Photoreceptors CRYTOCHROME2 and phytochrome B control chromatin compaction in arabidopsis

Plant Physiology

Volumn 154, Issue 4, 2010, Pages 1686-1696

  van Zanten, Martijn ^a,b   Tessadori, Federico ^a,c,d   McLoughlin, Fionn ^a,c   Smith, Reuben ^a,c   Millenaar, Frank F ^a,b,e   van Driel, Roel ^a,c   Voesenek, Laurentius A C J ^a   Peeters, Anton J M ^a,b   Fransz, Paul ^a,c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d HUBRECHT INSTITUTE   (Netherlands)

^e NONE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 78649787409     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.164616     Document Type: Article

References (68)

1. Ahmad M, Jarillo JA, Cashmore AR (1998a) Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell 10: 197-207
2. Ahmad M, Jarillo JA, Smirnova O, Cashmore AR (1998b) The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro. Mol Cell 1: 939-948
3. Benvenuto G, Formiggini F, Laflamme P, Malakhov M, Bowler C (2002) The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context. Curr Biol 12: 1529-1534
4. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510
5. Campell BR, Song YG, Posch TE, Cullis CA, Town CD (1992) Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene 112: 225-228
6. Casal JJ, Mazzella MA (1998) Conditional synergism between crypto-chrome 1 and phytochrome B is shown by the analysis of phyA, phyB, and hy4 simple, double, and triple mutants in Arabidopsis. Plant Physiol 118: 19-25
7. Casal JJ, Yanovsky MJ (2005) Regulation of gene expression by light. Int J Dev Biol 49: 501-511
8. Castillon A, Shen H, Huq E (2009) Blue light induces degradation of the negative regulator phytochrome interacting factor 1 to promote photomor-phogenic development of Arabidopsis seedlings. Genetics 182: 161-171
9. Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38: 87-117
10. Chen M, Tao Y, Lim J, Shaw A, Chory J (2005) Regulation of phytochrome B nuclear localization through light-dependent unmasking of nuclear-localization signals. Curr Biol 15: 637-642
11. Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR (2000) Random GFP: cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 97: 3718-3723
12. Devlin PF, Patel SR, Whitelam GC (1998) Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell 10: 1479-1487
13. Devlin PF, Robson PRH, Patel SR, Goosey L, Sharrock RA, Whitelam GC (1999) Phytochrome D acts in the shade-avoidance syndrome in Arabi-dopsis by controlling elongation growth and flowering time. Plant Physiol 119: 909-915
14. El-Assal S, Alonso-Blanco C, Peeters AJM, Raz V, Koornneef M (2001) A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 29: 435-440
15. Fankhauser C, Chen M (2008) Transposing phytochrome into the nucleus. Trends Plant Sci 13: 596-601
16. Filiault DL, Wessinger CA, Dinneny JR, Lutes J, Borevitz JO, Weigel D, Chory J, Maloof JN (2008) Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light. Proc Natl Acad Sci USA 105: 3157-3162
17. Franklin KA, Larner VS, Whitelam GC (2005) The signal transducing photoreceptors of plants. Int J Dev Biol 49: 653-664
18. Franklin KA, Praekelt U, Stoddart WM, Billingham OE, Halliday KJ, Whitelam GC (2003) Phytochromes B, D, and E act redundantly to control multiple physiological responses in Arabidopsis. Plant Physiol 131: 1340-1346
19. Fransz P, De Jong JH, Lysak M, Castiglione MR, Schubert I (2002) Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci USA 99: 14584-14589
20. Fransz P, Soppe W, Schubert I (2003) Heterochromatin in interphase nuclei of Arabidopsis thaliana. Chromosome Res 11: 227-240
21. Fransz P, ten Hoopen R, Tessadori F (2006) Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res 14: 71-82
22. Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7: 1869-1885
23. Guo H, Duong H, Ma N, Lin C (1999) The Arabidopsis blue light receptor cryptochrome 2 is a nuclear protein regulated by a blue light-dependent post-transcriptional mechanism. Plant J 19: 279-287
24. Guo HW, Yang H, Mockler TC, Lin CT (1998) Regulation of flowering time by Arabidopsis photoreceptors. Science 279: 1360-1363
25. Gyula P, Schäfer E, Nagy F (2003) Light perception and signalling in higher plants. Curr Opin Plant Biol 6: 446-452
26. Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410: 952-954
27. Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291: 2138-2141
28. Kleiner O, Kircher S, Harter K, Batschauer A (1999) Nuclear localization of the Arabidopsis blue light receptor cryptochrome 2. Plant J 19: 289-296
29. Kohchi T, Mukougawa K, Frankenberg N, Masuda M, Yokota A, Lagarias JC (2001) The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell 13: 425-436
30. Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229: 57-66
31. Koornneef M, Rolff E, Spruit CJP (1980) Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z Pflanzen-physiol 100: 147-160
32. Lin C, Shalitin D (2003) Cryptochrome structure and signal transduction. Annu Rev Plant Biol 54: 469-496
33. Lin C, Yang H, Guo H, Mockler T, Chen J, Cashmore AR (1998) Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc Natl Acad Sci USA 95: 2686-2690
34. Liscum E, Briggs WR (1995) Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. Plant Cell 7: 473-485
