Advertisement

Plant Molecular Biology

, Volume 77, Issue 6, pp 537–545 | Cite as

Plant MCM proteins: role in DNA replication and beyond

  • Narendra TutejaEmail author
  • Ngoc Quang Tran
  • Hung Quang Dang
  • Renu Tuteja
Review

Abstract

Mini-chromosome maintenance (MCM) proteins form heterohexameric complex (MCM2–7) to serve as licensing factor for DNA replication to make sure that genomic DNA is replicated completely and accurately once during S phase in a single cell cycle. MCMs were initially identified in yeast for their role in plasmid replication or cell cycle progression. Each of six MCM contains highly conserved sequence called “MCM box”, which contains two ATPase consensus Walker A and Walker B motifs. Studies on MCM proteins showed that (a) the replication origins are licensed by stable binding of MCM2–7 to form pre-RC (pre-replicative complex) during G1 phase of the cell cycle, (b) the activation of MCM proteins by CDKs (cyclin-dependent kinases) and DDKs (Dbf4-dependent kinases) and their helicase activity are important for pre-RC to initiate the DNA replication, and (c) the release of MCMs from chromatin renders the origins “unlicensed”. DNA replication licensing in plant is, in general, less characterized. The MCMs have been reported from Arabidopsis, maize, tobacco, pea and rice, where they are found to be highly expressed in dividing tissues such as shoot apex and root tips, localized in nucleus and cytosol and play important role in DNA replication, megagametophyte and embryo development. The identification of six MCM coding genes from pea and Arabidopsis suggest six distinct classes of MCM protein in higher plant, and the conserved function right across the eukaryotes. This overview of MCMs contains an emphasis on MCMs from plants and the novel role of MCM6 in abiotic stress tolerance.

Keywords

Cell cycle Pre-replicative complex (pre-RC) DNA replication licensing Licensing factor Mini-chromosome maintenance (MCM) 

Abbreviations

CDC6

Cell division cycle 6

CDT1

Cdc10-dependent transcript 1

DDKs

Dbf4-dependent kinases

E2F

Adenovirus E2 promoter factor

ETG

E2F target genes

HIF-1

Hypoxia-inducible factor 1

MCM

Mini-chromosome maintenance

ORC

Origin recognition complex

PRL

PROLIFERA

RBR

Retinoblastoma-related genes

ROA

Replication origin activator

Notes

Acknowledgments

Work on DNA replication and plant stress signaling in Tuteja’s Laboratory is supported by Department of Biotechnology (DBT), Government of India.

