Advertisement

Journal of Plant Research

, Volume 128, Issue 3, pp 399–405 | Cite as

Cell cycle reentry from the late S phase: implications from stem cell formation in the moss Physcomitrella patens

  • Masaki IshikawaEmail author
  • Mitsuyasu Hasebe
JPR Symposium Reprogramming of plant cells as adaptive strategies

Abstract

Differentiated cells are in a non-dividing, quiescent state, but some differentiated cells can reenter the cell cycle in response to appropriate stimuli. Quiescent cells are generally arrested at the G0/G1 phase, reenter the cell cycle, and progress to the S phase to replicate their genomic DNA. On the other hand, some types of cells are arrested at the different phase and reenter the cell cycle from there. In the moss Physcomitrella patens, the differentiated leaf cells of gametophores formed in the haploid generation contain approximately 2C DNA content, and DNA synthesis is necessary for reentry into the cell cycle, which is suggested to be arrested at late S phase. Here we review various cell-division reactivation processes in which cells reenter the cell cycle from the late S phase, and discuss possible mechanisms of such unusual cell cycle reentries with special emphasis on Physcomitrella.

Keywords

Cell cycle DNA synthesis Physcomitrella Wounding 

Notes

Acknowledgments

We thank Drs. Y. Tamada and I. Imai for critical reading of the manuscript, and Liechi Zhang for providing photographs of an excised leaf. This work was partially supported by the Japan Science and Technology Agency ERATO Program and the Ministry of Education, Culture, Sports, Science and Technology (No. 25291067 to M. H. and M. I.).

