MIDGET connects COP1-dependent development with endoreduplication in Arabidopsis thaliana

Plant Journal

Volumn 75, Issue 1, 2013, Pages 67-79

  Schrader, Andrea ^a   Welter, Bastian ^a   Hulskamp, Martin ^a   Hoecker, Ute ^a   Uhrig, Joachim F ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Arabidopsis thaliana; endoreduplication; hypocotyl elongation; photomorphogenesis; protein interaction; topoisomerase VI

Indexed keywords

ARABIDOPSIS THALIANA; ENDOREDUPLICATION; HYPOCOTYL ELONGATION; PHOTOMORPHOGENESIS; PROTEIN INTERACTION; TOPOISOMERASES;

BIOLOGY; PLANTS (BOTANY);

PROTEINS;

ANTHOCYANIN; ARABIDOPSIS PROTEIN; COP1 PROTEIN, ARABIDOPSIS; DNA TOPOISOMERASE IV; HYBRID PROTEIN; MULTIENZYME COMPLEX; UBIQUITIN PROTEIN LIGASE;

ARABIDOPSIS; ARTICLE; DARKNESS; ENDOREDUPLICATION; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; ONION; PHENOTYPE; PLANT GROWTH; PLANT LEAF; PLOIDY; SEEDLING; TOBACCO; TRANSGENIC PLANT; TWO HYBRID SYSTEM; ULTRASTRUCTURE;

ANTHOCYANINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DARKNESS; DNA TOPOISOMERASE IV; ENDOREDUPLICATION; GENE EXPRESSION REGULATION, PLANT; GERMINATION; HYPOCOTYL; MULTIENZYME COMPLEXES; MUTATION; ONIONS; PHENOTYPE; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PLOIDIES; RECOMBINANT FUSION PROTEINS; SEEDLING; TOBACCO; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN-PROTEIN LIGASES;

ARABIDOPSIS THALIANA;

EID: 84879209209     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12199     Document Type: Article

References (71)

