Molecular control and function of endoreplication in development and physiology

Trends in Plant Science

Volumn 16, Issue 11, 2011, Pages 624-634

  de Veylder, Lieven ^a,b   Larkin, John C ^c,d   Schnittger, Arp ^c  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE; DNA REPLICATION; PHYSIOLOGY; PLANT CELL; PLANT PHYSIOLOGY; POLYPLOIDY; REVIEW;

CELL CYCLE; DNA REPLICATION; PLANT CELLS; PLANT PHYSIOLOGICAL PHENOMENA; POLYPLOIDY;

EUKARYOTA;

EID: 80455173888     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2011.07.001     Document Type: Review

References (112)

1. Jakoby M., Schnittger A. Cell cycle and differentiation. Curr. Opin. Plant Biol. 2004, 7:661-669.
2. Boisnard-Lorig C., et al. Dynamic analyses of the expression of the HISTONE::YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell 2001, 13:495-509.
3. Gendreau E., et al. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 1997, 114:295-305.
4. Lee H.O., et al. Endoreplication: polyploidy with purpose. Genes Dev. 2009, 23:2461-2477.
5. Sabelli P.A., Larkins B.A. The contribution of cell cycle regulation to endosperm development. Sex Plant Reprod. 2009, 22:207-219.
6. Wilkins T.A., et al. Cotton biotechnology. Crit. Rev. Plant Sci. 2000, 19:511-550.
7. Chevalier C., et al. Elucidating the functional role of endoreduplication in tomato fruit development. Ann. Bot. 2011, 107:1159-1169.
8. Kondorosi E., Kondorosi A. Endoreduplication and activation of the anaphase-promoting complex during symbiotic cell development. FEBS Lett. 2004, 567:152-157.
9. Witkus E.R. Endomitotic tapetal cell divisions in Spinacia. Am. J. Bot. 1945, 32:326-330.
10. Lima-de-Faria A., et al. Relation between ribosomal RNA genes and the DNA satellites of Phaseolus coccineus. Hereditas 1975, 79:5-20.
11. Berckmans B., De Veylder L. Transcriptional control of the cell cycle. Curr. Opin. Plant Biol. 2009, 12:599-605.
12. Boudolf V., et al. B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana. Plant Cell 2004, 16:945-955.
13. Beemster G.T., et al. The Arabidopsis leaf as a model system for investigating the role of cell cycle regulation in organ growth. J. Plant Res. 2005, 119:43-50.
14. Boudolf V., et al. CDKB1;1 forms a functional complex with CYCA2;3 to suppress endocycle onset. Plant Physiol. 2009, 150:1482-1493.
15. Imai K.K., et al. The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 2006, 18:382-396.
16. Yoshizumi T., et al. Increased level of polyploidy1, a conserved repressor of CYCLINA2 transcription, controls endoreduplication in Arabidopsis. Plant Cell 2006, 18:2452-2468.
17. Kato K., et al. Preferential up-regulation of G2/M phase-specific genes by overexpression of the hyperactive form of NtmybA2 lacking its negative regulation domain in tobacco BY-2 cells. Plant Physiol. 2009, 149:1945-1957.
18. Ito M., et al. G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factors. Plant Cell 2001, 13:1891-1905.
19. Araki S., et al. Mitotic cyclins stimulate the activity of c-Myb-like factors for transactivation of G2/M phase-specific genes in tobacco. J. Biol. Chem. 2004, 279:32979-32988.
20. Wildermuth M.C. Modulation of host nuclear ploidy: a common plant biotroph mechanism. Curr. Opin. Plant Biol. 2010, 13:449-458.
21. Cebolla A., et al. The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J. 1999, 18:4476-4484.
22. Vinardell J.M., et al. Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 2003, 15:2093-2105.
23. Lammens T., et al. Atypical E2Fs: new players in the E2F transcription factor family. Trends Cell Biol. 2009, 19:111-118.
24. Larson-Rabin Z., et al. FZR2/CCS52A1 expression is a determinant of endoreduplication and cell expansion in Arabidopsis. Plant Physiol. 2009, 149:874-884.
25. Kasili R., et al. SIAMESE cooperates with the CDH1-like protein CCS52A1 to establish endoreplication in Arabidopsis thaliana trichomes. Genetics 2010, 185:257-268.
