"Big it up": Endoreduplication and cell-size control in plants

Current Opinion in Plant Biology

Volumn 6, Issue 6, 2003, Pages 544-553

  Sugimoto Shirasu, Keiko ^a   Roberts, Keith ^a  

^a JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0344583779     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2003.09.009     Document Type: Review

References (63)

1. Wilson EB: The Cell in Development and Heredity. New York: Macmillan; 1925.
2. Nagl W: DNA endoreduplication and polyteny understood as evolutionary strategies. Nature 1976, 261:614-615.
3. Edgar BA, Orr-Weaver TL: Endoreplication cell cycles: more for less. Cell 2001, 105:297-306.
4. Saucedo LJ, Edgar BA: Why size matters: altering cell size. Curr Opin Genet Dev 2002, 12:565-571. Another recent review from the Edgar laboratory on cell-size control in animals.
5. Martinez-Perez E, Shaw P, Moore G: The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 2001, 411:204-207.
6. Oakenfull EA, Riou-Khamlichi C, Murray JAH: Plant D-type cyclins and the control of G1 progression. Phil Trans R Soc Lond Ser B Biol Sci 2002, 357:749-760. See annotation for [7•].
7. 1 → S transition in plants.
8. Wuarin J, Buck V, Nurse P, Millar JBA: Stable association of mitotic Cyclin B/Cdc2 to replication origins prevents endoreduplication. Cell 2002, 111:419-431. The authors show that the binding of mitotic CycB/Cdc2 kinase to DNA replication origins in yeast is ORC dependent and is required to prevent reduplication. In its absence, origins are licensed to endoreduplicate.
9. Cebolla A, Vinardell JM, Kiss E, Olah B, Roudier F, Kondorosi A, Kondorosi E: The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 1999, 18:4476-4484.
10. Walker JD, Oppenheimer DG, Concienne J, Larkin JC: SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 2000, 127:3931-3940.
11. Schnittger A, Schobinger U, Stierhof YD, Hülskamp M: Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr Biol 2002, 12:415-420.
12. Schnittger A, Schobinger U, Bouyer D, Weinl C, Stierhof YD, Hülskamp M: Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc Natl Acad Sci USA 2002, 99:6410-6415.
13. Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, Jacqmard A, Kilby NJ, Murray JAH: Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 2003, 15:79-92.
14. Jasinski S, Riou-Khamlichi C, Roche O, Perennes C, Bergounioux C, Glab N: The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. J Cell Sci 2002, 15:973-982.
15. Schnittger A, Weinl C, Bouyer D, Schobinger U, Hülskamp M: Misexpression of the cyclin-dependent kinase inhibitor /CK1/ KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell 2003, 15:303-315. The work described in this paper tested the positive correlation between cell size and DNA content by attempting to uncouple the cell autonomous effects of DNA content from those imposed by total organ size. The expression of cell cycle inhibitors in individual trichomes provided at least partial evidence for the regulation of cell growth by DNA content.
16. De Veylder L, Beeckman T, Beemster GTS, Krols L, Terras P, Landrieu I, Van der Schueren E, Maes S, Naudts M, Inze D: Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 2001, 13:1653-1667.
17. Grafi G, Burnett RJ, Helentjaris T, Larkins BA, DeCaprio JA, Sellers WR, Kaelin WG Jr: A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. Proc Natl Acad Sci USA 1996, 93:8962-8967.
18. De Veylder L, Beeckman T, Beemster GTS, Engler JD, Ormenese S, Maes S, Naudts M, Van der Schueren E, Jacqmard A, Engler G et al.: Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 2002, 21:1360-1368. Ectopic expression of E2Fa-Dpa-induced sustained cell proliferation in normally differentiated plant cells and extra replication cycles in endoreduplicating cells.
19. Castellano MM, del Pozo JC, Ramirez-Parra E, Brown S, Gutierrez C: Expression and stability of Arabidopsis CDC6 are associated with endoreplication. Plant Cell 2001, 13:2671-2686.