References

  1. Aparicio T, Ibarra A, Mendez J (2006) Cdc45-MCM-GINS, a new power player for DNA replication. Cell Div 1:18PubMedCrossRefGoogle Scholar
  2. Arias RS, Filichkin SA, Strauss SH (2006) Divide and conquer: development and cell cycle genes in plant transformation. Trends Biotechnol 24(6):267–273PubMedCrossRefGoogle Scholar
  3. Bastida M, Puigdomenech P (2002) Specific expression of ZmPRL, the maize homolog of MCM7, during early embryogenesis. Plant Sci 162:97–106CrossRefGoogle Scholar
  4. Bell SP (2002) The origin recognition complex: from simple origins to complex functions. Genes Dev 16(6):659–672PubMedCrossRefGoogle Scholar
  5. Bell SP, Dutta A (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71:333–374PubMedCrossRefGoogle Scholar
  6. Blow JJ, Dutta A (2005) Preventing re-replication of chromosomal DNA. Nat Rev Mol Cell Biol 6(6):476–486PubMedCrossRefGoogle Scholar
  7. Boyer JS (1982) Plant productivity and environment. Science 218(4571):443–448PubMedCrossRefGoogle Scholar
  8. Bryant JA, Aves SJ (2011) Initiation of DNA replication: functional and evolutionary aspects. Ann Bot 107(7):1119–1126PubMedCrossRefGoogle Scholar
  9. Bryant JA, Moore K, Aves SJ (2001) Origins and complexes: the initiation of DNA replication. J Exp Bot 52(355):193–202PubMedCrossRefGoogle Scholar
  10. Castellano MM, del Pozo JC, Ramirez-Parra E, Brown S, Gutierrez C (2001) Expression and stability of Arabidopsis CDC6 are associated with endoreplication. Plant Cell 13(12):2671–2686PubMedCrossRefGoogle Scholar
  11. Castellano MM, Boniotti MB, Caro E, Schnittger A, Gutierrez C (2004) DNA replication licensing affects cell proliferation or endoreplication in a cell type-specific manner. Plant Cell 16(9):2380–2393CrossRefGoogle Scholar
  12. Cho JH, Kim HB, Kim HS, Choi SB (2008) Identification and characterization of a rice MCM2 homologue required for DNA replication. BMB Rep 41(8):581–586PubMedCrossRefGoogle Scholar
  13. Coleman TR, Carpenter PB, Dunphy WG (1996) The xenopus Cdc6 protein is essential for the initiation of a single round of DNA replication in cell-free extracts. Cell 87(1):53–63PubMedCrossRefGoogle Scholar
  14. Costa A, Pape T, van Heel M, Brick P, Patwardhan A, Onesti S (2006) Structural basis of the Methanothermobacter thermautotrophicus MCM helicase activity. Nucl Acids Res 34(20):5829–5838PubMedCrossRefGoogle Scholar
  15. Costas C, de la Paz Sanchez M, Stroud H, Yu Y, Oliveros JC, Feng S, Benguria A, Lopez-Vidriero I, Zhang X, Solano R, Jacobsen SE, Gutierrez C (2011) Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat Struct Mol Biol 18(3):395–400PubMedCrossRefGoogle Scholar
  16. Dambrauskas G, Aves SJ, Bryant JA, Francis D, Rogers HJ (2003) Genes encoding two essential DNA replication activation proteins, Cdc6 and Mcm3, exhibit very different patterns of expression in the tobacco BY-2 cell cycle. J Exp Bot 54(383):699–706PubMedCrossRefGoogle Scholar
  17. Dang HQ, Tran NQ, Gill SS, Tuteja R, Tuteja N (2011) A single subunit MCM6 from pea promotes salinity stress tolerance without affecting yield. Plant Mol Biol 76(1–2):19–34PubMedCrossRefGoogle Scholar
  18. De Veylder L, Larkin JC, Schnittger A (2011) Molecular control and function of endoreplication in development and physiology. Trends Plant Sci. PMID:21889902. [Epub ahead of print]Google Scholar
  19. Dita AM, Rispail N, Prats E, Rubiales D, Singh KB (2006) Biotechnology approaches to overcome biotic and abiotic stress constraints in legumes. Euphytica 147:1–24CrossRefGoogle Scholar