26. Vanstraelen M., et al. APC/CCCS52A complexes control meristem maintenance in the Arabidopsis root. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:11806-11811.
27. Mathieu-Rivet E., et al. Functional analysis of the anaphase promoting complex activator CCS52A highlights the crucial role of endo-reduplication for fruit growth in tomato. Plant J. 2010, 62:727-741.
28. Vlieghe K., et al. The DP-E2F-like gene DEL1 controls the endocycle in Arabidopsis thaliana. Curr. Biol. 2005, 15:59-63.
29. Walker J.D., et al. SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 2000, 127:3931-3940.
30. Churchman M.L., et al. SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 2006, 18:3145-3157.
31. Morohashi K., Grotewold E. A systems approach reveals regulatory circuitry for Arabidopsis trichome initiation by the GL3 and GL1 selectors. PLoS Genet. 2009, 5:e1000396.
32. Jakoby M.J., et al. Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-like transcriptional regulator MYB106. Plant Physiol. 2008, 148:1583-1602.
33. Roeder A.H., et al. Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biol. 2010, 8:e1000367.
34. Peres A., et al. Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J. Biol. Chem. 2007, 282:25588-25596.
35. Dewitte W., et al. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:14537-14542.
36. Schnittger A., et al. Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:6410-6415.
37. Van Leene J., et al. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 2010, 6:397.
38. Dissmeyer N., et al. The regulatory network of cell-cycle progression is fundamentally different in plants versus yeast or metazoans. Plant Signal. Behav. 2010, 5:12.
39. Dissmeyer N., et al. Control of cell proliferation, organ growth, and DNA damage response operate independently of dephosphorylation of the Arabidopsis Cdk1 homolog CDKA;1. The Plant Cell 2009, 21:3641-3654.
40. De Schutter K., et al. Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 2007, 19:211-225.
41. Gonzalez N., et al. The cell cycle-associated protein kinase WEE1 regulates cell size in relation to endoreduplication in developing tomato fruit. Plant J. 2007, 51:642-655.
42. Sun Y., et al. Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:4180-4185.
43. Cools T., et al. The Arabidopsis thaliana checkpoint kinase WEE1 protects against premature vascular differentiation during replication stress. Plant Cell 2011, 23:1435-1448.
44. Dissmeyer N., et al. T-loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. Plant Cell 2007, 19:972-985.
45. Menges M., et al. 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. 2005, 41:546-566.
46. Leiva-Neto J.T., et al. A dominant negative mutant of cyclin-dependent kinase A reduces endoreduplication but not cell size or gene expression in maize endosperm. Plant Cell 2004, 16:1854-1869.
47. Bramsiepe J., et al. Endoreplication controls cell fate maintenance. PLoS Genet. 2010, 6:e1000996.
48. Verkest A., et al. Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiol. 2005, 139:1099-1106.
49. Wang H., et al. The emerging importance of cyclin-dependent kinase inhibitors in the regulation of the plant cell cycle and related processes. Can. J. Bot. 2006, 84:640-650.
50. Weinl C., et al. Novel functions of plant cyclin-dependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. Plant Cell 2005, 17:1704-1722.
51. Verkest A., et al. The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 2005, 17:1723-1736.
52. Schnittger A., et al. Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell 2003, 15:303-315.
53. De Veylder L., et al. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 2001, 13:1653-1668.
54. Coelho C.M., et al. Cyclin-dependent kinase inhibitors in maize endosperm and their potential role in endoreduplication. Plant Physiol. 2005, 138:2323-2336.
55. Nafati M., et al. The specific overexpression of a cyclin-dependent kinase inhibitor in tomato fruit mesocarp cells uncouples endoreduplication and cell growth. Plant J. 2011, 65:543-556.
