Biopolym. Cell. 2004; 20(6):451-471.
Reviews
Genetical and epigenetical control of plant growth and development. Genes of photomorphogenesis and regulation of their expression by light
1Tsygankova V. A., 1Galkina L. A., 1Musatenko L. I., 2Sytnik K. M.
  1. V. Ye. Lashkaryov Institute of Semiconductor Physics, NAS of Ukraine
    41, Prospect Nauki, Kyiv, Ukraine, 03028
  2. M. G. Kholodny Institute of Botany, NAS of Ukraine
    2, Tereschenkivska Str., Kyiv, Ukraine, 01601

Abstract

The review is devoted to the analysis of literary data discovering mechanisms of light signals perception by plant cells and their realization on a genetic level. The physiological and biochemical characteristics of photoreceptors, i. e. effectors, which perceive light signals, and their classification according to the functional role are presented: 1) the red/far-red light-absorbing phytochromes and red light-perceiving chlorophyll; 2) the blue/UV-A/UV-B selectively light-absorbing photoreceptors: cryptochromes, phototropins and carotenoids as well as data about genes encoding photoreceptors phytochromes (PHYA-PHYE genes), cryptochromes (CRY1 and CRY2 genes) and phototropins (NPH and NPL1 genes) in Arabidopsis. The greatest attention in the review is assigned to the consideration on concrete genes, the expression of which is regulated by light signals through phytochrome A (FHY1, FHY3, SPA1, FIN2, FIN219, FAR1 genes); phytochrome B (RED1, PEF2, PEF3, PKS1, ATHB-2 genes) as well as through both phytochrome A and phytochrome B (PEF1, PSI2, PIF3, NDPK2, HY5, Elip genes). The data about discovering new genes: COP1, DET1, COP9, COP10 and SHL genes-the negative regulators of morphogenesis at dark, that act downstream of both phytochromes and cryptochromes are presented. The information concerns also the identification of the numerous genes referred to molecular physiological clock (endogenous oscillator) signaling components, which are involved in transducing the environmental signals to oscillator: ZTL, FKF1, LKP2, TOC1, CCA1, LHY, ELF3, GL, PHYA-PHYE, CRY1 and CRY2 genes as well s signaling components, which perceive information from oscillator: CAB2, CCR2, CAT3, psbA, psbD. The evidences about signal interaction of phytochromes and phytohormones are presented.

References

[1] Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW. Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell. 2001;13(12):2589-607.
[2] Thum KE, Kim M, Christopher DA, Mullet JE. Cryptochrome 1, cryptochrome 2, and phytochrome a co-activate the chloroplast psbD blue light-responsive promoter. Plant Cell. 2001;13(12):2747-60.
[3] Neff MM, Fankhauser C, Chory J. Light: an indicator of time and place. Genes Dev. 2000;14(3):257-71.
[4] Harari-Steinberg O, Ohad I, Chamovitz DA. Dissection of the light signal transduction pathways regulating the two early light-induced protein genes in Arabidopsis. Plant Physiol. 2001;127(3):986-97.
[5] Hsieh HL, Okamoto H, Wang M, Ang LH, Matsui M, Goodman H, Deng XW. FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev. 2000;14(15):1958-70.
[6] Hall A, Kozma-Bognar L, Toth R, Nagy F, Millar AJ. Conditional circadian regulation of PHYTOCHROME A gene expression. Plant Physiol. 2001;127(4):1808-18.
[7] Garner WW, Allard HA. Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J Agric Res. 1920; 18:553-606.
[8] Borthwick HA, Hendricks SB, Parker MW, Toole EH, Toole VK. A Reversible Photoreaction Controlling Seed Germination. Proc Natl Acad Sci U S A. 1952;38(8):662-6.
[9] Butler WL, Norris KH, Siegelman HW, Hendricks SB. Detection, assay, and preliminary purification of the pigment controlling photoresponsive development of plants. Proc Natl Acad Sci U S A. 1959;45(12):1703-8.
[10] Kendrick R. E., Kronenberg G. H. M. Photomorphogenesis in plants. Dordrecht: Kluver Acad. Publ., 1994.
