Retinoblastoma-related protein controls the transition to autotrophic plant development

Development

Volumn 138, Issue 14, 2011, Pages 2977-2986

  Gutzat, Ruben ^a   Borghi, Lorenzo ^a,c   Fütterer, Johannes ^a   Bischof, Sylvain ^a   Laizet, Yechan ^a,d   Hennig, Lars ^a,e   Feil, Regina ^b   Lunn, John ^b   Gruissem, Wilhelm ^a  

^a ETH ZURICH   (Switzerland)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d Univ Bordeaux   (France)

^e SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

ABI3; Arabidopsis; Cell cycle; Cell fate; Differentiation; Embryo development; Polycomb; PRC2; RBR; Retinoblastoma; Seedling establishment; Sucrose; Tumor

Indexed keywords

ARABIDOPSIS PROTEIN; HISTONE H3; RETINOBLASTOMA PROTEIN; SUCROSE;

ARABIDOPSIS; ARTICLE; AUTOTROPHY; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL DIVISION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENETIC TRANSCRIPTION; GERMINATION; HETEROTROPHY; HISTONE METHYLATION; METABOLIC REGULATION; NONHUMAN; PLANT DEVELOPMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; SEEDLING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; AUTOTROPHIC PROCESSES; CELL CYCLE; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GLUCOSE; HISTONES; IMMUNOBLOTTING; MASS SPECTROMETRY; MICROARRAY ANALYSIS; MICROSCOPY, ELECTRON, SCANNING; MODELS, BIOLOGICAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDLING;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79959446883     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.060830     Document Type: Article

References (87)