56. Anzola J.M., et al. Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:10308-10313.
57. Roodbarkelari F., et al. Cullin 4-ring finger-ligase plays a key role in the control of endoreplication cycles in Arabidopsis trichomes. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15275-15280.
58. Gusti A., et al. The Arabidopsis thaliana F-box protein FBL17 is essential for progression through the second mitosis during pollen development. PLoS ONE 2009, 4:e4780.
59. Kim H.J., et al. Control of plant germline proliferation by SCF(FBL17) degradation of cell cycle inhibitors. Nature 2008, 455:1134-1137.
60. Liu J., et al. Targeted degradation of the cyclin-dependent kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during Arabidopsis gametogenesis. The Plant Cell 2008, 20:1538-1554.
61. Ren H., et al. Degradation of the cyclin-dependent kinase inhibitor KRP1 is regulated by two different ubiquitin E3 ligases. Plant J. 2008, 53:705-716.
62. Kirik V., et al. MIDGET unravels functions of the Arabidopsis topoisomerase VI complex in DNA endoreduplication, chromatin condensation, and transcriptional silencing. Plant Cell 2007, 19:3100-3110.
63. Breuer C., et al. BIN4, a novel component of the plant DNA topoisomerase VI complex, is required for endoreduplication in Arabidopsis. Plant Cell 2007, 19:3655-3668.
64. Sugimoto-Shirasu K., et al. RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:18736-18741.
65. Sugimoto-Shirasu K., et al. DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr. Biol. 2002, 12:1782-1786.
66. Oostveldt P., Parijs R. Effect of light on nucleic-acid synthesis and polyploidy level in elongating epicotyl cells of Pisum sativum. Planta 1975, 124:287-295.
67. Kudo N., Mii M. Endoreduplication cycles during hypocotyl growth of cabbage (Brassica oleracea L.) under light and dark conditions. Plant Biotechnol. 2004, 21:295-298.
68. Gendreau E., et al. Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J. 1998, 13:221-230.
69. Tsumoto Y., et al. Light-dependent polyploidy control by a CUE protein variant in Arabidopsis. Plant Mol. Biol. 2006, 61:817-828.
70. Cookson S.J., Granier C. A dynamic analysis of the shade-induced plasticity in Arabidopsis thaliana rosette leaf development reveals new components of the shade-adaptative response. Ann. Bot. 2006, 97:443-452.
71. Barow M., Meister A. Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant Cell Environ. 2003, 26:571-584.
72. Radziejwoski A., et al. Atypical E2F activity coordinates PHR1 photolyase gene transcription with endoreduplication onset. EMBO J. 2011, 30:355-363.
73. Ramirez-Parra E., Gutierrez C. E2F regulates FASCIATA1, a chromatin assembly gene whose loss switches on the endocycle and activates gene expression by changing the epigenetic status. Plant Physiol. 2007, 144:105-120.
74. Adachi S., et al. Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:10004-10009.
75. Yoshiyama K., et al. Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:12843-12848.
76. Schubert V., et al. Sister chromatids are often incompletely aligned in meristematic and endopolyploid interphase nuclei of Arabidopsis thaliana. Genetics 2006, 172:467-475.
77. Yamasaki S., et al. Continuous UV-B irradiation induces endoreduplication and peroxidase activity in epidermal cells surrounding trichomes on cucumber cotyledons. J. Radiat. Res. 2010, 51:187-196.
78. Gendreau E., et al. Gibberellin and ethylene control endoreduplication levels in the Arabidopsis thaliana hypocotyl. Planta 1999, 209:513-516.
79. Perazza D., et al. Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics 1999, 152:461-476.
80. Swain S.M., et al. SPINDLY is a nuclear-localized repressor of gibberellin signal transduction expressed throughout the plant. Plant Physiol. 2002, 129:605-615.
81. Ishida T., et al. Auxin modulates the transition from the mitotic cycle to the endocycle in Arabidopsis. Development 2010, 137:63-71.