1. Ang, L.H., and, Deng, X.W., (1994) Regulatory hierarchy of photomorphogenic loci: allele-specific and light-dependent interaction between the HY5 and COP1 loci. Plant Cell, 6, 613-628.
2. Ang, L.H., Chattopadhyay, S., Wei, N., Oyama, T., Okada, K., Batschauer, A., and, Deng, X.W., (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol. Cell, 1, 213-222.
3. von Arnim, A.G., and, Deng, X.W., (1994) Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell, 79, 1035-1045.
4. Bates, A.D., and, Maxwell, A., (2005) DNA Topology, 2nd edn. Oxford: Oxford University Press.
5. Breuer, C., Stacey, N.J., West, C.E., Zhao, Y., Chory, J., Tsukaya, H., Azumi, Y., Maxwell, A., Roberts, K., and, Sugimoto-Shirasu, K., (2007) BIN4, a novel component of the plant DNA topoisomerase VI complex, is required for endoreduplication in Arabidopsis. Plant Cell, 19, 3655-3668.
6. Chen, M., (2008) Phytochrome nuclear body: an emerging model to study interphase nuclear dynamics and signaling. Curr. Opin. Plant Biol., 11, 503-508.
7. Chen, H., Huang, X., Gusmaroli, G., et al. (2010) Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell, 22, 108-123.
8. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J., 16, 735-743.
9. Corbett, K.D., and, Berger, J.M., (2003) Emerging roles for plant topoisomerase VI. Chem. Biol., 10, 107-111.
10. Deng, X.W., and, Quail, P.H., (1992) Genetic and Phenotypic Characterization of Cop-1 Mutants of Arabidopsis Thaliana. Plant J., 2, 83-95.
11. Dieterle, M., Buche, C., Schafer, E., and, Kretsch, T., (2003) Characterization of a novel non-constitutive photomorphogenic cop1 allele. Plant Physiol., 133, 1557-1564.
12. Dieterle, M., Bauer, D., Buche, C., Krenz, M., Schafer, E., and, Kretsch, T., (2005) A new type of mutation in phytochrome a causes enhanced light sensitivity and alters the degradation and subcellular partitioning of the photoreceptor. Plant J., 41, 146-161.
13. Dohmann, E.M., Levesque, M.P., De Veylder, L., Reichardt, I., Jurgens, G., Schmid, M., and, Schwechheimer, C., (2008) The Arabidopsis COP9 signalosome is essential for G2 phase progression and genomic stability. Development, 135, 2013-2022.
14. Dyachok, J., Zhu, L., Liao, F., He, J., Huq, E., and, Blancaflor, E.B., (2011) SCAR mediates light-induced root elongation in Arabidopsis through photoreceptors and proteasomes. Plant Cell, 23, 3610-3626.
15. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and, Pikaard, C.S., (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J., 45, 616-629.
16. van der Fits, L., Deakin, E.A., Hoge, J.H., and, Memelink, J., (2000) The ternary transformation system: constitutive virG on a compatible plasmid dramatically increases Agrobacterium-mediated plant transformation. Plant Mol. Biol., 43, 495-502.
17. Forterre, P., and, Gadelle, D., (2009) Phylogenomics of DNA topoisomerases: their origin and putative roles in the emergence of modern organisms. Nucleic Acids Res., 37, 679-692.
18. Franklin, K.A., and, Quail, P.H., (2010) Phytochrome functions in Arabidopsis development. J. Exp. Bot., 61, 11-24.
19. 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.
20. Gendreau, E., Hofte, H., Grandjean, O., Brown, S., and, Traas, J., (1998) Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J., 13, 221-230.
21. Gietz, R.D., and, Schiestl, R.H., (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc., 2, 31-34.
22. Gigolashvili, T., Berger, B., Mock, H.P., Muller, C., Weisshaar, B., and, Flugge, U.I., (2007) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J., 50, 886-901.
23. Harari-Steinberg, O., Ohad, I., and, Chamovitz, D.A., (2001) Dissection of the light signal transduction pathways regulating the two early light-induced protein genes in Arabidopsis. Plant Physiol., 127, 986-997.
24. Hartung, F., and, Puchta, H., (2001) Molecular characterization of homologues of both subunits A (SPO11) and B of the archaebacterial topoisomerase 6 in plants. Gene, 271, 81-86.
