Identification of primary target genes of phytochrome signaling. Early transcriptional control during shade avoidance responses in arabidopsis

Plant Physiology

Volumn 141, Issue 1, 2006, Pages 85-96

  Roig Villanova, Irma ^a   Bou, Jordi ^a   Sorin, Céline ^a   Devlin, Paul F ^b   Martínez García, Jaime F ^a,c  

^a INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; GROWTH KINETICS; MUTAGENESIS;

ARABIDOPSIS; LIGHT-GROWN PLANTS; PHYTOCHROME SIGNALING; SHADE AVOIDANCE SYNDROME (SAS);

PLANTS (BOTANY);

GENES; GROWTH; PHOTORECEPTORS; PLANTS; SEEDLINGS;

ARABIDOPSIS;

EID: 33745436506     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.076331     Document Type: Article

References (65)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
2. Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1: 213-222
3. Bauer D, Viczián A, Kircher S, Nobis T, Nitschke R, Kunkel T, Panigrahi KCS, Adám E, Fejes E, Schäfer E, et al (2004) Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16: 1433-1445
4. Boccalandro HE, Rossi MC, Saijo Y, Deng XW, Casal JJ (2004) Promotion of photomorphogenesis by COP1. Plant Mol Biol 56: 905-915
5. Boylan MT, Quail PH (1991) Phytochrome A overexpression inhibits hypocotyl elongation in transgenic Arabidopsis. Proc Natl Acad Sci USA 88: 10806-10810
6. Carabelli M, Morelli G, Whitelam G, Ruberti I (1996) Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proc Natl Acad Sci USA 93: 3530-3535
7. Carabelli M, Sessa G, Baima S, Morelli G, Ruberti I (1993) The Arabidopsis Athb-2 and Athb-4 genes are strongly induced by far-red-rich light. Plant J 4: 469-479
8. Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38: 87-117
9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
10. Craft J, Samalova M, Baroux C, Townley H, Martínez A, Jepson I, Tsiantis M, Moore I (2005) New pOp/LhG4 vectors for stringent glucocorticoid-dependent transgene expression in Arabidopsis. Plant J 41: 899-918
11. Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldman KA, Quail PH (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-finger motif and a G beta regulatory domain. Cell 71: 791-801
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 Arabidopsis by controlling elongation and flowering time. Plant Physiol 119: 1479-1487
14. Devlin PF, Yanovsky MJ, Kay SA (2003) A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol 133: 1-13
15. Duek PD, Elmer MV, van Oosten VR, Fankhauser C (2004) The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr Biol 14: 2296-2301
16. Edwards K, Johnstone C, Thomson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19: 1349
17. Fairchild CD, Schumaker MA, Quail PH (2000) HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev 14: 2377-2391
18. Hardtke CS, Deng XW (2000) The cell biology of the COP/DET/FUS proteins: regulating proteolysis in photomorphogenesis and beyond? Plant Physiol 124: 1548-1557
19. Holm M, Ma LG, Qu JL, Deng XW (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev 16: 1247-1259
20. Huq E, Al-Sady B, Hudson M, Kim C, Apel K, Quail PH (2004) PHYTOCHROME-INTERACTING FACTOR 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305: 1937-1941
21. Huq E, Al-Sady B, Quail PH (2003) Nuclear translocation of the photoreceptor phytochrome B is necessary for its biological function in seedling photomorphogenesis. Plant J 35: 660-664
22. Huq E, Quail PH (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21: 2441-2450
23. Jan YN, Jan YJ (1993) Functional gene cassettes in development. Proc Natl Acad Sci USA 90: 8305-8307
24. Khanna R, Huq E, Kikis EA, Al-Sady B, Lanzatella C, Quail PH (2004) A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic-helix-loop-helix transcription factors. Plant Cell 16: 3033-3044
25. Kim J, Yi H, Choi G, Shin B, Song PS, Choi G (2003) Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15: 2399-2407
26. Kircher S, Gil F, Kozma-Bognár L, Fejes E, Speth V, Husselstein-Muller T, Bauer D, Ádám E, Schäfer E, Nagy F (2002) Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14: 1541-1555
27. Li J, Nagpal F, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272: 398-401
28. Luccione LG, Oliveiro KA, Yanovsky MJ, Boccalandro HE, Casal JJ (2002) Brassinosteroid mutants uncover fine tuning of phytochrome signaling. Plant Physiol 128: 173-181
29. Ma L, Zhao H, Deng XW (2003) Analysis of the mutational effects of the COP/DET/FUS loci on genome expression profiles reveals their overlapping yet not identical roles in regulating Arabidopsis seedling development. Development 130: 969-981
30. Martínez-García JF, Huq E, Quail PH (2000) Direct targeting of light signals to a promoter element-bound transcription factor. Science 288: 859-863
31. Martínez-García JF, Virgos-Soler A, Prat S (2002) Control of photoperiod-regulated tuberization in potato by the Arabidopsis flowering-time gene CONSTANS. Proc Natl Acad Sci USA 99: 15211-15216