82. Chandran D., et al. Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:460-465.
83. Engler J.A., et al. Unravelling the plant cell cycle in nematode induced feeding sites. Genomics and Molecular Genetics of Plant-Nematode Interactions 2011, 349-368. Springer. J. Jones (Ed.).
84. Lingua G., et al. The nucleus of differentiated root plant cells: modifications induced by arbuscular mycorrhizal fungi. Eur. J. Histochem. 2001, 45:9-20.
85. Bainard L.D., et al. Mycorrhizal symbiosis stimulates endoreduplication in angiosperms. Plant Cell Environ. 2011, 34:1577-1585.
86. Sugimoto-Shirasu K., Roberts K. "Big it up" endoreduplication and cell-size control in plants. Curr. Opin. Plant Biol. 2003, 6:544-553.
87. Kondorosi E., et al. Plant cell-size control: growing by ploidy?. Curr. Opin. Plant Biol. 2000, 3:488-492.
88. Melaragno J.E., et al. Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 1993, 5:1661-1668.
89. Hulskamp M., et al. Pattern formation and cell differentiation: trichomes in Arabidopsis as a genetic model system. Int. Rev. Cytol. 1999, 186:147-178.
90. Marks M.D. Molecular genetic analysis of trichome development in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48:137-163.
91. Schnittger A., et al. Tissue layer and organ specificity of trichome formation are regulated by GLABRA1 and TRIPTYCHON in Arabidopsis. Development 1998, 125:2283-2289.
92. Kasili R., et al. BRANCHLESS TRICHOMES links cell shape and cell cycle control in Arabidopsis trichomes. Development 2011, 138:2379-2388.
93. Breuer C., et al. The trihelix transcription factor GTL1 regulates ploidy-dependent cell growth in the Arabidopsis trichome. Plant Cell 2009, 21:2307-2322.
94. Bourdon M., et al. In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH). Plant J. 2011, 66:1089-1099.
95. Gutierrez C. The Arabidopsis cell division cycle. The Arabidopsis Book 2008, 1-19. The American Society of Plant Biologists. R. Last (Ed.).
96. De Veylder L., et al. The ins and outs of the plant cell cycle. Nat. Rev. Mol. Cell Biol. 2007, 8:655-665.
97. Pines J. Cyclins and cyclin-dependent kinases: a biochemical view. Biochem. J. 1995, 308:697-711.
98. Pines J. Four-dimensional control of the cell cycle. Nat. Cell Biol. 1999, 1:E73-E79.
99. Kaldis P. The cdk-activating kinase (CAK): from yeast to mammals. Cell Mol. Life Sci. 1999, 55:284-296.
100. O'Farrell P.H. Triggering the all-or-nothing switch into mitosis. Trends Cell Biol. 2001, 11:512-519.
101. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7:644-656.
102. Sherr C.J., Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999, 13:1501-1512.
103. Vandepoele K., et al. Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 2002, 14:903-916.
104. Wang G., et al. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol. 2004, 135:1084-1099.
105. Ferreira P.C., et al. The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 1991, 3:531-540.
106. Hirayama T., et al. Identification of two cell-cycle-controlling cdc2 gene homologs in Arabidopsis thaliana. Gene 1991, 105:159-165.
107. Porceddu A., et al. A plant-specific cyclin-dependent kinase is involved in the control of G2/M progression in plants. J. Biol. Chem. 2001, 276:36354-36360.
108. Hattori N., et al. Periodic expression of the cyclin-dependent kinase inhibitor p57(Kip2) in trophoblast giant cells defines a G2-like gap phase of the endocycle. Mol. Biol. Cell 2000, 11:1037-1045.
109. Ullah Z., et al. Differentiation of trophoblast stem cells into giant cells is triggered by p57/Kip2 inhibition of CDK1 activity. Genes Dev. 2008, 22:3024-3036.
110. Kamura T., et al. Degradation of p57Kip2 mediated by SCFSkp2-dependent ubiquitylation. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10231-10236.
111. Ganier O., Mechali M. New cell or new cycle?. Genes Dev. 2008, 22:2908-2913.
112. Garcia-Higuera I., et al. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat. Cell Biol. 2008, 10:802-811.