25. Hartung, F., Angelis, K.J., Meister, A., Schubert, I., Melzer, M., and, Puchta, H., (2002) An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants. Curr. Biol., 12, 1787-1791.
26. Hoecker, U., and, Quail, P.H., (2001) The phytochrome A-specific signaling intermediate SPA1 interacts directly with COP1, a constitutive repressor of light signaling in Arabidopsis. J. Biol. Chem., 276, 38173-38178.
27. Holm, M., Hardtke, C.S., Gaudet, R., and, Deng, X.W., (2001) Identification of a structural motif that confers specific interaction with the WD40 repeat domain of Arabidopsis COP1. EMBO J., 20, 118-127.
28. 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.
29. Indorf, M., Cordero, J., Neuhaus, G., and, Rodriguez-Franco, M., (2007) Salt tolerance (STO), a stress-related protein, has a major role in light signalling. Plant J., 51, 563-574.
30. Jach, G., Pesch, M., Richter, K., Frings, S., and, Uhrig, J.F., (2006) An improved mRFP1 adds red to bimolecular fluorescence complementation. Nat. Methods, 3, 597-600.
31. Jang, S., Marchal, V., Panigrahi, K.C., Wenkel, S., Soppe, W., Deng, X.W., Valverde, F., and, Coupland, G., (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J., 27, 1277-1288.
32. Kirik, V., Schrader, A., Uhrig, J.F., and, Hulskamp, M., (2007) MIDGET unravels functions of the Arabidopsis topoisomerase VI complex in DNA endoreduplication, chromatin condensation, and transcriptional silencing. Plant Cell, 19, 3100-3110.
33. Kondorosi, E., Roudier, F., and, Gendreau, E., (2000) Plant cell-size control: growing by ploidy? Curr. Opin. Plant Biol., 3, 488-492.
34. Lange, H., Shropshire, J., and, Mohr, H., (1971) An analysis of phytochrome-mediated anthocyanin synthesis. Plant Physiol., 47, 649-655.
35. Laubinger, S., Fittinghoff, K., and, Hoecker, U., (2004) The SPA quartet: a family of WD-repeat proteins with a central role in suppression of photomorphogenesis in Arabidopsis. Plant Cell, 16, 2293-2306.
36. Liu, L.J., Zhang, Y.C., Li, Q.H., Sang, Y., Mao, J., Lian, H.L., Wang, L., and, Yang, H.Q., (2008) COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell, 20, 292-306.
37. Liu, B., Zuo, Z., Liu, H., Liu, X., and, Lin, C., (2011) Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev., 25, 1029-1034.
38. Martel, F., Grundemann, D., and, Schomig, E., (2002) A simple method for elimination of false positive results in RT-PCR. J. Biochem. Mol. Biol., 35, 248-250.
39. McNellis, T.W., von Arnim, A.G., Araki, T., Komeda, Y., Misera, S., and, Deng, X.W., (1994) Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell, 6, 487-500.
40. McNellis, T.W., Torii, K.U., and, Deng, X.W., (1996) Expression of an N-Terminal Fragment of COP1 Confers a Dominant-Negative Effect on Light-Regulated Seedling Development in Arabidopsis. Plant Cell, 8, 1491-1503.
41. Melaragno, J.E., Mehrotra, B., and, Coleman, A.W., (1993) Relationship between Endopolyploidy and Cell Size in Epidermal Tissue of Arabidopsis. Plant Cell, 5, 1661-1668.
42. Neff, M.M., and, Chory, J., (1998) Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol., 118, 27-35.
43. Nemeth, K., Salchert, K., Putnoky, P., et al. (1998) Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev., 12, 3059-3073.
44. Ruxton, G.D., (2006) The unequal variance t-test is an underused alternative to Student's t-test and the Mann-Whitney U test. Behav. Ecol., 17, 688-690.
45. Saedler, R., Mathur, N., Srinivas, B.P., Kernebeck, B., Hulskamp, M., and, Mathur, J., (2004) Actin control over microtubules suggested by DISTORTED2 encoding the Arabidopsis ARPC2 subunit homolog. Plant Cell Physiol., 45, 813-822.
46. Saijo, Y., Sullivan, J.A., Wang, H., Yang, J., Shen, Y., Rubio, V., Ma, L., Hoecker, U., and, Deng, X.W., (2003) The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev., 17, 2642-2647.
47. Santoni, V., Delarue, M., Caboche, M., and, Bellini, C., (1997) A comparison of two-dimensional electrophoresis data with phenotypical traits in Arabidopsis leads to the identification of a mutant (cri1) that accumulates cytokinins. Planta, 202, 62-69.