References

  1. Alt FW, Kellems RE, Bertino JR, Schimke RT (1978) Selective multiplication of dihydrofolate reductase genes in methotrexate-resistant variants of cultured murine cells. J Biol Chem 253:1357–1370PubMedGoogle Scholar
  2. Banks JA et al (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–963CrossRefPubMedCentralPubMedGoogle Scholar
  3. Beeckman T, Burssens S, Inze D (2001) The peri-cell-cycle in Arabidopsis. J Exp Bot 52:403–411CrossRefPubMedGoogle Scholar
  4. Beerman I, Seita J, Inlay MA, Weissman IL, Rossi DJ (2014) Quiescent hematopoietic stem cells accumulate DNA damage during aging that is repaired upon entry into cell cycle. Cell Stem Cell 15:37–50CrossRefPubMedGoogle Scholar
  5. Berger C, Pallavi SK, Prasad M, Shashidhara LS, Technau GM (2005) A critical role for cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster. Nat Cell Biol 7:56–62CrossRefPubMedGoogle Scholar
  6. Blakely LM, Evans TA (1979) Cell dynamics studies on the pericycle of radish seedling roots. Plant Sci Lett 14:79–83CrossRefGoogle Scholar
  7. Cao L, Peng B, Yao L, Zhang X, Sun K, Yang X, Yu L (2010) The ancient function of RB–E2F pathway: insights from its evolutionary history. Biol Direct 5:55CrossRefPubMedCentralPubMedGoogle Scholar
  8. Casimiro I et al (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171CrossRefPubMedGoogle Scholar
  9. Chen T, Dent SY (2014) Chromatin modifiers and remodellers: regulators of cellular differentiation. Nat Rev Genet 15:93–106CrossRefPubMedCentralPubMedGoogle Scholar
  10. Chen-Kiang S (2003) Cell-cycle control of plasma cell differentiation and tumorigenesis. Immunol Rev 194:39–47CrossRefPubMedGoogle Scholar
  11. Cionini PG, Zolfino C, Cavallini A (1985) Extra DNA synthesis in the dedifferentiating cells of Vicia faba roots. Protoplasma 124:213–218CrossRefGoogle Scholar
  12. Costanzo M et al (2004) CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast. Cell 117:899–913CrossRefPubMedGoogle Scholar
  13. Cove DJ (1992) Regulation of development in the moss, Physcomitrella patens. In: Russo VE, Brody S, Cove DJ, Ottolenghi S (eds) Development: the molecular genetic approach. Spring-Verlag, Berlin, pp 179–193CrossRefGoogle Scholar
  14. Cove DJ, Knight CD (1993) The moss Physcomitrella patens, a model system with potential for the study of plant reproduction. Plant Cell 5:1483–1488CrossRefPubMedCentralPubMedGoogle Scholar
  15. Cove D, Bezanilla M, Harries P, Quatrano R (2006) Mosses as model systems for the study of metabolism and development. Annu Rev Plant Biol 57:497–520CrossRefPubMedGoogle Scholar
  16. Cross FR, Buchler NE, Skotheim JM (2011) Evolution of networks and sequences in eukaryotic cell cycle control. Philos Trans R Soc B 366:3532–3544CrossRefGoogle Scholar
  17. De Veylder L, Beeckman T, Inze D (2007) The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 8:655–665CrossRefPubMedGoogle Scholar
  18. den Boer BG, Murray JA (2000) Triggering the cell cycle in plants. Trends Cell Biol 10:245–250CrossRefGoogle Scholar
  19. Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627CrossRefPubMedCentralPubMedGoogle Scholar
  20. Gaamouche T et al (2010) Cyclin-dependent kinase activity maintains the shoot apical meristem cells in an undifferentiated state. Plant J 64:26–37PubMedGoogle Scholar
  21. Gutierrez C, Ramirez-Parra E, Castellano MM, del Pozo JC (2002) G1 to S transition: more than a cell cycle engine switch. Curr Opin Plant Biol 5:480–486CrossRefPubMedGoogle Scholar
  22. Hajkova P et al (2008) Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452:877–881CrossRefPubMedGoogle Scholar
  23. Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP, Surani MA (2010) Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329:78–82CrossRefPubMedGoogle Scholar
  24. Hyldig SM, Croxall N, Contreras DA, Thomsen PD, Alberio R (2011) Epigenetic reprogramming in the porcine germ line. BMC Dev Biol 11:11CrossRefPubMedCentralPubMedGoogle Scholar
  25. Ide S, Miyazaki T, Maki H, Kobayashi T (2010) Abundance of ribosomal RNA gene copies maintains genome integrity. Science 327:693–696CrossRefPubMedGoogle Scholar
  26. Ishikawa M et al (2011) Physcomitrella cyclin-dependent kinase A links cell cycle reactivation to other cellular changes during reprogramming of leaf cells. Plant Cell 23:2924–2938CrossRefPubMedCentralPubMedGoogle Scholar
  27. Kaufmann K, Pajoro A, Angenent GC (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 11:830–842CrossRefPubMedGoogle Scholar
  28. Klein G, Klein E (1986) Conditioned tumorigenicity of activated oncogenes. Cancer Res 46:3211–3224PubMedGoogle Scholar
  29. Kobayashi T, Ganley AR (2005) Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309:1581–1584CrossRefPubMedGoogle Scholar
  30. Kofuji R, Hasebe M (2014) Eight types of stem cells in the life cycle of the moss Physcomitrella patens. Curr Opin Plant Biol 17:13–21CrossRefPubMedGoogle Scholar
  31. Kotogany E, Dudits D, Horvath GV, Ayaydin F (2010) A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine. Plant Methods 6:5CrossRefPubMedCentralPubMedGoogle Scholar
  32. Lee TJ et al (2010) Arabidopsis thaliana chromosome 4 replicates in two phases that correlate with chromatin state. PLoS Genet 6:e1000982CrossRefPubMedCentralPubMedGoogle Scholar
  33. Leon J, Rojo E, Sanchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1–9CrossRefPubMedGoogle Scholar
  34. Matsui A, Ihara T, Suda H, Mikami H, Semba K (2013) Gene amplification: mechanisms and involvement in cancer. Biomol Concepts 4:567–582CrossRefPubMedGoogle Scholar
