A mutation in plant-specific SWI2/SNF2-Like chromatin-remodeling proteins, DRD1 and DDM1, delays leaf senescence in arabidopsis thaliana

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Cho, Eun Ju ^a   Choi, Seung Hee ^a   Kim, Ji Hong ^a   Kim, Ji Eun ^a   Lee, Min Hee ^a   Chung, Byung Yeoup ^a   Woo, Hye Ryun ^b   Kim, Jin Hong ^a,c  

^a Korea Atomic Energy Research Institute   (South Korea)

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

^c University of Science and Technology (UST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; ARTICLE; CENTROMERIC REPEAT; CHLOROPHYLL CONTENT; DDM1 GENE; DRD1 GENE; EPIGENETICS; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; GENETIC ASSOCIATION; GENETIC PARAMETERS; LEAF SENESCENCE; NONHUMAN; PHOTOSYNTHESIS; PLANT GENE; PROTEIN CONTENT; PROTEIN FUNCTION; TRANSCRIPTIONALLY SILENT INFORMATION REPEAT; WILD TYPE; ARABIDOPSIS; CENTROMERE; CHEMISTRY; CHROMATIN; CLUSTER ANALYSIS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY; PLANT LEAF; ULTRASTRUCTURE;

ARABIDOPSIS PROTEIN; CHLOROPHYLL; CHROMATIN; DDM1 PROTEIN, ARABIDOPSIS; DNA BINDING PROTEIN; DNA DIRECTED RNA POLYMERASE; DRD1 PROTEIN, ARABIDOPSIS; RNA; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CENTROMERE; CHLOROPHYLL; CHROMATIN; CLUSTER ANALYSIS; DNA-BINDING PROTEINS; DNA-DIRECTED RNA POLYMERASES; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOME-WIDE ASSOCIATION STUDY; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAVES; RNA; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84954419010     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0146826     Document Type: Article

References (58)

