Senescence meets dedifferentiation

Plants

Volumn 4, Issue 3, 2015, Pages 356-368

  Rapp, Yemima Givaty ^a   Ransbotyn, Vanessa ^a   Grafi, Gideon ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Chromatin structure; Dedifferentiation; Reversal of senescence; Ribosome biogenesis; Senescence; Transposable elements

Indexed keywords

EID: 85041616065     PISSN: None     EISSN: 22237747     Source Type: Journal    
DOI: 10.3390/plants4030356     Document Type: Review

References (91)

1. Buchanan-Wollaston, V.; Earl, S.; Harrison, E.; Mathas, E.; Navabpour, S.; Page, T.; Pink, D. The molecular analysis of leaf senescence—A genomics approach. Plant Biotechnol. J. 2003, 1, 3–22.
2. Lim, P.O.; Kim, H.J.; Nam, H.G. Leaf senescence. Annu. Rev. Plant Biol. 2007, 58, 115–136.
3. Gepstein, S. Leaf senescence—Not just a “wear and tear” phenomenon. Genome Biol. 2004, 5, 212.
4. Lin, J.F.; Wu, S.H. Molecular events in senescing Arabidopsis leaves. Plant J. 2004, 39, 612–628.
5. Guo, Y.; Cai, Z.; Gan, S. Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ. 2004, 27, 521–549.
6. Andersson, A.; Keskitalo, J.; Sjödin, A.; Bhalerao, R.; Sterky, F.; Wissel, K.; Tandre, K.; Aspeborg, H.; Moyle, R.; Ohmiya, Y.; et al. A transcriptional timetable of autumn senescence. Genome Biol. 2004, 5, R24.
7. Breeze, E.; Harrison, E.; McHattie, S.; Hughes, L.; Hickman, R.; Hill, C.; Kiddle, S.; Kim, Y.S.; Penfold, C.A.; Jenkins, D.; et al. High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 2011, 23, 873–894.
8. Lev-Yadun, S.; Holopainen, J.K. Why red-dominated autumn leaves in America and yellow-dominated autumn leaves in Northern Europe? New Phytol. 2009, 183, 506–512.
9. Matile, P. Biochemistry of Indian summer: Physiology of autumnal leaf coloration. Exp. Gerontol. 2000, 35, 145–158.
10. Hoch, W.A.; Zeldin, E.L.; McCown, B.H.Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol. 2001, 21, 1–8.
11. Archetti, M.; Döring, T.F.; Hagen, S.B.; Hughes, N.M.; Leather, S.R.; Lee, D.W.; Lev-Yadun, S.; Manetas, Y.; Ougham, H.J.; Schaberg, P.G.; et al. Unravelling the evolution of autumn colours: An interdisciplinary approach. Trends Ecol. Evol. 2009, 24, 166–173.
12. Hadfield, K.A.; Bennett, A.B. Programmed senescence of plant organs. Cell Death Differ. 1997, 4, 662–670.
13. Jibran, R.; Hunter, D.A.; Dijkwel, P.P. Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Biol. 2013, 82, 547–561.
14. Zacarias, L.; Reid, M.S. Role of growth regulators in the senescence of Arabidopsis thaliana leaves. Physiol. Plant. 1990, 80, 549–554.
15. Guo, Y.; Gan S. Leaf senescence: Signals, execution, and regulation. Curr. Top. Dev. Biol. 2005, 71, 83–112.
16. Kim, J.; Chang, C.; Tucker, M.L. To grow old: Regulatory role of ethylene and jasmonic acid in senescence. Front. Plant Sci. 2015, 6, doi: 10.3389/fpls.2015.00020.
17. Richmond, A.E.; Lang, A. Effect of kinetin on protein content and survival of detached Xanthium leaves. Science 1957, 125, 650–651.
18. Goldthwaite, J.J.; Laetsch, W.M. Control of senescence in Rumex leaf discs by gibberellic acid. Plant Physiol. 1968, 43, 1855–1858.
19. Nooden, L.D.; Kahanak, G.M.; Okatan,Y. Prevention of monocarpic senescence in soybeans with auxin and cytokinin: An antidote for self-destruction. Science 1979, 206, 841–843.
20. Gan, S.; Amasino, R.M. Inhibition of leaf senescence by autoregulated production of cytokinin. Science 1995, 270, 1986–1988.
21. Ori, N.; Juarez, M.T.; Jackson, D.; Yamaguchi, J.; Banowetz, G.M.; Hake, S. Leaf senescence is delayed in tobacco plants expressing the maize homeobox gene knotted1 under the control of a senescence—Activated promoter. Plant Cell 1999, 11, 1073–1080.
22. Mandahar, C.L.; Suri, R.A. Cytokinin-like activity in green islands formed around infection spots of Alternaria brassicicola on mustard leaves in nature and their role in pathogenesis. Biol. Plant. 1987, 29, 76–79.