20. Larkins BA, Dilkes BP, Dante RA, Coelho CM, Woo YM, Liu Y: Investigating the hows and whys of DNA endoreduplication. J Exp Bot 2001, 52:183-192.
21. Kondorosi E, Roudier F, Gendreau E: Plant cell-size control: growing by ploidy? Curr Opin Plant Biol 2000, 3:488-492.
22. Hülskamp M, Misra S, Jürgens G: Genetic dissection of trichome cell development in Arabidopsis. Cell 1994, 76:555-566.
23. Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD: A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 1991, 67:483-493.
24. Payne CT, Zhang F, Lloyd AM: GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 2000, 156:1349-1362.
25. Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC: The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 1999, 11:1337-1349.
26. Schiefelbein J: Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr Opin Plant Biol 2003, 6:74-78.
27. Perazza D, Herzog M, Hülskamp M, Brown S, Dorne AM, Bonneville JM: Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics 1999, 152:461-476.
28. Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jürgens G, Hülskamp M: TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 2002, 21:5036-5046.
29. Robertson M, Swain SM, Chandler PM, Olszewski NE: Identification of a negative regulator of gibberellin action, HvSPY, in barley. Plant Cell 1998, 10:995-1007.
30. Swain SM, Tseng TS, Thornton TM, Gopalraj M, Olszewski NE: SPINDLY is a nuclear-localized repressor of gibberellin signal transduction expressed throughout the plant. Plant Physiol 2002, 129:605-615.
31. Autran D, Jonak C, Belcram K, Beemster GTS, Kronenberger J, Grandjean O, Inze D, Traas J: Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 2002, 21:6036-6049. The Arabidopsis mutant swp exhibits a dwarf phenotype that can be attributed to reduced cell number. In mutant leaves, this phenotype is partially compensated for by an increase in cell size, which is correlated with increased endoreduplication. This work suggests that a compensatory mechanism operates to maintain organ size.
32. Bonneville JM, Refy AE, Hülskamp M, Bechtold N, Herzog M: A huge gene to prevent huge trichomes: KAKTUS encodes a ubiquitin ligase related protein. Abstract 3-72, 13th International Conference on Arabidopsis Research, 28 June-2 July 2002, Seville.
33. Downes BP, Stupar RM, Gingerich DJ, Vierstra RD: The HECT ubiquitin-protein ligase (UPL) family of Arabidopsis: UPL3 has a specific role in trichome development. Abstract 73, 14th International Conference on Arabidopsis Research, 20-24 June 2003, Wisconsin.
34. Kirik V, Bouyer D, Schobinger U, Bechtold N, Herzog M, Bonneville JM, Hülskamp M: CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein. Curr Biol 2001, 11:1891-1895.
35. Hase Y, Tanaka A, Baba T, Watanabe H: FRL1 is required for petal and sepal development in Arabidopsis. Plant J 2000, 24:21-32.
36. Sugimoto-Shirasu K, Stacey NJ, Corsar J, Roberts K, McCann MC: DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr Biol 2002, 12:1782-1786. See annotation to [37•].
37. Hartung F, Angelis KJ, Meister A, Schubert I, Melzer M, Puchta H: An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants. Curr Biol 2002, 12:1787-1791. The work described in [36••,37•] shows that Arabidopsis topo VI is required for successive rounds of endocycling. In topo VI mutants, failure to increase ploidy results in smaller cell sizes, supporting the nuclear-cytoplasmic ratio theory.
38. Yin YH, Cheong H, Friedrichsen D, Zhao YD, Hu JP, Mora-Garcia S, Chory J: A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proc Natl Acad Sci USA 2002, 99:10191-10196.
39. Buhler C, Gadelle D, Forterre P, Wang JC, Bergerat A: Reconstitution of DNA topoisomerase VI of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli. Nucleic Acids Res 1998, 26:5157-5162.
40. Corbett KD, Berger JM: Emerging roles for plant topoisomerase VI. Chem Biol 2003, 10:107-111. This excellent review discusses the possible roles of plant topo VI in handling DNA during successive endocycles.