35. Liu H, Yu X, Li K, Klejnot J, Yang H, Lisiero D, Lin C (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322: 1535-1539
36. Lorrain S, Genoud T, Fankhauser C (2006) Let there be light in the nucleus! Curr Opin Plant Biol 9: 509-514
37. Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13: 2589-2607
38. Martinez-Zapater JM, Estelle MA, Somerville CR (1986) A high repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet 204: 417-423
39. Más P, Devlin PF, Panda S, Kay SA (2000) Functional interaction of phytochrome B and cryptochrome 2. Nature 408: 207-211
40. Mathieu O, Jasencakova Z, Vaillant I, Gendrel AV, Colot V, Schubert I, Tourmente S (2003) Changes in 5S rDNA chromatin organization and transcription during heterochromatin establishment in Arabidopsis. Plant Cell 15: 2929-2939
41. Mazzella MA, Cerdán PD, Staneloni RJ, Casal JJ (2001) Hierarchical coupling of phytochromes and cryptochromes reconciles stability and light modulation of Arabidopsis development. Development 128: 2291-2299
42. Millenaar FF, Cox MC, van Berkel YE, Welschen RA, Pierik R, Voesenek LA, Peeters AJM (2005) Ethylene-induced differential growth of petioles in Arabidopsis: analyzing natural variation, response kinetics, and regulation. Plant Physiol 137: 998-1008
43. Millenaar FF, van Zanten M, Cox MCH, Pierik R, Voesenek LACJ, Peeters AJM (2009) Differential petiole growth in Arabidopsis thaliana: photo-control and hormonal regulation. New Phytol 184: 141-152
44. Mockler TC, Guo H, Yang H, Duong H, Lin C (1999) Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development 126: 2073-2082
45. Nagatani A, Reed JW, Chory J (1993) Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A. Plant Physiol 102: 269-277
46. Naumann K, Fischer A, Hofmann I, Krauss V, Phalke S, Irmler K, Hause G, Aurich AC, Dorn R, Jenuwein T, et al (2005) Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabi-dopsis. EMBO J 24: 1418-1429
47. Ohgishi M, Saji K, Okada K, Sakai T (2004) Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. Proc Natl Acad Sci USA 101: 2223-2228
48. Pavet V, Quintero C, Cecchini NM, Rosa AL, Alvarez ME (2006) Arabi-dopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by pseudomonas syringae. Mol Plant Microbe Interact 19: 577-587
49. Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I, et al (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16: 1021-1034
50. Reed JW, Nagatani A, Elich TD, Fagan M, Chory J (1994) Phytochrome A and phytochrome B have overlapping but distinct functions in Arabi-dopsis development. Plant Physiol 104: 1139-1149
51. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5: 147-157
52. Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98: 6969-6974
53. Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14: 1723-1735
54. Schubert I, Fransz PF, Fuchs J, de Jong JH (2001) Chromosome painting in plants. Methods Cell Sci 23: 57-69
55. Shalitin D, Yang H, Mockler TC, Maymon M, Guo H, Whitelam GC, Lin C (2002) Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature 417: 763-767
56. Soppe WJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz PF (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21: 6549-6559
57. Sullivan JA, Deng XW (2003) From seed to seed: the role of photoreceptors in Arabidopsis development. Dev Biol 260: 289-297
58. Tessadori F, Chupeau MC, Chupeau Y, Knip M, Germann S, van Driel R, Fransz P, Gaudin V (2007a) Large-scale dissociation and sequential reassembly of pericentric heterochromatin in dedifferentiated Arabi-dopsis cells. J Cell Sci 120: 1200-1208
59. Tessadori F, Schulkes RK, van Driel R, Fransz P (2007b) Light-regulated large-scale reorganization of chromatin during the floral transition in Arabidopsis. Plant J 50: 848-857
60. Tessadori F, van Driel R, Fransz P (2004) Cytogenetics as a tool to study gene regulation. Trends Plant Sci 9: 147-153
61. Tessadori F, van Zanten M, Pavlova P, Clifton R, Pontvianne F, Snoek LB, Millenaar FF, Schulkes R-K, van Driel R, Voesenek LACJ, et al (2009) Phytochrome B and histone deacetylase 6 control light-induced chromatin compaction in Arabidopsis thaliana. PLoS Genet 5: e1000638
62. Wang H, Ma LG, Li JM, Zhao HY, Deng XW (2001) Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294: 154-158
63. Wu G, Spalding EP (2007) Separate functions for nuclear and cytoplasmic cryptochrome 1 during photomorphogenesis of Arabidopsis seedlings. Proc Natl Acad Sci USA 104: 18813-18818
64. Yang HQ, Wu YJ, Tang RH, Liu D, Liu Y, Cashmore AR (2000) The C termini of Arabidopsis cryptochromes mediate a constitutive light response. Cell 103: 815-827
65. Yanovsky MJ, Mazzella MA, Casal JJ (2000) A quadruple photoreceptor mutant still keeps track of time. Curr Biol 10: 1013-1015
66. Yi C, Deng XW (2005) COP1-from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol 15: 618-625
67. Yu X, Klejnot J, Zhao X, Shalitin D, Maymon M, Yang H, Lee J, Liu X, Lopez J, Lin C (2007) Arabidopsis cryptochrome 2 completes its post-translational life cycle in the nucleus. Plant Cell 19: 3146-3156
68. Yu X, Sayegh R, Maymon M, Warpeha K, Klejnot J, Yang H, Huang J, Lee J, Kaufman L, 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