  20. Dresselhaus T, Srilunchang KO, Leljak-Levanic D, Schreiber DN, Garg P (2006) The fertilization-induced DNA replication factor MCM6 of maize shuttles between cytoplasm and nucleus, and is essential for plant growth and development. Plant Physiol 140(2):512–527PubMedCrossRefGoogle Scholar
  21. Duderstadt KE, Berger JM (2008) AAA+ ATPases in the initiation of DNA replication. Crit Rev Biochem Mol Biol 43(3):163–187PubMedCrossRefGoogle Scholar
  22. Dyson T (1999) World food trends and prospects to 2025. Proc Natl Acad Sci USA 96(11):5929–5936PubMedCrossRefGoogle Scholar
  23. Edwards MC, Tutter AV, Cvetic C, Gilbert CH, Prokhorova TA, Walter JC (2002) MCM2–7 complexes bind chromatin in a distributed pattern surrounding the origin recognition complex in xenopus egg extracts. J Biol Chem 277(36):33049–33057PubMedCrossRefGoogle Scholar
  24. Fitch MJ, Donato JJ, Tye BK (2003) Mcm7, a subunit of the presumptive MCM helicase, modulates its own expression in conjunction with Mcm1. J Biol Chem 278(28):25408–25416PubMedCrossRefGoogle Scholar
  25. Fu YV, Yardimci H, Long DT, Ho TV, Guainazz A, Bermudez VP, Hurwitz J, van Oijen A, Schärer OD, Walter JC (2011) Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146(6):931–941PubMedCrossRefGoogle Scholar
  26. Gordon-Kamm W, Dilkes BP, Lowe K, Hoerster G, Sun X, Ross M, Church L, Bunde C, Farrell J, Hill P, Maddock S, Snyder J, Sykes L, Li Z, Woo YM, Bidney D, Larkins BA (2002) Stimulation of the cell cycle and maize transformation by disruption of the plant retinoblastoma pathway. Proc Natl Acad Sci USA 99(18):11975–11980PubMedCrossRefGoogle Scholar
  27. Hirano H, Harashima H, Shinmyo A, Sekine M (2008) Arabidopsis RETINOBLASTOMA-RELATED PROTEIN 1 is involved in G1 phase cell cycle arrest caused by sucrose starvation. Plant Mol Biol 66(3):259–275PubMedCrossRefGoogle Scholar
  28. Holding DR, Springer PS (2002) The Arabidopsis gene PROLIFERA is required for proper cytokinesis during seed development. Planta 214(3):373–382PubMedCrossRefGoogle Scholar
  29. Huang X, Springer PS, Kaloshian I (2003) Expression of the Arabidopsis MCM Gene PROLIFERA during root-knot and cyst nematode infection. Phytopathology 93(1):35–41PubMedCrossRefGoogle Scholar
  30. Hubbi ME, Luo W, Baek JH, Semenza GL (2011) MCM proteins are negative regulators of hypoxia-inducible factor 1. Mol cell 42(5):700–712PubMedCrossRefGoogle Scholar
  31. Kim JS, Kim KA, Oh TR, Park CM, Kang H (2008) Functional characterization of DEAD-box RNA helicases in Arabidopsis thaliana under abiotic stress conditions. Plant Cell Physiol 49(10):1563–1571PubMedCrossRefGoogle Scholar
  32. Lee TJ, Pascuzzi PE, Settlage SB, Shultz RW, Tanurdzic M, Rabinowicz PD, Menges M, Zheng P, Main D, Murray JA, Sosinski B, Allen GC, Martienssen RA, Hanley-Bowdoin L, Vaughn MW, Thompson WF (2010) Arabidopsis thaliana chromosome 4 replicates in two phases that correlate with chromatin state. PLoS Genet 6(6):e1000982PubMedCrossRefGoogle Scholar
  33. Lei M, Kawasaki Y, Tye BK (1996) Physical interactions among Mcm proteins and effects of Mcm dosage on DNA replication in Saccharomyces cerevisiae. Mol Cell Biol 16(9):5081–5090PubMedGoogle Scholar
  34. Liang DT, Hodson JA, Forsburg SL (1999) Reduced dosage of a single fission yeast MCM protein causes genetic instability and S phase delay. J Cell Sci 112(Pt 4):559–567PubMedGoogle Scholar
  35. Liu HH, Liu J, Fan SL, Song MZ, Han XL, Liu F, Shen FF (2008) Molecular cloning and characterization of a salinity stress-induced gene encoding DEAD-box helicase from the halophyte Apocynum venetum. J Exp Bot 59(3):633–644PubMedCrossRefGoogle Scholar
  36. Luo Y, Liu YB, Dong YX, Gao XQ, Zhang XS (2009) Expression of a putative alfalfa helicase increases tolerance to abiotic stress in Arabidopsis by enhancing the capacities for ROS scavenging and osmotic adjustment. J Plant Physiol 166(4):385–394PubMedCrossRefGoogle Scholar
