摘要
植物感受外界光信号的变化,并改变体内一些重要基因的表达,从而导致生长发育的变化。这种信号传导系统包括光信号输入途径,生物钟振荡器系统和信号输出系统三部分。ZTL蛋白既是蓝光受体,又影响生物钟蛋白的稳定性,调节生物钟的功能和正常运转。本研究以对拟南芥基因AtZTL功能较详细的研究为基础,以拟南芥为研究材料,以大豆基因GmZTL为研究对象,应用一定技术分析研究GmZTL蛋白在调控生物振荡器和信号输出路径及光周期影响开花途径中的生物学功能。
通过生物信息学分析发现,GmZTL和AtZTL的同源性高达85.9%,但是GmZTL蛋白还含有一个WD、两个F-Box、一个Radical SAM、一个PPR重复区域,这些功能区域在AtZTL中是没有的。
以拟南芥为材料分别过表达GmZTL、GFP:GmZTL和GmZTL:GFP等基因,发现这些过表达植株的表现型与AtZTL过表达植株的表现型十分类似:(1)GmZTL过表达植株在长日下和野生型相比表现出晚开花,但是在短日下,部分GmZTL过表达植株又表现出和野生型相比晚花的表现型;(2)GFP:GmZTL和GmZTL:GFP过表达植株表现出和GmZTL过表达植株相类似的表现型;(3)GmZTL过表达植株在红光下表现出下胚轴伸长,但在蓝光下的表现型与野生型一致;(4)GmZTL mRNA的表达无论在长日还是在短日下都没有生物节律的变化;(5)GmZTL在上胚轴、单叶、第三复叶、花和荚中的表达水平很高,为组成型表达。结果表明,大豆GmZTL可能具有拟南芥ZTL类似的功能,但还具有拟南芥ZTL所不具备的新功能,是生物钟的调节元件之一。本研究结果为开花分子机理的深入研究和生产应用奠定了重要基础。
The plant perceives the environmental signals and alters in its development pathway by changing the expression patterns of many genes.This signal cascade includes the input pathway of the clock,the central oscillator and the output pathway of the clock. ZTL protein not only acts as a photoreceptor of blue light,but also influences the stabilization of the clock protein and regulates clock functions and maintains regular running of the clock.This research is based on the detailed functional understand of AtZTL and take Arabidopsis as research material and GmZTL as object to study.We applied some technologies to study the biological function of GmZTL protein in regulating biological oscillator and signal output ways and the influence of photoperiod to flowering pathway.
The analysis of bioinformatics of GmZTL and AtZTL showed that there is 85.9% identity between them and they are in the closest relation compared to homologs in other plants.There are several domains found in GmZTL but not in AtZTL,such as a WD,two F-Box,a Radical SAM and a PPR repeat.
We have created the overexpressors of GmZTL,GFP:GmZTL and GmZTL:GFP in Arabidopsis and found that these overexpressors showed a very similar phenotype with that of AtZTL.(1) The overexpressors of GmZTL flower late in long days compared to the wild type.But in short days many overexpressors of GmZTL show a phenotype of early flowering compared to wild type(2) The overexpressors of GFP:GmZTL and GmZTL:GFP show a very similar phenotype with the overexpressors of GmZTL.(3) Compared to their parents(ztl mutation),the overexpressors of GmZTL have a long hypocotyl in red light,but not in blue light.(4) The expression of GmZTL mRNA did not show circadian change in long days or short days.(5) GmZTL is constitutive expression,but high levels in epicotyls,unifoliolates,the third trifoliolates,flowers and pods.In summary,GmZTL may have not only similar functions to that of AtZTL but some new functions,and it is a regulator of the clock.The results paved a way in further researching in the molecular mechanism of flowering and the production in soybean.
引文
1.Ahmad M,Cashmore AR.HY4 gene of A.thaliana encodes a protein with characteristics of a blue-light photoreceptor.Nature(1993)366:162-166.