1. Agne, B., Andres, C., Montandon, C., Christ, B., Ertan, A., Jung, F., Infanger, S., Bischof, S., Baginsky, S. and Kessler, F. (2010). The acidic A-domain of Arabidopsis TOC159 occurs as a hyperphosphorylated protein. Plant Physiol. 153, 1016-1030.
2. Aichinger, E., Villar, C. B., Farrona, S., Reyes, J. C., Hennig, L. and Kohler, C. (2009). CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet. 5, e1000605.
3. Annicotte, J. S., Blanchet, E., Chavey, C., Iankova, I., Costes, S., Assou, S., Teyssier, J., Dalle, S., Sardet, C. and Fajas, L. (2009). The CDK4-pRB-E2F1 pathway controls insulin secretion. Nat. Cell Biol. 11, 1017-1023.
4. Bentsink, L. and Koornneef, M. (2008). Seed dormancy and germination. In The Arabidopsis Book. Rockville: The American Society of Plant Biologists. 6:e0119. doi:10.1199/tab.011.
5. Bieri, S., Potrykus, I. and Fütterer, J. (2002). Geminivirus sequences as bidirectional transcription termination/polyadenylation signals for economic construction of stably expressed transgenes. Mol. Breed. 10, 107-117.
6. Borghi, L., Gutzat, R., Futterer, J., Laizet, Y., Hennig, L. and Gruissem, W. (2010). Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22, 1792-1811.
7. Bouveret, R., Schonrock, N., Gruissem, W. and Hennig, L. (2006). Regulation of flowering time by Arabidopsis MSI1. Development 133, 1693-1702.
8. Bowler, C., Benvenuto, G., Laflamme, P., Molino, D., Probst, A. V., Tariq, M. and Paszkowski, J. (2004). Chromatin techniques for plant cells. Plant J. 39, 776-789.
9. Brand, U., Grunewald, M., Hobe, M. and Simon, R. (2002). Regulation of CLV3 expression by two homeobox genes in Arabidopsis. Plant Physiol. 129, 565-575.
10. Braybrook, S. A. and Harada, J. J. (2008). LECs go crazy in embryo development. Trends Plant Sci. 13, 624-630.
11. Breitling, R., Armengaud, P., Amtmann, A. and Herzyk, P. (2004). Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 573, 83-92.
12. Burkhart, D. L. and Sage, J. (2008). Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat. Rev. Cancer 8, 671-682.
13. Calo, E., Quintero-Estades, J. A., Danielian, P. S., Nedelcu, S., Berman, S. D. and Lees, J. A. (2010). Rb regulates fate choice and lineage commitment in vivo. Nature 466, 1110-1114.
14. Carranco, R., Chandrasekharan, M. B., Townsend, J. C. and Hall, T. C. (2004). Interaction of PvALF and VP1 B3 domains with the beta-phaseolin promoter. Plant Mol. Biol. 55, 221-237.
15. Chanvivattana, Y., Bishopp, A., Schubert, D., Stock, C., Moon, Y. H., Sung, Z. R. and Goodrich, J. (2004). Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131, 5263-5276.
16. Chen, Z., Hafidh, S., Poh, S. H., Twell, D. and Berger, F. (2009). Proliferation and cell fate establishment during Arabidopsis male gametogenesis depends on the Retinoblastoma protein. Proc. Natl. Acad. Sci. USA 106, 7257-7262.
17. Dasgupta, B. and Milbrandt, J. (2009). AMP-activated protein kinase phosphorylates retinoblastoma protein to control mammalian brain development. Dev. Cell 16, 256-270.
18. De Veylder, L., Beeckman, T., Beemster, G. T., de Almeida Engler, J., Ormenese, S., Maes, S., Naudts, M., Van Der Schueren, E., Jacqmard, A., Engler, G. et al. (2002). Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J. 21, 1360-1368.
19. Deeken, R., Engelmann, J. C., Efetova, M., Czirjak, T., Muller, T., Kaiser, W. M., Tietz, O., Krischke, M., Mueller, M. J., Palme, K. et al. (2006). An integrated view of gene expression and solute profiles of Arabidopsis tumors: a genome-wide approach. Plant Cell 18, 3617-3634.
20. Desvoyes, B., Ramirez-Parra, E., Xie, Q., Chua, N. H. and Gutierrez, C. (2006). Cell type-specific role of the retinoblastoma/E2F pathway during Arabidopsis leaf development. Plant Physiol. 140, 67-80.
21. Durfee, T., Feiler, H. S. and Gruissem, W. (2000). Retinoblastoma-related proteins in plants: homologues or orthologues of their metazoan counterparts? Plant Mol. Biol. 43, 635-642.
22. Ebel, C., Mariconti, L. and Gruissem, W. (2004). Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429, 776-780.
23. Fait, A., Angelovici, R., Less, H., Ohad, I., Urbanczyk-Wochniak, E., Fernie, A. R. and Galili, G. (2006). Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol. 142, 839-854.
24. Gehring, C. (2010). Adenyl cyclases and cAMP in plant signaling-past and present. Cell Commun. Signal. 8, 15.
25. Gendreau, E., Traas, J., Desnos, T., Grandjean, O., Caboche, M. and Hofte, H. (1997). Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114, 295-305.
26. Goodrich, D. W., Wang, N. P., Qian, Y. W., Lee, E. Y. and Lee, W. H. (1991). The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle. Cell 67, 293-302.
27. Graham, I. A. (2008). Seed storage oil mobilization. Annu. Rev. Plant Biol. 59, 115-142.
28. Hendriks, J. H., Kolbe, A., Gibon, Y., Stitt, M. and Geigenberger, P. (2003). ADP-glucose pyrophosphorylase is activated by posttranslational redoxmodification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol. 133, 838-849.