  37. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444(2):139–158PubMedCrossRefGoogle Scholar
  38. Mahbubani HM, Chong JP, Chevalier S, Thommes P, Blow JJ (1997) Cell cycle regulation of the replication licensing system: involvement of a Cdk-dependent inhibitor. J Cell Biol 136(1):125–135PubMedCrossRefGoogle Scholar
  39. Masuda HP, Ramos GB, de Almeida-Engler J, Cabral LM, Coqueiro VM, Macrini CM, Ferreira PC, Hemerly AS (2004) Genome based identification and analysis of the pre-replicative complex of Arabidopsis thaliana. FEBS Lett 574:192–202PubMedCrossRefGoogle Scholar
  40. Moyer SE, Lewis PW, Botchan MR (2006) Isolation of the Cdc45/MCM2–7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc Natl Acad Sci USA 103(27):10236–10241PubMedCrossRefGoogle Scholar
  41. Nguyen VQ, Co C, Li JJ (2001) Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature 411(6841):1068–1073PubMedCrossRefGoogle Scholar
  42. Ni DA, Sozzani R, Blanchet S, Domenichini S, Reuzeau C, Cella R, Bergounioux C, Raynaud C (2009) The Arabidopsis MCM2 gene is essential to embryo development and its over-expression alters root meristem function. New Phytol 184(2):311–322PubMedCrossRefGoogle Scholar
  43. Nishitani H, Lygerou Z (2004) DNA replication licensing. Front Biosci 9:2115–2132PubMedCrossRefGoogle Scholar
  44. Nishitani H, Lygerou Z, Nishimoto T, Nurse P (2000) The Cdt1 protein is required to license DNA for replication in fission yeast. Nature 404(6778):625–628PubMedCrossRefGoogle Scholar
  45. Nishitani H, Taraviras S, Lygerou Z, Nishimoto T (2001) The human licensing factor for DNA replication Cdt1 accumulates in G1 and is destabilized after initiation of S-phase. J Biol Chem 276(48):44905–44911PubMedCrossRefGoogle Scholar
  46. Ogura T, Wilkinson AJ (2001) AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6(7):575–597Google Scholar
  47. Pavletich NP, Pabo CO (1991) Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science 252(5007):809–817PubMedCrossRefGoogle Scholar
  48. Piatti S, Bohm T, Cocker JH, Diffley JF, Nasmyth K (1996) Activation of S-phase-promoting CDKs in late G1 defines a “point of no return” after which Cdc6 synthesis cannot promote DNA replication in yeast. Genes Dev 10(12):1516–1531PubMedCrossRefGoogle Scholar
  49. Pinstrup-Andersen P, Pandya-Lorch R, Rosegrant MW (1999) World food prospects: critical issues for the early Twenty-First century In: Food Policy Report—International Food Policy Research Institute (USA). International Food Policy Research Institute, Washington, DC, USAGoogle Scholar
  50. Ramachandra Reddy A, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161(11):1189–1202PubMedCrossRefGoogle Scholar
  51. Sabelli PA, Burgess SR, Kush AK, Young MR, Shewry PR (1996) cDNA cloning and characterisation of a maize homologue of the MCM proteins required for the initiation of DNA replication. Mol Gen Genet 252(1–2):125–136PubMedCrossRefGoogle Scholar
  52. Sabelli PA, Parker J, Barlow P (1999) cDNA and promoter sequences for MCM3 homologues from maize, and protein localization in cycling cells. J Exp Bot 50:1315–1322CrossRefGoogle Scholar
  53. Sabelli PA, Hoerster G, Lizarraga LE, Brown SW, Gordon-Kamm WJ, Larkins BA (2009) Positive regulation of minichromosome maintenance gene expression, DNA replication, and cell transformation by a plant retinoblastoma gene. Proc Natl Acad Sci USA 106(10):4042–4047PubMedCrossRefGoogle Scholar
  54. Sanan-Mishra N, Pham XH, Sopory SK, Tuteja N (2005) Pea DNA helicase 45 overexpression in tobacco confers high salinity tolerance without affecting yield. Proc Natl Acad Sci USA 102(2):509–514PubMedCrossRefGoogle Scholar