[11] Yeh KC, Lagarias JC. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc Natl Acad Sci U S A. 1998;95(23):13976-81.
[12] Yeh KC, Wu SH, Murphy JT, Lagarias JC. A cyanobacterial phytochrome two-component light sensory system. Science. 1997;277(5331):1505-8.
[13] Mancinelli A. L. The physiology of phytochrome actions. Photomorphogenesis in plants. Eds R. E. Kendrick, G. H. M. Kronenberg. Dordrecht: Kluver Acad. Publ., 1994:211-269.
[14] Roux S. J. Signal transduction in phytochrome responses. Photomorphogenesis in plants. Eds R. E. Kendrick, G. H. M. Kronenberg. Dordrecht: Kluver Acad. Publ., 1994:187-209.
[15] Vince-Prue D. The duration of light and photoperiodic responses. Photomorphogenesis in plants. Eds R. E. Kendrick, G. H. M. Kronenberg. Dordrecht: Kluver Acad. Publ., 1994:447-490.
[16] Smith H, Whitelam GC. The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ. 1997; 20(6):840-844.
[17] Shinomura T, Nagatani A, Hanzawa H, Kubota M, Watanabe M, Furuya M. Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1996;93(15):8129-33.
[18] Cerdan PD1, Staneloni RJ, Casal JJ, Sanchez RA. A 146 bp fragment of the tobacco Lhcb1*2 promoter confers very-low-fluence, low-fluence and high-irradiance responses of phytochrome to a minimal CaMV 35S promoter. Plant Mol Biol. 1997;33(2):245-55.
[19] Cerdan PD, Yanovsky MJ, Reymundo FC, Nagatani A, Staneloni RJ, Whitelam GC, Casal JJ. Regulation of phytochrome B signaling by phytochrome A and FHY1 in Arabidopsis thaliana. Plant J. 1999;18(5):499-507.
[20] Shinomura T, Uchida K, Furuya M. Elementary processes of photoperception by phytochrome A for high-irradiance response of hypocotyl elongation in Arabidopsis. Plant Physiol. 2000;122(1):147-56.
[21] McCourt P. Genetic analysis of hormone signalling. Annu Rev Plant Physiol Plant Mol Biol. 1999; 50(1):219-243.
[22] Becraft PW, Kang SH, Suh SG. The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. Plant Physiol. 2001;127(2):486-96.
[23] Toth R, Kevei E, Hall A, Millar AJ, Nagy F, Kozma-Bognar L. Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiol. 2001;127(4):1607-16.
[24] Abe H, Takio K., Titani K, Furuya M. Amino-terminal amino acid sequences of pea phytochrome II fragments obtained by limited proteolysis. Plant Cell Physiol. 1989; 30(8):1089-97.
[25] Clack T, Mathews S, Sharrock RA. The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol Biol. 1994;25(3):413-27.
[26] Clough RC, Jordan-Beebe ET, Lohman KN, Marita JM, Walker JM, Gatz C, Vierstra RD. Sequences within both the N- and C-terminal domains of phytochrome A are required for PFR ubiquitination and degradation. Plant J. 1999;17(2):155-67.
[27] Somers DE, Quail PH. Phytochrome-Mediated Light Regulation of PHYA- and PHYB-GUS Transgenes in Arabidopsis thaliana Seedlings. Plant Physiol. 1995;107(2):523-534.
[28] Shinomura T, Nagatani A, Chory J, Furuya M. The Induction of Seed Germination in Arabidopsis thaliana Is Regulated Principally by Phytochrome B and Secondarily by Phytochrome A. Plant Physiol. 1994;104(2):363-371.
[29] Nagatani A, Reed JW, Chory J. Isolation and Initial Characterization of Arabidopsis Mutants That Are Deficient in Phytochrome A. Plant Physiol. 1993;102(1):269-277.
[30] Johnson E, Bradley M, Harberd NP, Whitelam GC. Photoresponses of Light-Grown phyA Mutants of Arabidopsis (Phytochrome A Is Required for the Perception of Daylength Extensions). Plant Physiol. 1994;105(1):141-149.