32. McNellis TW, von Arnim AG, Araki T, Komeda Y, Misera S, Deng XW (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
33. Monte E, Tepperman JM, Al-Sady B, Kaczorowski KA, Alonso JM, Ecker JR, Li X, Zhang Y, Quail PH (2004) The phytochrome-interacting transcription factor, PIF3, acts early, selectively and positively in light-induced chloroplast development. Proc Natl Acad Sci USA 101: 16091-16098
34. Ni M, Tepperman JM, Quail PH (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95: 657-667
35. Oh E, Kim J, Park E, Kim J-I, Kang C, Choi G (2004) PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16: 3045-3058
36. Ohgishi M, Oka A, Morelli G, Ruberti I, Aoyama T (2001) Negative autoregulation of the Arabidopsis homeobox gene ATHB-2. Plant J 25: 389-398
37. Osterlund MT, Ang L-H, Deng XW (1999) The role of COP1 in repression of Arabidopsis photomorphogenenic development. Trends Cell Biol 9: 113-118
38. Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462-466
39. Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11: 2983-2995
40. Pepper A, Delaney T, Washburn T, Poole D, Chory J (1994) DET1, a negative regulator of light-mediated development and gene expression in Arabidopsis, encodes a novel nuclear-localized protein. Cell 78: 109-116
41. Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3: 85-93
42. Rodríguez-Concepción M, Gruissem W (1999) Arachidonic acid alters tomato HMG expression and fruit growth and induces 3-hydroxy-3- methylglutaryl coenzyme A reductase-independent lycopene accumulation. Plant Physiol 119: 41-48
43. Sablowski RWM, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92: 93-103
44. Saijo Y, Sullivan JA, Wang H, Yang J, Shen Y, Rubio V, Ma L, Hoecker U, Deng XW (2003) The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HYS activity. Genes Dev 17: 2642-2647
45. Salter MG, Franklin KA, Whitelam GC (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426: 680-683
46. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288: 1613-1616
47. Sawa S, Ohgishi M, Goda H, Higuchi K, Shimada Y, Yoshida S, Koshiba T (2002) The HAT2 gene, a member of the HD-ZIP gene family, isolated as an auxin inducible gene by DNA microarray screening, affects auxin response in Arabidopsis. Plant J 32: 1011-1022
48. Schäfer E, Bowler C (2002) Phytochrome-mediated photoperception and signal transduction in higher plants. EMBO Rep 3: 1042-1048
49. Schena M, Lloyd AM, Davis RW (1993) The HAT4 gene of Arabidopsis encodes a developmental regulator. Genes Dev 7: 367-379
50. Schroeder DF, Gahrtz M, Maxwell BB, Cook RK, Kan JM, Alonso JM, Ecker JR, Chory J (2002) De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr Biol 12: 1462-1472
51. Seo HS, Watanabe E, Tokutomi S, Nagatani A, Chua NH (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev 18: 617-622
52. Seo HS, Yang JY, Ishikawa M, Bolle C, Ballesteros ML, Chua NH (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423: 995-999
53. Sessa G, Carabelli M, Sassi M, Ciolfi A, Possenti M, Mittempergher F, Becker J, Morelli G, Ruberti I (2005) A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev 19: 2811-2815
54. Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol 33: 481-518
55. Smith H, Whitelam GC (1997) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ 20: 840-844
56. Steindler C, Matteuci A, Sessa G, Weimar T, Ohgishi M, Aoyama T, Morelli G, Ruberti I (1999) Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development 126: 4235-4245
57. Suzuki G, Yanagawa Y, Kwok SF, Matsui M, Deng XW (2002) Arabidopsis COP10 is a ubiquitin-conjugating enzyme variant that acts together with COP1 and the COP9 signalosome in repressing photomorphogenesis. Genes Dev 16: 554-559
58. Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH (2001) Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc Natl Acad Sci USA 98: 9437-9442
59. Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15: 1749-1770
60. Valvekens D, Van Montagu M, Van Lijsebettens M (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants using kanamycin selection. Proc Natl Acad Sci USA 85: 5536-5540
61. von Arnim AG, Osterlund MT, Kwok SF, Deng XW (1997) Genetic and developmental control of nuclear accumulation of COP1, a repressor of photomorphogenesis in Arabidopsis. Plant Physiol 114: 779-788
62. Wagner D, Sablowski RWM, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285: 582-584
63. Wagner D, Tepperman JM, Quail PH (1991) Overexpression of phytochrome B induces short hypocotyl phenotype in transgenic Arabidopsis. Plant Cell 3: 1275-1288
64. Yamashino T, Matsushika A, Fujimori T, Sato S, Kato T, Tabata S, Mizuno T (2003) A link between circadian-controlled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol 44: 619-629
65. Yanagawa Y, Sullivan JA, Komatsu S, Gusmaroli G, Suzuki G, Yin J, Ishibashi T, Saijo Y, Rubio V, Kimura S, et al (2004) Arabidopsis COP10 forms a complex with DBB1 and DET1 in vivo and enhances the ubiquitin conjugating enzymes. Genes Dev 18: 2171-2181