23. Giron, D.; Kaiser, W.; Imbault, N.; Casas, J. Cytokinin-mediated leaf manipulation by a leafminer caterpillar. Biol. Lett. 2007, 3, 340–343.
24. Fletcher, R.A.; Osborne, D.J. Gibberellin, as a regulator of protein and ribonucleic acid synthesis during senescence in leaf cells of Taraxacum officinale. Can. J. Bot. 1966, 44, 739–745.
25. Beevers, L. Effect of gibberellic acid on the senescence of leaf discs of Nasturtium (Tropaeolum majus). Plant Physiol. 1966, 41, 1074–1076.
26. Thomas, H. Senescence, ageing and death of the whole plant. New Phytol. 2013, 197, 696–711.
27. Wittenbach, V.A. Induced senescence of intact wheat seedlings and its reversibility Plant Phys. 1977, 59, 1038–1042.
28. Greening, M.T.; Butterfield, F.J.; Harris, N. Chloroplast ultrastructure during senescence and regreening of flax cotyledons. New Phytol. 1982, 92, 279–285.
29. Zavaleta-Mancera, H.A.; Thomas, B.J.; Thomas, H.; Scott, I.M. Regreening of senescent Nicotiana leaves. II. Redifferentiation of plastids. J. Exp. Bot. 1999, 50, 1683–1689.
30. Girardin, P.; Deltour, A.; Tollenaar, M. Effect of temporary N starvation in maize on leaf senescence. Can. J. Plant Sci. 1985, 65, 819–829.
31. Schildhauer, J.; Wiedemuth, K.; Humbeck, K. Supply of nitrogen can reverse senescence processes and affect expression of genes coding for plastidic glutamine synthetase and lysine-ketoglutarate reductase/saccharopine dehydrogenase. Plant Biol. 2008, 1, 76–84.
32. Balazadeh, S.; Schildhauer, J.; Araújo, W.L.; Munné-Bosch, S.; Fernie, A.R.; Proost, S.; Humbeck, K.; Mueller-Roeber, B. Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: Transcriptomic and metabolomic consequences. J. Exp. Bot. 2014, 65, 3975–3992.
33. Thomas, H.; Ougham, H.J.; Wagstaff, C.; Stead, A.D. Defining senescence and death. J. Exp. Bot. 2003, 54, 1127–1132.
34. Theise, N.D. New principles of cell plasticity. C. R. Biol. 2002, 325, 1039–1043.
35. Bloom, W. Cellular differentiation and tissue culture. Physiol. Rev. 1937, 17, 589–617.
36. Thornton, C.S. The histogenesis of muscle in the regenerating fore limb of larval Amblystoma punctatum. J. Morph. 1938, 62, 17–47.
37. Hay, E.D. Electron microscopic observations of muscle dedifferentiation in regenerating Amblystoma limbs. Dev. Biol. 1959, 1, 555–585.
38. Grafi, G.; Avivi, Y. Stem cells: A lesson from dedifferentiation. Trends Biotechnol. 2004, 22, 388–389.
39. McKay, R. Stem cells—Hype and hope. Nature 2000, 406, 361–364.
40. Zhao, J.; Morozova, N.; Williams, L.; Libs, L.; Avivi, Y.; Grafi, G. Two phases of chromatin decondensation during dedifferentiation of plant cells: Distinction between competence for cell fate switch and a commitment for S phase. J. Biol. Chem. 2001, 276, 22772–22778.
41. Grafi, G. How cells dedifferentiate: A lesson from plants. Dev. Biol. 2004, 268, 1–6.
42. Damri, M.; Granot, G.; Ben-Meir, H.; Avivi, Y.; Plaschkes, I.; Chalifa-Caspi, V.; Wolfson, M.; Fraifeld, V.; Grafi, G. Senescing cells share common features with dedifferentiating cells. Rejuvenation Res. 2009, 12, 435–443.
43. Grafi, G.; Chalifa-Caspi, V.; Nagar, T.; Plaschkes, I.; Barak, S.; Ransbotyn, V. Plant response to stress meets dedifferentiation. Planta 2011, 233, 433–438.
44. Gaspar-Maia, A.; Alajem, A.; Meshorer, E.; Ramalho-Santos, M. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 2011, 12, 36–47.
45. Grafi, G.; Florentin, A.; Ransbotyn, V.; Morgenstern, Y. The stem cell state in plant development and in response to stress. Front. Plant Sci. 2011, 2, doi: 10.3389/fpls.2011.00053.
46. MacRae, E.K.; Meetz, G.D. Electron microscopy of the ammoniacal silver reaction for histones in the erythropoietic cells of the chick. J. Cell Biol. 1970, 45, 235–245.