[31] Somers DE, Devlin PF, Kay SA. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science. 1998;282(5393):1488-90.
[32] Reed JW, Nagatani A, Elich TD, Fagan M, Chory J. Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development. Plant Physiol. 1994;104(4):1139-1149.
[33] Hirschfeld M, Tepperman JM, Clack T, Quail PH, Sharrock RA. Coordination of phytochrome levels in phyB mutants of Arabidopsis as revealed by apoprotein-specific monoclonal antibodies. Genetics. 1998;149(2):523-35.
[34] Devlin PF, Patel SR, Whitelam GC. Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell. 1998;10(9):1479-87.
[35] Devlin PF, Robson PR, Patel SR, Goosey L, Sharrock RA, Whitelam GC. Phytochrome D acts in the shade-avoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. Plant Physiol. 1999;119(3):909-15.
[36] Qin M, Kuhn R, Moran S, Quail PH. Overexpressed phytochrome C has similar photosensory specificity to phytochrome B but a distinctive capacity to enhance primary leaf expansion. Plant J. 1997;12(5):1163-72.
[37] Gendreau E, Hofte H, Grandjean O, Brown S, Traas J. Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J. 1998;13(2):221-30.
[38] Devlin PF, Halliday KJ, Harberd NP, Whitelam GC. The rosette habit of Arabidopsis thaliana is dependent upon phytochrome action: novel phytochromes control internode elongation and flowering time. Plant J. 1996;10(6):1127-34.
[39] Yang HQ, Tang RH, Cashmore AR. The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell. 2001;13(12):2573-87.
[40] Mockler TC, Guo H, Yang H, Duong H, Lin C. Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development. 1999;126(10):2073-82.
[41] Furuya M., Song P. S. Assembly and properties of holophytochrome. Photomorphogenesis in plants. Eds R. E. Kendrick, G. H. M. Kronenberg. Dordrecht: Kluver Acad. Publ., 1994:105-140.
[42] Wang X, Iino M. Interaction of cryptochrome 1, phytochrome, and ion fluxes in blue-light-induced shrinking of Arabidopsis hypocotyl protoplasts. Plant Physiol. 1998;117(4):1265-79.
[43] Christie JM, Reymond P, Powell GK, Bernasconi P, Raibekas AA, Liscum E, Briggs WR. Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science. 1998;282(5394):1698-701.
[44] Janoudi AK, Gordon WR, Wagner D, Quail P, Poff KL. Multiple phytochromes are involved in red-light-induced enhancement of first-positive phototropism in Arabidopsis thaliana. Plant Physiol. 1997;113(3):975-9.
[45] Woitzik F., Mohr H. Control of hypocotyl phototropism by phytochrome in dicotyledonous seedlings (Sesamum indicum L.). Plant Cell Environ. 1988; 11(7):653-61.
[46] Nozue K, Kanegae T, Imaizumi T, Fukuda S, Okamoto H, Yeh KC, Lagarias JC, Wada M. A phytochrome from the fern Adiantum with features of the putative photoreceptor NPH1. Proc Natl Acad Sci U S A. 1998;95(26):15826-30.
[47] Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR. Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature. 2001;410(6831):952-4.
[48] Pratt L. H. Distribution and localization of phytochrome within the plant. Photomorphogenesis in plants. Eds R. E. Kendrick, G. H. M. Kronenberg. Dordrecht: Kluver Acad. Publ., 1994:163-185.
[49] Sakamoto K, Nagatani A. Nuclear localization activity of phytochrome B. Plant J. 1996;10(5):859-68.
[50] Kircher S, Kozma-Bognar L, Kim L, Adam E, Harter K, Schafer E, Nagy F. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell. 1999;11(8):1445-56.
[51] Yamaguchi R, Nakamura M, Mochizuki N, Kay SA, Nagatani A. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J Cell Biol. 1999;145(3):437-45.
[52] Lamond AI, Earnshaw WC. Structure and function in the nucleus. Science. 1998;280(5363):547-53.