  55. Sheu YJ, Stillman B (2010) The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4. Nature 463(7277):113–117PubMedCrossRefGoogle Scholar
  56. Shultz RW, Tatineni VM, Hanley-Bowdoin L, Thompson WF (2007) Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice. Plant Physiol 144(4):1697–1714PubMedCrossRefGoogle Scholar
  57. Shultz RW, Lee TJ, Allen GC, Thompson WF, Hanley-Bowdoin L (2009) Dynamic localization of the DNA replication proteins MCM5 and MCM7 in plants. Plant Physiol 150(2):658–669PubMedCrossRefGoogle Scholar
  58. Springer PS, McCombie WR, Sundaresan V, Martienssen RA (1995) Gene trap tagging of PROLIFERA, an essential MCM2–3-5-like gene in Arabidopsis. Science 268(5212):877–880PubMedCrossRefGoogle Scholar
  59. Springer PS, Holding DR, Groover A, Yordan C, Martienssen RA (2000) The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development 127(9):1815–1822PubMedGoogle Scholar
  60. Stevens R, Mariconti L, Rossignol P, Perennes C, Cella R, Bergounioux C (2002) Two E2F sites in the Arabidopsis MCM3 promoter have different roles in cell cycle activation and meristematic expression. J Biol Chem 277(36):32978–32984PubMedCrossRefGoogle Scholar
  61. Stillman B (1994) Initiation of chromosomal DNA replication in eukaryotes. Lessons from lambda. J Biol Chem 269(10):7047–7050PubMedGoogle Scholar
  62. Takahashi N, Lammens T, Boudolf V, Maes S, Yoshizumi T, De Jaeger G, Witters E, Inze D, De Veylder L (2008) The DNA replication checkpoint aids survival of plants deficient in the novel replisome factor ETG1. EMBO J 27(13):1840–1851PubMedCrossRefGoogle Scholar
  63. Tran LS, Nakashima K, Sakuma Y, Osakabe Y, Qin F, Simpson SD, Maruyama K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2007) Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J 49(1):46–63PubMedCrossRefGoogle Scholar
  64. Tran NQ, Dang HQ, Tuteja R, Tuteja N (2010) A single subunit MCM6 from pea forms homohexamer and functions as DNA helicase. Plant Mol Biol 74(4–5):327–336PubMedCrossRefGoogle Scholar
  65. Tubon TC, Tansey WP, Herr W (2004) A nonconserved surface of the TFIIB zinc ribbon domain plays a direct role in RNA polymerase II recruitment. Mol Cell Biol 24(7):2863–2874PubMedCrossRefGoogle Scholar
  66. Tuteja N (1997) Unraveling DNA helicases from plant cells. Plant Mol Biol 33(6):947–952PubMedCrossRefGoogle Scholar
  67. Tuteja N (2000) Plant cell and viral helicases: essential enzymes for nucleic acid transactions. Crit Rev Plant Sci 19:449–478Google Scholar
  68. Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Methods Enzymol 428:419–438PubMedCrossRefGoogle Scholar
  69. Tuteja N, Tuteja R (1996) DNA helicases: the long unwinding road. Nat Genet 13(1):11–12PubMedCrossRefGoogle Scholar
  70. Tuteja N, Tuteja R (2004) Prokaryotic and eukaryotic DNA helicases. Essential molecular motor proteins for cellular machinery. Eur J Biochem 271(10):1835–1848PubMedCrossRefGoogle Scholar
  71. Weigel D, Jurgens G (2002) Stem cells that make stems. Nature 415(6873):751–754PubMedCrossRefGoogle Scholar
  72. Wildwater M, Campilho A, Perez–Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123(7):1337–1349PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Narendra Tuteja
    • 1
    Email author
  • Ngoc Quang Tran
    • 2
  • Hung Quang Dang
    • 1
  • Renu Tuteja
    • 1
  1. 1.International Centre for Genetic Engineering and Biotechnology (ICGEB)New DelhiIndia
  2. 2.Department of Biological Chemistry and Molecular PharmacologyHarvard Medical SchoolBostonUSA

Personalised recommendations