48. Schmidt, R., and, Mohr, H., (1981) Time-dependent changes in the responsiveness to light of phytochrome-mediated anthocyanin synthesis. Plant, Cell Environ., 4, 433-437.
49. Schwechheimer, C., and, Deng, X.W., (2001) COP9 signalosome revisited: a novel mediator of protein degradation. Trends Cell Biol., 11, 420-426.
50. Schwechheimer, C., and, Isono, E., (2010) The COP9 signalosome and its role in plant development. Eur. J. Cell Biol., 89, 157-162.
51. Seo, H.S., Yang, J.Y., Ishikawa, M., Bolle, C., Ballesteros, M.L., and, Chua, N.H., (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature, 423, 995-999.
52. Seo, H.S., Watanabe, E., Tokutomi, S., Nagatani, A., and, Chua, N.H., (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev., 18, 617-622.
53. Shaw, P.J., and, Brown, J.W., (2004) Plant nuclear bodies. Curr. Opin. Plant Biol., 7, 614-620.
54. Soellick, T.R., and, Uhrig, J.F., (2001) Development of an optimized interaction-mating protocol for large-scale yeast two-hybrid analyses. Genome Biol., 2, RESEARCH0052.
55. Stacey, M.G., and, von Arnim, A.G., (1999) A novel motif mediates the targeting of the Arabidopsis COP1 protein to subnuclear foci. J. Biol. Chem., 274, 27231-27236.
56. Stacey, M.G., Hicks, S.N., and, von Arnim, A.G., (1999) Discrete domains mediate the light-responsive nuclear and cytoplasmic localization of Arabidopsis COP1. Plant Cell, 11, 349-364.
57. Sugimoto-Shirasu, K., Stacey, N.J., Corsar, J., Roberts, K., and, McCann, M.C., (2002) DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr. Biol., 12, 1782-1786.
58. Sugimoto-Shirasu, K., Roberts, G.R., Stacey, N.J., McCann, M.C., Maxwell, A., and, Roberts, K., (2005) RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth. Proc. Natl. Acad. Sci. USA, 102, 18736-18741.
59. Torii, K.U., McNellis, T.W., and, Deng, X.W., (1998) Functional dissection of Arabidopsis COP1 reveals specific roles of its three structural modules in light control of seedling development. EMBO J., 17, 5577-5587.
60. Traas, J., Hülskamp, M., Gendreau, E., and, Höfte, H., (1998) Endoreduplication and development: rule without dividing. Curr. Opin. Plant Biol., 1, 498-503.
61. Voinnet, O., Pinto, Y.M., and, Baulcombe, D.C., (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA, 96, 14147-14152.
62. Wei, N., Serino, G., and, Deng, X.W., (2008) The COP9 signalosome: more than a protease. Trends Biochem. Sci., 33, 592-600.
63. Wenkel, S., Turck, F., Singer, K., Gissot, L., Le Gourrierec, J., Samach, A., and, Coupland, G., (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell, 18, 2971-2984.
64. Whitelam, G.C., and, Halliday, K.J., (2007) Light and Plant Development. Oxford; Ames, Iowa: Blackwell Pub.
65. Yi, C., and, Deng, X.W., (2005) COP1-from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol., 15, 618-625.
66. Yin, Y., Cheong, H., Friedrichsen, D., Zhao, Y., Hu, J., Mora-Garcia, S., and, Chory, J., (2002) A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proc. Natl Acad. Sci. USA, 99, 10191-10196.
67. Yu, J.W., Rubio, V., Lee, N.Y., et al. (2008) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol. Cell, 32, 617-630.
68. Yu, X., Sayegh, R., Maymon, M., Warpeha, K., Klejnot, J., Yang, H., Huang, J., Lee, J., Kaufman, L., and, Lin, C., (2009) Formation of nuclear bodies of Arabidopsis CRY2 in response to blue light is associated with its blue light-dependent degradation. Plant Cell, 21, 118-130.
69. Yu, X., Liu, H., Klejnot, J., and, Lin, C., (2010) The Cryptochrome Blue Light Receptors. Arabidopsis Book, 8, e0135.
70. Zhu, D., Maier, A., Lee, J.H., Laubinger, S., Saijo, Y., Wang, H., Qu, L.J., Hoecker, U., and, Deng, X.W., (2008) Biochemical characterization of Arabidopsis complexes containing CONSTITUTIVELY PHOTOMORPHOGENIC1 and SUPPRESSOR OF PHYA proteins in light control of plant development. Plant Cell, 20, 2307-2323.
71. Zuo, Z., Liu, H., Liu, B., Liu, X., and, Lin, C., (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr. Biol., 21, 841-847. Bundesministerium für Bildung und Forschung