[53] Murphy JT, Lagarias JC. The phytofluors: a new class of fluorescent protein probes. Curr Biol. 1997;7(11):870-6.
[54] Lagarias JC, Rapoport H. Chromopeptides from phytochrome. The structure and linkage of the PR form of the phytochrome chromophore. J Am Chem Soc. 1980;102(14):4821–8.
[55] Davis SJ, Kurepa J, Vierstra RD. The Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases. Proc Natl Acad Sci U S A. 1999;96(11):6541-6.
[56] Kay SA. PAS, present, and future: clues to the origins of circadian clocks. Science. 1997;276(5313):753-4.
[57] Huang ZJ, Edery I, Rosbash M. PAS is a dimerization domain common to Drosophila period and several transcription factors. Nature. 1993;364(6434):259-62.
[58] Taylor BL, Zhulin IB. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev. 1999;63(2):479-506.
[59] Elich TD, Chory J. Biochemical characterization of Arabidopsis wild-type and mutant phytochrome B holoproteins. Plant Cell. 1997;9(12):2271-80.
[60] Lapko VN, Jiang X-Y, Smith DL, Song P-S. Mass spectrometric characterization of oat phytochrome A: Isoforms and posttranslational modifications. Protein Sci. 1999;8(5):1032–44
[61] Ahmad M. Seeing the world in red and blue: insight into plant vision and photoreceptors. Curr Opin Plant Biol. 1999;2(3):230-5.
[62] Fankhauser C, Yeh KC, Lagarias JC, Zhang H, Elich TD, Chory J. PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science. 1999;284(5419):1539-41.
[63] Kendrick R. E., Bossen M. E. Photocontrol of ion fluxes and membrane properties in plants. Phytochrome and photoregulation in plants. Ed. M. Furuya. Tokyo: Acad, press, 1987:215-224.
[64] Racusen R. H., Galston A. W. Developmental significance of light-mediated electrical responses in plant tissue. Photomorphogenesis. Ed. W. Shropshire, Jr., H. Mohr. Berlin: Springer, 1983:687-703.
[65] Serlin B. S., Lew R. R., Krasnoshtein F., Krol J., Sumida K. D. Phytochrome activation of K+ channels and chloroplast rotation in Mougeotia: the escape times. Plant Cell Physiol. 1996; 37(2):175-179.
[66] Wayne R, Hepler PK. The role of calcium ions in phytochrome-mediated germination of spores of Onoclea sensibilis L. Planta. 1984;160(1):12-20.
[67] Shacklock P. S., Read N. D., Trewavas A. J. Cytosolic free calcium mediates red light-induced photomorphogenesis. Nature. 1992. 358(6389):753-755.
[68] Mustilli AC, Bowler C. Tuning in to the signals controlling photoregulated gene expression in plants. EMBO J. 1997;16(19):5801-6.
[69] Choi G, Yi H, Lee J, Kwon YK, Soh MS, Shin B, Luka Z, Hahn TR, Song PS. Phytochrome signalling is mediated through nucleoside diphosphate kinase 2. Nature. 1999;401(6753):610-3.
[70] Ogura T., Tanaka N., Yabe N., Komatsu S., Hasunuma K. Characterization of protein complexes containing nucleoside diphosphate kinase with characteristics of light signal transduction through phytochrome in etiolated pea seedlings. Photochem Photobiol. 1999; 69(3):397-403.
[71] Ni M, Tepperman JM, Quail PH. PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell. 1998;95(5):657-67.
[72] Sugano S, Andronis C, Green RM, Wang ZY, Tobin EM. Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein. Proc Natl Acad Sci U S A. 1998;95(18):11020-5.
[73] Soh MS, Hong SH, Hanzawa H, Furuya M, Nam HG. Genetic identification of FIN2, a far red light-specific signaling component of Arabidopsis thaliana. Plant J. 1998;16(4):411-9.
[74] Hudson M, Ringli C, Boylan MT, Quail PH. The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev. 1999;13(15):2017-27.
