabolic genes in Arabidopsis. PLoS Genet 11: e1005399
56. Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137: 103-112
57. Samach A, Coupland G (2000) Time measurement and the control of flowering in plants. BioEssays 22: 38-47
58. Savitzky A, Golay MJE (1964) Smoothing and differentiation of data by simplified least squares procedures. Anal Chem 36: 1627
59. Smart CM (1994) Gene-expression during leaf senescence. DNA Res 126: 419-448
60. Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432
61. Soltow QA, Jones DP, Promislow DE (2010) A network perspective on metabolism and aging. Integr Comp Biol 50: 844-854
62. Sormani R, Masclaux-Daubresse C, Daniel-Vedele F, Chardon F (2011) Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana. PLoS One 6: e28070
63. Southworth LK, Owen AB, Kim SK (2009) Aging mice show a decreasing correlation of gene expression within genetic modules. PLoS Genet 5: e1000776
64. Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5: 537-542
65. Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74: 787-799
66. 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 38: 188-200
67. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111
68. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515
69. Tsai MH, Cook JA, Chandramouli GV, DeGraff W, Yan H, Zhao S, Coleman CN, Mitchell JB, Chuang EY (2007) Gene expression profiling of breast, prostate, and glioma cells following single versus fractionated doses of radiation. Cancer Res 67: 3845-3852
70. Tsukaya H (2013) Leaf development. Arabidopsis Book 11: e0163
71. Vardi N, Levy S, Gurvich Y, Polacheck T, Carmi M, Jaitin D, Amit I, Barkai N (2014) Sequential feedback induction stabilizes the phosphate starvation response in budding yeast. Cell Reports 9: 1122-1134
72. Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20: 759-771
73. Viñuela A, Snoek LB, Riksen JA, Kammenga JE (2010) Genome-wide gene expression regulation as a function of genotype and age in C. elegans. Genome Res 20: 929-937
74. Wang L, Gu X, Xu D, Wang W, Wang H, Zeng M, Chang Z, Huang H, Cui X (2011a) miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Exp Bot 62: 761-773
75. Wang XB, Jovel J, Udomporn P, Wang Y, Wu Q, Li WX, Gasciolli V, Vaucheret H, Ding SW (2011b) The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 23: 1625-1638
76. Wang Y, Henriksson E, Söderman E, Henriksson KN, Sundberg E, Engström P (2003) The Arabidopsis homeobox gene, ATHB16, regulates leaf development and the sensitivity to photoperiod in Arabidopsis. Dev Biol 264: 228-239
77. Wieland S, Thimme R, Purcell RH, Chisari FV (2004) Genomic analysis of the host response to hepatitis B virus infection. Proc Natl Acad Sci USA 101: 6669-6674
78. Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death -regulation by multiple layers of control and implications for aging in general. J Cell Sci 126: 4823-4833
79. Woo HR, Kim JH, Kim J, Kim J, Lee U, Song IJ, Kim JH, Lee HY, Nam HG, Lim PO (2010) The RAV1 transcription factor positively regulates leaf senescence in Arabidopsis. J Exp Bot 61: 3947-3957
80. Yilmaz A, Mejia-Guerra MK, Kurz K, Liang X, Welch L, Grotewold E (2011) AGRIS: the Arabidopsis Gene Regulatory Information Server, an update. Nucleic Acids Res 39: D1118-D1122
81. Zoschke R, Liere K, Börner T (2007) From seedling to mature plant: Arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. Plant J 50: 710-722