2.Alabadi D,Oyama T,Yanovsky MJ,Harmon FG,Mas P,Kay SA.Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock.Science(2001)293:880-889
3.Allen T,Koustenis A,Theodorou G,Somers DE,Kay SA,Whitelam GC,Devlin PF.Arabidopsis FHY3 Specifically Gates Phytochrome Signaling to the Circadian Clock..plant cell,(2006) 18,2506-2516
4.Andrade MA,Gonzalez-Guzman M,Serrano R,Rodriguez PL.A combination of the F-box motif and kelch repeats defines a large Arabidopsis family of F-box proteins.Plant Molecular Biology(2001)46,603-614
5.Araki T,Komeda Y.Analysis of the role of the late-flowering locus,GI,in the flowering of Arabidopsis thaliana.Plant Journal(1993)3:231-239
6.Barak S,Tobin EM,Andronis C,Sugano S,Green RM.All in good time:the Arabidopsis circadian clock.Trends in plant science(2000) 5(12):517-522
7.Bouly JP,Giovarti B,Djamei A,Mueller M,Zeugner A,Dudkin EA,Batschauer A,Ahmad M.Novel ATP-binding and autophosphorylation activity associated with Arabidopsis and human cryptochrome-1.Biochem.(2003) 270,921-928.
8.Brautigam CA,Smith BS,Ma Z,Palnitkar M,Tomchick DR,Machius M,Deisenhofer J.Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana.PNAS(2004)101(33):12142-12147
9.BriggsWR,Christie JM.Phototropins 1 and 2:versatile plant blue-light receptors.Trends in Plant Science(2002)7,204-210
10.Canton F and Quail P.Both phyA and phyB mediate light-imposed repression of PHYA gene expression in Arabidopsis.Plant Physiol.(1999) 121,1207-1215
11.Clark T.and Mathews S and 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)25,413-427
12.David KM,Armbruster U,Tama N,Putterill J.Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark.FEBS Letters,(2006)580:1193-1197
13.Devlin PF,Kay SA.Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity.Plant Cell (2000)12, 2499-2510
14. Devlin PF. Signs of the time: environmental input to the circadian clock. Journal of experimental botany(2002)53(374):1535-1550.
15. Ding Z, Doyle MR, Amasino RM, Davis SJ. A complex genetic interaction between Arabidopsis thaliana TOC1 and CCA1/LHY in driving the circadian clock and in output regulation. Genetics, (2007)176,1501-1510
16. Ding Z, Millar AJ, Davis AM, Davis SJ. TIME FOR COFFEE Encodes a Nuclear Regulator in the Arabidopsis thaliana Circadian Clock. Plant Cell, (2007) 19:1522-1536
17. Doyle MR, Davis SJ, Bastow RM, McWatters HG, Kozma-Bognar L, Nagy F, Millar AJ , Amasino RM. The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature (2002)419: 74—77
18. Eriksson ME, Millar AJ. The Circadian Clock. A Plant's Best Friend in Spinning World. Plant Physiology, (2003)132: 732-738
19. Farre EM, Harmer SL, Harmon FG, Yanovsky MJ, Kay SA. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. (2005)15,47-54
20. 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 membrane-spanning domains. EMBO Journal (1999)18,4679-4688
21. Fukamatsu Y, Mitsui S, Yasuhara M, Tokioka Y, Ihara N, Fujita S, Kiyosue T. Identification of LOV KELCH PROTEIN2 (LKP2)-interacting Factors That Can Recruit LKP2 to Nuclear Bodies. Plant Cell Physiol. (2005)46(8): 1340-1349
22. Green RM, Tobin EM. Loss of the circadian clock associated protein 1 in Arabidopsis results in altered clock-regulated gene expression. Proc Natl Acad Sci (1999)96:4176-4179
23. Guo H., Duong H., Ma N., Lin C. The Arabidopsis blue light receptor cryptochrome 2 is a nuclear protein regulated by a blue light-dependent post-transcriptional mechanism. Plant Journal (1999)19:279-287.
24. Han L, Mason M, Risseeuw EP, Crosby WL, Somers DE. Formation of an SCFZTL complex is required for proper regulation of circadian timing. The Plant Journal, (2004)40: 291-301
25. 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: 2110-2113
26. Harmer SL, Panda S, Kay SA .Molecular bases of circadian rhythms. Annu Rev Cell Dev Biol (2001) 17: 215-253
27. Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, Kay SA. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. PNAS,(2005)102 (29) 10387-10392
28. Hennig L, Stoddart WM, Dieterle M, Whitelam GC, Schafer E. Phytochrome E controls light-induced germination of Arabidopsis. Plant Physiol. (2002)128,194-200.