29. Hennig, L. and Derkacheva, M. (2009). Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet. 25, 414-423.
30. Hennig, L., Gruissem, W., Grossniklaus, U. and Kohler, C. (2004). Transcriptional programs of early reproductive stages in Arabidopsis. Plant Physiol. 135, 1765-1775.
31. Henriques, R., Magyar, Z., Monardes, A., Khan, S., Zalejski, C., Orellana, J., Szabados, L., de la Torre, C., Koncz, C. and Bogre, L. (2010). Arabidopsis S6 kinase mutants display chromosome instability and altered RBR1-E2F pathway activity. EMBO J. 29, 2979-2993.
32. Hirano, H., Harashima, H., Shinmyo, A. and Sekine, M. (2008). Arabidopsis RETINOBLASTOMA-RELATED PROTEIN 1 is involved in G1 phase cell cycle arrest caused by sucrose starvation. Plant Mol. Biol. 66, 259-275.
33. Honma, T. and Goto, K. (2001). Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409, 525-529.
34. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., Widmayer, P., Gruissem, W. and Zimmermann, P. (2008). Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics 2008, 420747.
35. Ingouff, M., Jullien, P. E. and Berger, F. (2006). The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. Plant Cell 18, 3491-3501.
36. Inze, D. and De Veylder, L. (2006). Cell cycle regulation in plant development. Annu. Rev. Genet. 40, 77-105.
37. Johnston, A. J., Matveeva, E., Kirioukhova, O., Grossniklaus, U. and Gruissem, W. (2008). A dynamic reciprocal RBR-PRC2 regulatory circuit controls Arabidopsis gametophyte development. Curr. Biol. 18, 1680-1686.
38. Johnston, A. J., Kirioukhova, O., Barrell, P. J., Rutten, T., Moore, J. M., Baskar, R., Grossniklaus, U. and Gruissem, W. (2010). Dosage-sensitive function of retinoblastoma related and convergent epigenetic control are required during the Arabidopsis life cycle. PLoS Genet. 6, e1000988.
39. Jordan, C. V., Shen, W., Hanley-Bowdoin, L. K. and Robertson, D. N. (2007). Geminivirus-induced gene silencing of the tobacco retinoblastoma-related gene results in cell death and altered development. Plant Mol. Biol. 65, 163-175.
40. Jullien, P. E., Mosquna, A., Ingouff, M., Sakata, T., Ohad, N. and Berger, F. (2008). Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol. 6, e194.
41. Karimi, M., Inze, D. and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195.
42. Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. and Poethig, R. S. (2001). KANADI regulates organ polarity in Arabidopsis. Nature 411, 706-709.
43. Knudsen, E. S. and Knudsen, K. E. (2006). Retinoblastoma tumor suppressor: where cancer meets the cell cycle. Exp. Biol. Med. (Maywood) 231, 1271-1281.
44. Korenjak, M. and Brehm, A. (2005). E2F-Rb complexes regulating transcription of genes important for differentiation and development. Curr. Opin. Genet. Dev. 15, 520-527.
45. Kwiatkowska, D. (2004). Surface growth at the reproductive shoot apex of Arabidopsis thaliana pin-formed 1 and wild type. J. Exp. Bot. 55, 1021-1032.
46. Lageix, S., Catrice, O., Deragon, J. M., Gronenborn, B., Pelissier, T. and Ramirez, B. C. (2007). The nanovirus-encoded Clink protein affects plant cell cycle regulation through interaction with the retinoblastoma-related protein. J. Virol. 81, 4177-4185.
47. Lee, W. H., Bookstein, R., Hong, F., Young, L. J., Shew, J. Y. and Lee, E. Y. (1987). Human retinoblastoma susceptibility gene: cloning, identification, and sequence. Science 235, 1394-1399.
48. Lopez-Molina, L., Mongrand, S. and Chua, N. H. (2001). A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl. Acad. Sci. USA 98, 4782-4787.
49. Lopez-Molina, L., Mongrand, S., McLachlin, D. T., Chait, B. T. and Chua, N. H. (2002). ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J. 32, 317-328.
50. Lu, P., Vogel, C., Wang, R., Yao, X. and Marcotte, E. M. (2007). Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 25, 117-124.
51. Lynn, K., Fernandez, A., Aida, M., Sedbrook, J., Tasaka, M., Masson, P. and Barton, M. K. (1999). The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126, 469-481.
52. Menges, M., Hennig, L., Gruissem, W. and Murray, J. A. (2003). Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol. Biol. 53, 423-442.
53. Mizukami, Y. and Ma, H. (1992). Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71, 119-131.
54. Monke, G., Altschmied, L., Tewes, A., Reidt, W., Mock, H. P., Baumlein, H. and Conrad, U. (2004). Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta 219, 158-166.
55. Moulager, M., Corellou, F., Verge, V., Escande, M. L. and Bouget, F. Y. (2010). Integration of light signals by the retinoblastoma pathway in the control of S phase entry in the picophytoplanktonic cell Ostreococcus. PLoS Genet. 6, e1000957.
56. Nakashima, K., Fujita, Y., Katsura, K., Maruyama, K., Narusaka, Y., Seki, M., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2006). Transcriptional regulation of ABI3-and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol. Biol. 60, 51-68.