41. Feger G, Vaessin H, Su TT, Wolff E, Jan LY, Jan YN: dpa, a member of the MCM family, is required for mitotic DNA-replication but not endoreplication in Drosophila. EMBO J 1995, 14:5387-5398.
42. Satina S, Blakeslee AF: Periclinal chimeras in Datura stramonium in relation to development of leaf and flower. Am J Bot 1941, 28:862-871.
43. Melaragno JE, Mehrotra B, Coleman AW: Relationship between endopolyploidy and cell-size in epidermal tissue of Arabidopsis. Plant Cell 1993, 5:1661-1668.
44. Gendreau E, Traas J, DesnosT, Grandjean O, Caboche M, Höfte H: Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 1997, 114:295-305.
45. Beemster GT, De Vusser K, De Tavernier E, De Bock K, Inzé D: Variation in growth rate between Arabidopsis ecotypes is correlated with cell division and A-type cyclin-dependent kinase activity. Plant Physiol 2002, 129:854-864.
46. Conlon I, Raff M: Differences in the way a mammalian cell and yeast cells coordinate cell growth and cell-cycle progression. J Biol 2003, 2:7. The authors use Schwann cell cultures to provide compelling evidence that the strict cell-size controls found in yeast probably do not operate in animals. In animals, cell size at division depends instead on the relative levels of both mitogens and growth factors provided by neighbouring cells.
47. Gendreau E, Orbovic V, Höfte H, Traas J: Gibberellin and ethylene control endoreduplication levels in the Arabidopsis thaliana hypocotyl. Planta 1999, 209:513-516.
48. Montagne J, Stewart MJ, Stocker H, Hafen E, Kozma SC, Thomas G: Drosophila S6 kinase: a regulator of cell size. Science 1999, 285:2126-2129.
49. Zhang J, Schneider C, Ottmers L, Rodriguez R, Day A, Markwardt J, Schneider BL: Genomic scale mutant hunt identifies cell size homeostasis genes in S. cerevisiae. Curr Biol 2002, 12:1992-2001.
50. Jorgensen P, Nishikawa JL, Breitkreutz BJ, Tyers M: Systematic identification of pathways that couple cell growth and division in yeast. Science 2002, 297:395-400.
51. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR: Ploidy regulation of gene expression. Science 1999, 285:251-254.
52. Lee HS, Chen ZJ: Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. Proc Natl Acad Sci USA 2001, 98:6753-6758.
53. Collett CE, Harberd NP, Leyser O: Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 2000, 124:553-562.
54. Mizukami Y: A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 2001, 4:533-539.
55. Tsukaya H: Organ shape and size: a lesson from studies of leaf morphogenesis. Curr Opin Plant Biol 2003, 6:57-62.
56. Potter CJ, Xu T: Mechanisms of size control. Curr Opin Genet Dev 2001, 11:279-286.
57. Mizukami Y, Fischer RL: Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 2000, 97:942-947.
58. Hemerly A, Engler Jde A, Bergounioux C, Van Montagu M, Engler G, Inzé D, Ferreira P: Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J 1995, 14:3925-3936.
59. Wang H, Zhou Y, Gilmer S, Whitwill S, Fowke LC: Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J 2000, 24:613-623.
60. Cockcroft CE, den Boer BG, Healy JM, Murray JA: Cyclin D control of growth rate in plants. Nature 2000, 405:575-579.
61. Nath U, Crawford BC, Carpenter R, Coen E: Genetic control of surface curvature. Science 2003, 299:1404-1407. The CINCINATA (CYN) gene encodes a transcription factor that appears to act to sensitise cells, particularly those in the marginal regions of the leaf, to proliferation arrest signals. This work focuses attention on the delicate balance in normal plant organ development between the period of cell proliferation and subsequent growth and expansion.
62. Downes BP, Stupar RM, Gingerich DJ, Vierstra RD: The HECT ubiquitin protein ligase family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J 2003, 35:729-742.
63. El Refy A, Perazza D, Zekraoui L, Valay J-G, Bechtold N, Brown S, Hülskamp M, Herzog M, Bonneville J-M: The Arabidopsis KAKTUS gene encodes a HECT protein and controls the number of endoreduplication cycles. Mol Gen Genet 2003, in press.