47. Murphy, M.J., Jr.; Bertles, J.F.; Gordon, A.S. Identifying characteristics of the haematopoietic precursor cell. J. Cell Sci. 1971, 9, 23–47.
48. Miura, A.B.; Shibata, A.; Akihama, T.; Endo, Y.; Saito, Y. Ultrastructure of developing erythrocytes. Tohoku J. Exp. Med. 1974, 112, 299–313.
49. Weintraub, H. The nucleosome repeat length increases during erythropoiesis in the chick. Nucleic Acids Res. 1978, 5, 1179–1188.
50. Robinson, P.J.; Rhodes, D. Structure of the ‘30 nm’ chromatin fibre: a key role for the linker histone. Curr. Opin. Struct. Biol. 2006, 16, 336–343.
51. Booker, C.E.; Dwivedi, R.S. Ultrastructure of meristematic cells of dormant and released buds in Tradescantia paludosa. Exp. Cell Res. 1973, 82, 255–261.
52. Yadav, R.K.; Girke, T.; Pasala, S.; Xie, M.; Reddy, G.V. Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc. Natl. Acad. Sci. USA 2009, 106, 4941–4946.
53. 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. Plant J. 2009, 58, 333–346.
54. Florentin, A.; Damri, M.; Grafi, G. Stress induces plant somatic cells to acquire some features of stem cells accompanied by selective chromatin reorganization. Dev. Dyn. 2013, 242, 1121–1133.
55. Pecinka, A.; Dinh, H.Q.; Baubec, T.; Rosa, M.; Lettner, N.; Mittelsten Scheid, O. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 2010, 22, 3118–3129.
56. Grafi, G.; Barak, S. Stress induces cell dedifferentiation in plants. Biochim. Biophys. Acta 2015, 1849, 378–384.
57. Halicka, H.D.; Zhao, H.; Podhorecka, M.; Traganos, F.; Darzynkiewicz, Z. Cytometric detection of chromatin relaxation, an early reporter of DNA damage response. Cell Cycle 2009, 8, 2233–2237.
58. Abrahan, C.E.; Insua, M.F.; Politi, L.E.; German, O.L.; Rotstein, N.P. Oxidative stress promotes proliferation and dedifferentiation of retina glial cells in vitro. J. Neurosci. Res. 2009, 87, 964–977.
59. Shoshani, O.; Zipori, D. Mammalian cell dedifferentiation as a possible outcome of stress. Stem Cell Rev. 2011, 7, 488–493.
60. Shoshani, O., Zipori, D. Stress as a fundamental theme in cell plasticity. Biochim. Biophys. Acta 2015, 1849, 371–377.
61. Williams, L.; Zhao, J.; Morozova, N.; Li, Y.; Avivi, Y.; Grafi, G. Chromatin reorganization accompanying cellular dedifferentiation is associated with modifications of histone H3, redistribution of HP1, and activation of E2F-target genes. Dev. Dyn. 2003, 228, 113–120.
62. Krul, W.R. Nucleic acid and protein metabolism of senescing and regenerating soybean cotyledons. Plant Physiol. 1974, 54, 36–40.
63. Makrides, S.C.; Goldthwaite, J. Biochemical changes during bean leaf growth, maturity and senescence: Contents of DNA, polyribosomes, ribosomal RNA, protein and chlorophyll. J. Exp. Bot. 1981, 32, 725–735.
64. Skadsen, R.W.; Cherry, J.H. Quantitative changes in in vitro and in vivo protein synthesis in aging and rejuvenated soybean cotyledons. Plant Physiol. 1983, 71, 861–868.
65. Srivastava, B.I.; Arglebe, C. Studies on ribosomes from barley leaves: Changes during senescence. Plant Physiol. 1967, 42, 1497–503.
66. Eilam, Y.; Butler, R.D.; Simon, E.W. Ribosomes and polysomes in cucumber leaves during growth and senescence. Plant Physiol. 1971, 47, 317–323.
67. Steeves, T.A.; Sussex, I.M. Analytical studies of the shoot apex. In Patterns in Plant Development; Cambridge University Press: Cambridge, NY, USA, 1989; pp. 62–85.
68. Cheung, T.H.; Rando, T.A. Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 2013, 14, 329–340.
69. Kidwell, M.G.; Lisch, D.R. Perspective: Transposable elements, parasitic DNA, and genome evolution. Evolution 2001, 55, 1–24.
70. Lisch, D. Epigenetic regulation of transposable elements in plants. Annu. Rev. Plant Biol. 2009, 60, 43–66.
71. Grandbastien, M.A. LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim. Biophys. Acta 2015, 1849, 403–416.