1. Lim PO, Nam HG. The molecular and genetic control of leaf senescence and longevity in Arabidopsis. Current topics in developmental biology. 2005; 67:49-83. doi: 10.1016/S0070-2153(05)67002-0 PMID: 15949531.
2. Lim PO, Kim HJ, Nam HG. Leaf senescence. Annual review of plant biology. 2007; 58:115-36. doi: 10.1146/annurev.arplant.57.032905.105316 PMID: 17177638.
3. Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, et al. Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. The Plant cell. 2007; 19(4):1362-75. doi: 10.1105/tpc.106.042911 PMID: 17416733.
4. Kuriyama H, Fukuda H. Developmental programmed cell death in plants. Current opinion in plant biology. 2002; 5(6):568-73. PMID: 12393021.
5. Obara K, Kuriyama H, Fukuda H. Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant physiology. 2001; 125(2):615-26. PMID: 11161019.
6. Breeze E, Harrison E, Page T, Warner N, Shen C, Zhang C, et al. Transcriptional regulation of plant senescence: from functional genomics to systems biology. Plant biology. 2008; 10 Suppl 1:99-109. doi: 10.1111/j.1438-8677.2008.00076.x PMID: 18721315.
7. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, et al. The molecular analysis of leaf senescence-a genomics approach. Plant biotechnology journal. 2003; 1(1):3-22. doi: 10.1046/j.1467-7652.2003.00004.x PMID: 17147676.
8. Hinderhofer K, Zentgraf U. Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta. 2001; 213(3):469-73. PMID: 11506370.
9. Miao Y, Laun T, Zimmermann P, Zentgraf U. Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant molecular biology. 2004; 55(6):853-67. doi: 10.1007/s11103-004-2142-6PMID: 15604721.
10. Zentgraf U, Laun T, Miao Y. The complex regulation of WRKY53 during leaf senescence of Arabidopsis thaliana. European journal of cell biology. 2010; 89(2-3):133-7. doi: 10.1016/j.ejcb.2009.10.014 PMID: 20004496.
11. Ay N, Irmler K, Fischer A, Uhlemann R, Reuter G, Humbeck K. Epigenetic programming via histone methylation at WRKY53 controls leaf senescence in Arabidopsis thaliana. The Plant journal: for cell and molecular biology. 2009; 58(2):333-46. doi: 10.1111/j.1365-313X.2008.03782.x PMID: 19143996.
12. Wilson VL, Jones PA. DNA methylation decreases in aging but not in immortal cells. Science. 1983; 220(4601):1055-7. PMID: 6844925.
13. Chinnusamy V, Zhu JK. Epigenetic regulation of stress responses in plants. Current opinion in plant biology. 2009; 12(2):133-9. doi: 10.1016/j.pbi.2008.12.006 PMID: 19179104.
14. Lim PO, Kim Y, Breeze E, Koo JC, Woo HR, Ryu JS, et al. Overexpression of a chromatin architecturecontrolling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. The Plant journal: for cell and molecular biology. 2007; 52(6):1140-53. doi: 10.1111/j.1365-313X.2007.03317.x PMID: 17971039.
15. Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJ. Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Current biology: CB. 2004; 14(9):801- 5. doi: 10.1016/j.cub.2004.04.037PMID: 15120073.
16. Kanno T, Aufsatz W, Jaligot E, Mette MF, Matzke M, Matzke AJ. A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO reports. 2005; 6(7):649-55. doi: 10.1038/sj.embor.7400446PMID: 15947783.
17. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJ, Matzke M. Endogenous targets of RNAdirected DNA methylation and Pol IV in Arabidopsis. The EMBO journal. 2006; 25(12):2828-36. doi: 10.1038/sj.emboj.7601150 PMID: 16724114.
18. Chan SW, Henderson IR, Jacobsen SE. Gardening the genome: DNA methylation in Arabidopsis thaliana. Nature reviews Genetics. 2005; 6(5):351-60. doi: 10.1038/nrg1601 PMID: 15861207.
19. Vongs A, Kakutani T, Martienssen RA, Richards EJ. Arabidopsis thaliana DNA methylation mutants. Science. 1993; 260(5116):1926-8. PMID: 8316832.
20. Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, et al. Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant physiology. 2009; 149(2):885- 93. doi:10.1104/pp.108.130013 PMID: 19074627.
21. Liu W, Saint DA. A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics. Analytical biochemistry. 2002; 302 (1):52-9. PMID: 11846375.
22. Lichtenthaler HK. [34] Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in enzymology. 1987;(148C: ):350-82.
23. Kruger NJ. The Bradford method for protein quantitation. Basic protein and peptide protocols: Springer; 1994. p. 9-15.
24. Kim J-H, Lee MH, Moon YR, Kim J-S, Wi SG, Kim TH, et al. Characterization of metabolic disturbances closely linked to the delayed senescence of Arabidopsis leaves after γ irradiation. Environmental and experimental botany. 2009; 67(2):363-71.
25. Suorsa M, Regel RE, Paakkarinen V, Battchikova N, Herrmann RG, Aro EM. Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. European journal of biochemistry/FEBS. 2004; 271(1):96-107. PMID: 14686923.
26. Kim J-H, Lee C-H. In vivo deleterious effects specific to reactive oxygen species on photosystem I and II after photo-oxidative treatments of rice (Oryza sativa L.) leaves. Plant science. 2005; 168(4):1115-25.
27. Chan SW, Henderson IR, Zhang X, Shah G, Chien JS, Jacobsen SE. RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS genetics. 2006; 2(6):e83. doi: 10.1371/journal.pgen.0020083 PMID: 16741558.
28. Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG. Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. The Plant Journal. 1997; 12(3):527-35. PMID: 9351240.
29. Park SY, Yu JW, Park JS, Li J, Yoo SC, Lee NY, et al. The senescence-induced staygreen protein regulates chlorophyll degradation. The Plant cell. 2007; 19(5): 1649-64. doi: 10.1105/tpc.106.044891 PMID: 17513504.