57. Park, J. A., Ahn, J. W., Kim, Y. K., Kim, S. J., Kim, J. K., Kim, W. T. and Pai, H. S. (2005). Retinoblastoma protein regulates cell proliferation, differentiation, and endoreduplication in plants. Plant J. 42, 153-163.
58. Penfield, S., Rylott, E. L., Gilday, A. D., Graham, S., Larson, T. R. and Graham, I. A. (2004). Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1. Plant Cell 16, 2705-2718.
59. Penfield, S., Pinfield-Wells, H. M. and Graham, I. A. (2006). Storage reserve mobilisation and seedling establishment in Arabidopsis. In The Arabidopsis Book. Rockville: The American Society of Plant Biologists. 4:e0100. doi:10.1199/ tab.0100.
60. R Development Core Team (2009). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
61. Reidt, W., Wohlfarth, T., Ellerstrom, M., Czihal, A., Tewes, A., Ezcurra, I., Rask, L. and Baumlein, H. (2000). Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J. 21, 401-408.
62. Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J. A. (1999). Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541-1544.
63. Riou-Khamlichi, C., Menges, M., Healy, J. M. and Murray, J. A. (2000). Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol. Cell. Biol. 20, 4513-4521.
64. Rolland, F., Baena-Gonzalez, E. and Sheen, J. (2006). Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675-709.
65. Romanel, E. A., Schrago, C. G., Counago, R. M., Russo, C. A. and Alves-Ferreira, M. (2009). Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification. PLoS ONE 4, e5791.
66. Rook, F. and Bevan, M. W. (2003). Genetic approaches to understanding sugarresponse pathways. J. Exp. Bot. 54, 495-501.
67. Sambrook, J. and Russell, D. (2006). The Condensed Protocols From Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
68. Santos-Mendoza, M., Dubreucq, B., Baud, S., Parcy, F., Caboche, M. and Lepiniec, L. (2008). Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J. 54, 608-620.
69. Schauer, S. E., Jacobsen, S. E., Meinke, D. W. and Ray, A. (2002). DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci. 7, 487-491.
70. Schmid, M., Davison, T. S., Henz, S. R., Pape, U. J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D. and Lohmann, J. U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
71. Schmidt, T. G. and Skerra, A. (2007). The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins. Nat. Protoc. 2, 1528-1535.
72. Schuettengruber, B. and Cavalli, G. (2009). Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136, 3531-3542.
73. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
74. Simon, J. A. and Kingston, R. E. (2009). Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10, 697-708.
75. Soni, R., Carmichael, J. P., Shah, Z. H. and Murray, J. A. (1995). A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7, 85-103.
76. Stuitje, A. R., Verbree, E. C., van der Linden, K. H., Mietkiewska, E. M., Nap, J. P. and Kneppers, T. J. (2003). Seed-expressed fluorescent proteins as versatile tools for easy (co)transformation and high-throughput functional genomics in Arabidopsis. Plant Biotechnol. J. 1, 301-309.
77. Suzuki, M., Kao, C. Y. and McCarty, D. R. (1997). The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell 9, 799-807.
78. Tsukagoshi, H., Morikami, A. and Nakamura, K. (2007). Two B3 domain transcriptional repressors prevent sugar-inducible expression of seed maturation genes in Arabidopsis seedlings. Proc. Natl. Acad. Sci. USA 104, 2543-2547.
79. van den Heuvel, S. and Dyson, N. J. (2008). Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9, 713-724.
80. Vandepoele, K., Vlieghe, K., Florquin, K., Hennig, L., Beemster, G. T., Gruissem, W., Van de Peer, Y., Inze, D. and De Veylder, L. (2005). Genomewide identification of potential plant E2F target genes. Plant Physiol. 139, 316-328.
81. von Schaewen, A., Stitt, M., Schmidt, R., Sonnewald, U. and Willmitzer, L. (1990). Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J. 9, 3033-3044.
82. Weise, A., Barker, L., Kuhn, C., Lalonde, S., Buschmann, H., Frommer, W. B. and Ward, J. M. (2000). A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell 12, 1345-1355.
83. Wildwater, M., Campilho, A., Perez-Perez, J. M., Heidstra, R., Blilou, I., Korthout, H., Chatterjee, J., Mariconti, L., Gruissem, W. and Scheres, B. (2005). The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337-1349.
84. Wyrzykowska, J., Schorderet, M., Pien, S., Gruissem, W. and Fleming, A. J. (2006). Induction of differentiation in the shoot apical meristem by transient overexpression of a retinoblastoma-related protein. Plant Physiol. 141, 1338-1348.
85. Zhang, X., Henriques, R., Lin, S. S., Niu, Q. W. and Chua, N. H. (2006). Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641-646.
86. Zhang, X., Clarenz, O., Cokus, S., Bernatavichute, Y. V., Pellegrini, M., Goodrich, J. and Jacobsen, S. E. (2007). Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 5, e129.
87. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.