[75] Hoecker U, Xu Y, Quail PH. SPA1: a new genetic locus involved in phytochrome A-specific signal transduction. Plant Cell. 1998;10(1):19-33.
[76] Halliday KJ, Hudson M, Ni M, Qin M, Quail PH. poc1: an Arabidopsis mutant perturbed in phytochrome signaling because of a T DNA insertion in the promoter of PIF3, a gene encoding a phytochrome-interacting bHLH protein. Proc Natl Acad Sci U S A. 1999;96(10):5832-7.
[77] Steindler C, Matteucci A, Sessa G, Weimar T, Ohgishi M, Aoyama T, Morelli G, Ruberti I. Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development. 1999;126(19):4235-45.
[78] Adamska I. ELIPs: light-induced stress proteins. Physiol. Plant. 1997. 100(4):794-805.
[79] Grimm B, Kloppstech K. The early light-inducible proteins of barley. Characterization of two families of 2-h-specific nuclear-coded chloroplast proteins. Eur J Biochem. 1987;167(3):493-9.
[80] Adamska I, Roobol-B?za M, Lindahl M, Andersson B. Isolation of pigment-binding early light-inducible proteins from pea. Eur J Biochem. 1999;260(2):453-60.
[81] Deng XW, Quail PH. Signalling in light-controlled development. Semin Cell Dev Biol. 1999;10(2):121-9.
[82] Wei N, Deng XW. Making sense of the COP9 signalosome. A regulatory protein complex conserved from Arabidopsis to human. Trends Genet. 1999;15(3):98-103.
[83] Osterlund MT, Ang LH, Deng XW. The role of COP1 in repression of Arabidopsis photomorphogenic development. Trends Cell Biol. 1999;9(3):113-8.
[84] Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell. 1998;1(2):213-22.
[85] Hagen G, Martin G, Li Y, Guilfoyle TJ. Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol Biol. 1991;17(3):567-79.
[86] Peng Z, Serino G, Deng XW. Molecular characterization of subunit 6 of the COP9 signalosome and its role in multifaceted developmental processes in Arabidopsis. Plant Cell. 2001;13(11):2393-407.
[87] Oyama T, Shimura Y, Okada K. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev. 1997;11(22):2983-95.
[88] Pepper AE, Seong-Kim M, Hebst SM, Ivey KN, Kwak SJ, Broyles DE. shl, a New set of Arabidopsis mutants with exaggerated developmental responses to available red, far-red, and blue light. Plant Physiol. 2001;127(1):295-304.
[89] Komeili A, O'Shea EK. Roles of phosphorylation sites in regulating activity of the transcription factor Pho4. Science. 1999;284(5416):977-80.
[90] Chory J. Light modulation of vegetative development. Plant Cell. 1997;9(7):1225-34.
[91] Kende H, Zeevaart J. The Five "Classical" Plant Hormones. Plant Cell. 1997;9(7):1197-1210.
[92] McGrath R. B., Ecker J. R. Ethylene signaling in Arabidopsis: Events from the membrane to the nucleus. Plant Physiol Biochem. 1998; 36(1-2):103-113.
[93] Jacobsen SE, Olszewski NE. Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell. 1993;5(8):887-96.
[94] Jackson SD, James P, Prat S, Thomas B. Phytochrome B affects the levels of a graft-transmissible signal involved in tuberization. Plant Physiol. 1998;117(1):29-32.
[95] Li J., Chory J. Brassinosteroid actions in plants. J Exp Bot. 1999; 50(332):275-282.
[96] Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takatsuto S, Yoshida S, Chory J. BAS1: A gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc Natl Acad Sci U S A. 1999;96(26):15316-23.
[97] Kim BC, Soh MS, Hong SH, Furuya M, Nam HG. Photomorphogenic development of the Arabidopsis shy2-1D mutation and its interaction with phytochromes in darkness. Plant J. 1998;15(1):61-8.
[98] Tian Q, Reed JW. Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development. 1999;126(4):711-21.
[99] Schultz TF, Kiyosue T, Yanovsky M, Wada M, Kay SA. A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell. 2001;13(12):2659-70.