  35. Menand B, Calder G, Dolan L (2007) Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens. J Exp Bot 58:1843–1849CrossRefPubMedGoogle Scholar
  36. Menges M, de Jager SM, Gruissem W, Murray JA (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41:546–566CrossRefPubMedGoogle Scholar
  37. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefPubMedGoogle Scholar
  38. Molyneaux K, Wylie C (2004) Primordial germ cell migration. Int J Dev Biol 48:537–544CrossRefPubMedGoogle Scholar
  39. Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marin MI, Martinez-Macias MI, Ariza RR, Roldan-Arjona T (2006) DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc Natl Acad Sci USA 103:6853–6858CrossRefPubMedCentralPubMedGoogle Scholar
  40. Nakagami H, Sekine M, Murakami H, Shinmyo A (1999) Tobacco retinoblastoma-related protein phosphorylated by a distinct cyclin-dependent kinase complex with Cdc2/cyclin D in vitro. Plant J 18:243–252CrossRefPubMedGoogle Scholar
  41. Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A (2002) Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobacco. Plant Cell 14:1847–1857CrossRefPubMedCentralPubMedGoogle Scholar
  42. Natali L, Cavallini A, Cremonini R, Bassi P, Cionini PG (1986) Amplification of nuclear DNA sequences during induced plant cell dedifferentiation. Cell Differ 18:157–161CrossRefPubMedGoogle Scholar
  43. Pajalunga D, Mazzola A, Franchitto A, Puggioni E, Crescenzi M (2008) The logic and regulation of cell cycle exit and reentry. Cell Mol Life Sci 65:8–15CrossRefPubMedGoogle Scholar
  44. Pauklin S, Vallier L (2013) The cell-cycle state of stem cells determines cell fate propensity. Cell 155:135–147CrossRefPubMedCentralPubMedGoogle Scholar
  45. Petruk S et al (2012) TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150:922–933CrossRefPubMedCentralPubMedGoogle Scholar
  46. Planchais S, Glab N, Inze D, Bergounioux C (2000) Chemical inhibitors: a tool for plant cell cycle studies. FEBS Lett 476:78–83CrossRefPubMedGoogle Scholar
  47. Polyn S, Willems A, De Veylder L (2014) Cell cycle entry, maintenance, and exit during plant development. Curr Opin Plant Biol 23:1–7CrossRefPubMedGoogle Scholar
  48. Rensing SA et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69CrossRefPubMedGoogle Scholar
  49. Rogers SO, Bendich AJ (1987a) Heritability and variability in ribosomal RNA genes of Vicia faba. Genetics 117:285–295PubMedCentralPubMedGoogle Scholar
  50. Rogers SO, Bendich AJ (1987b) Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer. Plant Mol Biol 9:509–520CrossRefPubMedGoogle Scholar
  51. Saitou M, Kagiwada S, Kurimoto K (2012) Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 139:15–31CrossRefPubMedGoogle Scholar
  52. Schween G, Gorr G, Hohe A, Reski R (2003) Unique tissue-specific cell cycle in Physcomitrella. Plant Biol (Stuttg) 5:50–58CrossRefGoogle Scholar
  53. Seki Y et al (2007) Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 134:2627–2638CrossRefPubMedGoogle Scholar
  54. Shulaev V, Oliver DJ (2006) Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol 141:367–372CrossRefPubMedCentralPubMedGoogle Scholar
  55. Singh AM et al (2013) Cell-cycle control of developmentally regulated transcription factors accounts for heterogeneity in human pluripotent cells. Stem Cell Rep 1:532–544CrossRefGoogle Scholar
  56. Sugiyama M, Yeung E, Shoji Y, Komamine A (1995) Possible involvement of DNA-repair events in the transdifferentiation of mesophyll cells of Zinnia elegans into tracheary elements. J Plant Res 85:351–361CrossRefGoogle Scholar
  57. Surani MA, Hajkova P (2010) Epigenetic reprogramming of mouse germ cells toward totipotency. Cold Spring Harb Symp Quant Biol 75:211–218CrossRefPubMedGoogle Scholar
  58. Sustar A, Schubiger G (2005) A transient cell cycle shift in Drosophila imaginal disc cells precedes multipotency. Cell 120:383–393CrossRefPubMedGoogle Scholar
  59. Takata M et al (1998) Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J 17:5497–5508CrossRefPubMedCentralPubMedGoogle Scholar
  60. Takebayashi S, Sugimura K, Saito T, Sato C, Fukushima Y, Taguchi H, Okumura K (2005) Regulation of replication at the R/G chromosomal band boundary and pericentromeric heterochromatin of mammalian cells. Exp Cell Res 304:162–174CrossRefPubMedGoogle Scholar
  61. Tsubouchi T et al (2013) DNA synthesis is required for reprogramming mediated by stem cell fusion. Cell 152:873–883CrossRefPubMedCentralPubMedGoogle Scholar
  62. Weinberg RA (1995) The retinoblastoma protein and cell cycle control. Cell 81:323–330CrossRefPubMedGoogle Scholar
  63. White EJ et al (2004) DNA replication-timing analysis of human chromosome 22 at high resolution and different developmental states. Proc Natl Acad Sci USA 101:17771–17776CrossRefPubMedCentralPubMedGoogle Scholar
  64. Zavitz KH, Zipursky SL (1997) Controlling cell proliferation in differentiating tissues: genetic analysis of negative regulators of G1→S-phase progression. Curr Opin Cell Biol 9:773–781CrossRefPubMedGoogle Scholar
  65. Zetterberg A, Larsson O, Wiman KG (1995) What is the restriction point? Curr Opin Cell Biol 7:835–842CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  1. 1.National Institute for Basic BiologyOkazakiJapan
  2. 2.Department of Basic Biology, School of Life ScienceSOKENDAI (The Graduate University for Advanced Studies)OkazakiJapan

Personalised recommendations