72. Zhu, W.; Kuo, D.; Nathanson, J.; Satoh, A.; Pao, G.M.; Yeo, G.W.; Bryant, S.V.; Voss, S.R.; Gardiner, D.M.; Hunter, T. Retrotransposon long interspersed nucleotide element-1 (LINE-1) is activated during salamander limb regeneration. Dev. Growth Differ. 2012, 54, 673–685.
73. Pearce, S.R.; Kumar, A.; Flavell, A.J. Activation of the Ty1-copia group retrotransposons of potato (Solanum tuberosum) during protoplast isolation. Plant Cell Rep. 1996, 15, 949–953.
74. Pouteau, S.; Huttner, E.; Grandbastien, M.A.; Caboche, M. Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J. 1991, 10, 1911–1918.
75. McClintock, B. The significance of responses of the genome to challenge. Science 1984, 226, 792–801.
76. Melayah, D.; Bonnivard, E.; Chalhoub, B.; Audeon, C.; Grandbastien, M.A. The mobility of the tobacco Tnt1 retrotransposon correlates with its transcriptional activation by fungal factors. Plant J. 2001, 28, 159–168.
77. Gepstein, S.; Glick, B.R. Strategies to ameliorate abiotic stress-induced plant senescence. Plant Mol. Biol. 2013, 82, 623–633.
78. Cantu, D.; Pearce, S.P.; Distelfeld, A.; Christiansen, M.W.; Uauy, C.; Akhunov, E.; Fahima, T.; Dubcovsky, J. Effect of the down-regulation of the high Grain Protein Content (GPC) genes on the wheat transcriptome during monocarpic senescence. BMC Genomics 2011, 12, doi: 10.1186/1471-2164-12-492492.
79. Eaton, C.J.; Cox, M.P.; Ambrose, B.; Becker, M.; Hesse, U.; Schardl, C.L.; Scott, B. Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiol. 2010, 153, 1780–1794.
80. Bundock, P.; Hooykaas, P. An Arabidopsis hAT-like transposase is essential for plant development. Nature 2005, 436, 282–284.
81. Macia, A.; Blanco-Jimenez, E.; García-Pérez, J.L. Retrotransposons in pluripotent cells: Impact and new roles in cellular plasticity. Biochim. Biophys. Acta 2015, 1849, 417–426.
82. Garcia-Perez, J.L.; Marchetto, M.C.; Muotri, A.R.; Coufal, N.G.; Gage, F.H.; O’Shea, K.S.; Moran, J.V. LINE-1 retrotransposition in human embryonic stem cells. Hum. Mol. Genet. 2007, 16, 1569–1577.
83. Wissing, S.; Muñoz-Lopez, M.; Macia, A.; Yang, Z.; Montano, M.; Collins, W.; Garcia-Perez, J.L.; Moran, J.V.; Greene, W.C. Reprogramming somatic cells into iPS cells activates LINE-1 retroelement mobility. Hum. Mol. Genet. 2012, 21, 208–218.
84. Wallace, N.A.; Belancio, V.P.; Deininger, P. L1 mobile element expression causes multiple types of toxicity. Gene 2008, 419, 75–81.
85. Belgnaoui, S.M.; Gosden, R.G.; Semmes, O.J.; Haoudi, A. Human LINE-1 retrotransposon induces DNA damage and apoptosis in cancer cells. Cancer Cell Int. 2006, 6, doi: 10.1186/1475-2867-6-13.
86. Gasior, S.L.; Wakeman, T.P.; Xu, B.; Deininger, P.L. The human LINE-1 retrotransposon creates DNA double-strand breaks. J. Mol. Biol. 2006, 357, 1383–1393.
87. De Cecco, M.; Criscione, S.W.; Peckham, E.J.; Hillenmeyer, S.; Hamm, E.A.; Manivannan, J.; Peterson, A.L.; Kreiling, J.A.; Neretti, N.; Sedivy, J.M. Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell 2013, 12, 247–256.
88. Wang, J.; Geesman, G.J.; Hostikka, S.L.; Atallah, M.; Blackwell, B.; Lee, E.; Cook, P.J.; Pasaniuc, B.; Shariat, G.; Halperin, E.; et al. Inhibition of activated pericentromeric SINE/Alu repeat transcription in senescent human adult stem cells reinstates self-renewal. Cell Cycle 2011, 10, 3016–3030.
89. Tessadori, F.; Chupeau, M.C.; Chupeau, Y.; Knip, M.; Germann, S.; van Driel, R.; Fransz, P.; Gaudin, V. Large-scale dissociation and sequential reassembly of pericentric heterochromatin in dedifferentiated Arabidopsis cells. J. Cell Sci. 2007, 120, 1200–1208.
90. Grafi, G. Stress cycles in stem cells/iPSCs development: Implications for tissue repair. Biogerontology 2013, 14, 603–608.
91. Larkin, P.J.; Scowcroft, W.R. Somaclonal variation—A novel source of variability from cell cultures for plant improvement. Theor. Appl. Genet. 1981, 60, 197–214.