[100] Devlin PF, Kay SA. Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell. 2000;12(12):2499-2510.
[101] Engelmann W, Simon K, Phen CJ. Leaf movement rhythm in Arabidopsis thaliana. Z Naturforschung; 1992; 47:925-928.
[102] Dowson-Day MJ, Millar AJ. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J. 1999;17(1):63-71.
[103] Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carr? IA, Coupland G. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell. 1998;93(7):1219-29.
[104] Somers DE, Devlin PF, Kay SA. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science. 1998;282(5393):1488-90.
[105] Somers DE, Schultz TF, Milnamow M, Kay SA. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell. 2000;101(3):319-29.
[106] Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell. 2000;101(3):331-40.
[107] Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science. 2000;289(5480):768-71.
[108] Wang ZY, Tobin EM. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell. 1998;93(7):1207-17.
[109] Covington MF, Panda S, Liu XL, Strayer CA, Wagner DR, Kay SA. ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell. 2001;13(6):1305-15.
[110] Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 1999;18(17):4679-88.
[111] Adams J, Kelso R, Cooley L. The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 2000;10(1):17-24.
[112] Gu YZ, Hogenesch JB, Bradfield CA. The PAS superfamily: sensors of environmental and developmental signals. Annu Rev Pharmacol Toxicol. 2000;40:519-61.
[113] Galan JM, Peter M. Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism. Proc Natl Acad Sci U S A. 1999;96(16):9124-9.
[114] Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell. 1997;91(2):209-19.
[115] Gray WM, Estelle I. Function of the ubiquitin-proteasome pathway in auxin response. Trends Biochem Sci. 2000;25(3):133-8.
[116] Salomon M, Christie JM, Knieb E, Lempert U, Briggs WR. Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry. 2000;39(31):9401-10.
[117] Goosey L, Palecanda L, Sharrock RA. Differential patterns of expression of the Arabidopsis PHYB, PHYD, and PHYE phytochrome genes. Plant Physiol. 1997;115(3):959-69.
[118] Kim L, Kircher S, Toth R, Adam E, Schafer E, Nagy F. Light-induced nuclear import of phytochrome-A:GFP fusion proteins is differentially regulated in transgenic tobacco and Arabidopsis. Plant J. 2000;22(2):125-33.
[119] Millar AJ, Straume M, Chory J, Chua NH, Kay SA. The regulation of circadian period by phototransduction pathways in Arabidopsis. Science. 1995;267(5201):1163-6.
[120] Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science. 2000;290(5499):2110-3.
[121] Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell. 2001;13(1):113-23.
[122] Kay SA, Nagatani A, Keith B, Deak M, Furuya M, Chua NH. Rice Phytochrome Is Biologically Active in Transgenic Tobacco. Plant Cell. 1989;1(8):775-782.
[123] Zhong HH, Resnick AS, Straume M, Robertson McClung C. Effects of synergistic signaling by phytochrome A and cryptochrome1 on circadian clock-regulated catalase expression. Plant Cell. 1997;9(6):947-55.
[124] Robson PRH, Smith H. Fundamental and biotechnological applications of phytochrome transgenes. Plant Cell Environ. 1997; 20(6):831-839.
[125] Robson PR, McCormac AC, Irvine AS, Smith H. Genetic engineering of harvest index in tobacco through overexpression of a phytochrome gene. Nat Biotechnol. 1996;14(8):995-8.
[126] Thiele A, Herold M, Lenk I, Quail PH, Gatz C. Heterologous expression of Arabidopsis phytochrome B in transgenic potato influences photosynthetic performance and tuber development. Plant Physiol. 1999;120(1):73-82.
[127] Olsen J. E., Junttila O., Nielsen J., Eriksson M. E., Martinussen I., Olsson O., Sandberg G., Moritz T. Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. Plant J. 1997; 12(6):1339-1350.
[128] Kuno N, Muramatsu T, Hamazato F, Furuya M. Identification by large-scale screening of phytochrome-regulated genes in etiolated seedlings of Arabidopsis using a fluorescent differential display technique. Plant Physiol. 2000;122(1):15-24.