30. Bate NJ, Rothstein SJ, Thompson JE. Expression of nuclear and chloroplast photosynthesis-specific genes during leaf senescence. Journal of experimental botany. 1991; 42(6):801-11.
31. Hortensteiner S. Chlorophyll degradation during senescence. Annual review of plant biology. 2006; 57:55-77. doi: 10.1146/annurev.arplant.57.032905.105212 PMID: 16669755.
32. Holton TA, Cornish EC. Genetics and Biochemistry of Anthocyanin Biosynthesis. The Plant cell. 1995; 7(7):1071-83. doi: 10.1105/tpc.7.7.1071 PMID: 12242398.
33. Hoch WA, Singsaas EL, McCown BH. Resorption protection. Anthocyanins facilitate nutrient recovery in autumn by shielding leaves from potentially damaging light levels. Plant physiology. 2003; 133 (3):1296-305. doi: 10.1104/pp.103.027631 PMID: 14526111.
34. Matile P, Hortensteiner S, Thomas H. Chlorophyll Degradation. Annual review of plant physiology and plant molecular biology. 1999; 50:67-95. doi: 10.1146/annurev.arplant.50.1.67 PMID: 15012204.
35. Pruzinska A, Tanner G, Anders I, Roca M, Hortensteiner S. Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100(25):15259-64. doi: 10.1073/pnas.2036571100PMID: 14657372.
36. Folly P, Engel N. Chlorophyll b to chlorophyll a conversion precedes chlorophyll degradation in Hordeum vulgare L. The Journal of biological chemistry. 1999; 274 (31):21811-6. PMID: 10419497.
37. Roberts DR, Thompson JE, Dumbroff EB, Gepstein S, Mattoo AK. Differential changes in the synthesis and steady-state levels of thylakoid proteins during bean leaf senescence. Plant molecular biology. 1987; 9(4):343-53. doi: 10.1007/BF00014909PMID: 24277087.
38. Noodén LD, Guiamét JJ, John I. Senescence mechanisms. Physiologia plantarum. 1997; 101(4):746- 53.
39. Mae T, Kai N, Makino A, Ohira K. Relation between ribulose bisphosphate carboxylase content and chloroplast number in naturally senescing primary leaves of wheat. Plant and cell physiology. 1984; 25 (2):333-6.
40. Feller U, Anders I, Mae T. Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. Journal of experimental botany. 2008; 59(7):1615-24. doi: 10.1093/jxb/erm242 PMID: 17975207.
41. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, et al. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. The Plant journal: for cell and molecular biology. 2005; 42(4):567-85. doi: 10.1111/j.1365-313X.2005.02399.x PMID: 15860015.
42. Guo Y, Cai Z, Gan S. Transcriptome of Arabidopsis leaf senescence. Plant, cell & environment. 2004; 27(5):521-49.
43. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, et al. High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. The Plant cell. 2011; 23 (3):873-94. doi: 10.1105/tpc.111.083345 PMID: 21447789.
44. Gentry M, Hennig L. Remodelling chromatin to shape development of plants. Experimental cell research. 2014; 321(1):40-6. doi: 10.1016/j.yexcr.2013.11.010 PMID: 24270012.
45. Han SK, Sang Y, Rodrigues A, Biol F, Wu MF, Rodriguez PL, et al. The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in Arabidopsis. The Plant cell. 2012; 24(12):4892-906. doi:10.1105/tpc.112.105114 PMID: 23209114.
46. Shaked H, Avivi-Ragolsky N, Levy AA. Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics. 2006; 173(2):985-94. doi: 10.1534/genetics.105.051664 PMID: 16547115.
47. Singhal RP, Mays-Hoopes LL, Eichhorn GL. DNA methylation in aging of mice. Mechanisms of ageing and development. 1987; 41(3):199-210. PMID: 3431172.
48. Sedivy JM, Banumathy G, Adams PD. Aging by epigenetics-a consequence of chromatin damage? Experimental cell research. 2008; 314(9):1909-17. doi: 10.1016/j.yexcr.2008.02.023 PMID: 18423606.
49. He XJ, Chen T, Zhu JK. Regulation and function of DNA methylation in plants and animals. Cell research. 2011; 21(3):442-65. doi: 10.1038/cr.2011.23 PMID: 21321601.
50. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell. 2006; 126(6):1189-201. doi: 10.1016/j.cell.2006.08.003 PMID: 16949657.
51. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nature genetics. 2007; 39(1):61-9. doi: 10.1038/ng1929 PMID: 17128275.
52. Steimer A, Amedeo P, Afsar K, Fransz P, Mittelsten Scheid O, Paszkowski J. Endogenous targets of transcriptional gene silencing in Arabidopsis. The Plant cell. 2000; 12(7):1165-78. PMID: 10899982.
53. Ay N, Janack B, Humbeck K. Epigenetic control of plant senescence and linked processes. Journal of experimental botany. 2014; 65(14):3875-87. doi: 10.1093/jxb/eru132 PMID: 24683182.
54. Tsuchiya T, Eulgem T. An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(37):E3535-43. doi: 10.1073/pnas.1312545110 PMID: 23940361.
55. Bilichak A, Ilnystkyy Y, Hollunder J, Kovalchuk I. The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PloS one. 2012; 7(1):e30515. doi: 10.1371/journal.pone.0030515 PMID: 22291972.
56. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, et al. Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(32):E2183-91. doi: 10.1073/pnas.1209329109 PMID: 22733782.
57. Pontvianne F, Abou-Ellail M, Douet J, Comella P, Matia I, Chandrasekhara C, et al. Nucleolin is required for DNA methylation state and the expression of rRNA gene variants in Arabidopsis thaliana. PLoS genetics. 2010; 6(11):e1001225. doi: 10.1371/journal.pgen.1001225 PMID: 21124873.
58. Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MF, Yariv I, et al. Large-scale identification of leaf senescence-associated genes. The Plant journal: for cell and molecular biology. 2003; 36(5):629-42. PMID: 14617064.