29. Hicks, K.A.,Millar, A.J.,Carre, I.A., Somers, D.E.,Straume, M., Meeks-Wagner, D.R.,and Kay, S.A.. Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science (1996)274, 790-792
30. Hicks KA, Albertson TM, Wagner DR. EARLY FLOWERING3 Encodes a Novel Protein That Regulates Circadian Clock Function and Flowering in Arabidopsis. The Plant Cell, (2001)13,1281-1292
31. 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, 523-535.
32. Hudson, M.E., Lisch, D.R., and Quail, P.H.. The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant Journal. (2003)34,453—471
33. Huq E, Al-Sady B, Hudson M, Kim C, Apel K, Quail P. Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science (2004)305: 1937-1941
34. Huq E, Tepperman J, and Quail P. GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. PNAS (2000)97, 9789-9794
35. Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA. FKF1 is essential for photoperiodic-specific light signaling in Arabidopsis. NATURE (2003)426:302-306
36. Jarillo JA, Capel J, Tang RH, Yang HQ, Alonso JM, Ecker JR, Cashmore AR.. An Arabidopsis circadian clock component interacts with both CRY1 and phyB.NATURE, (2001)410:487-490
37. Jay C. Dunlap, Jennifer J. Loros, and Patricia J. DeCoursey. Chronobiology: Biological Timekeeping. (Sunderland, MA: Sinauer Associates) (2004)
38. Johnson, C.H. et al. A clockwork green: circadian programs in photosynthetic organisms. In Biological Rhythms and Photoperiodism in Plants (Lumsden, P.J. and Millar, A.J., eds), BIOS Scientifical Publishers, (1998) 1-34.
39. Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM. The GIGANTEA-Regulated MicroRNA172 Mediates Photoperiodic Flowering Independent of CONSTANS in Arabidopsis. Plant Cell,(2007) 19:2736-2748
40. Kaczorowski KA, Quail PH. Arabidopsis PSEUDO-RESPONSE REGULATOR7 is a signaling intermediate in phytochrome-regulated seedling deetiolation and phasing of the circadian clock. Plant Cell (2003)15,2654-2665
41. Kazama T, Toriyama K. A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett. (2003) 544:99-102
42. Kevei E, Gyula P, Hall A, Kozma-Bognar L, Kim WY, Eriksson ME, Toth R, Hanano S, Feher B, Southern MM, Bastow RM, Viczian A, Hibberd V, Davis SJ, Somers DE, Nagy F, Millar AJ. Forward Genetic Analysis of the Circadian Clock Separates the Multiple Functions of ZEITLUPE. Plant Physiology, (2006)140:933-945
43. Khanna R, Kikis EA, Quail PH. EARLY FLOWERING 4 Functions in Phytochrome B-Regulated Seedling De-Etiolation. Plant Physiology, (2003)133: 1530-1538
44. Khanna R, Shen Y, Marion CM, Tsuchisaka A, Theologis A, Schafer E, Quail PH. The Basic Helix-Loop-Helix Transcription Factor PIF5 Acts on Ethylene Biosynthesis and Phytochrome Signaling by Distinct Mechanisms. The Plant Cell, (2007) 19:3915-3929
45. Kiba T, Henriques R, Sakakibara H, Chua NH. Targeted Degradation of PSEUDO-RESPONSE REGULATOR5 by a SCFZTL Complex Regulates Clock Function and Photomorphogenesis in Arabidopsis thaliana. Plant Cell,(2007) 19:2516-2530
46. Kikis EA, Khanna R, Quail PH. ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. Plant Journal (2005)44: 300-313
47. Kikis EA, Khanna R, Quail PH. An Arabidopsis protein closely related to Synechocystis cryptochrome is targeted to organelles. Plant Journal. (2003)35:93-103.
48. Kim WY, Fujiwara S, Suh SS, Kim J, Kim Y, Han L, David K, Putterill J, Nam HG, Somers DE. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature, (2007)449, 356-360
49. Kim WY, Hicks KA, Somers DE. Independent Roles for EARLY FLOWERING 3 and ZEITLUPE in the Control of Circadian Timing,Hypocotyl Length, and Flowering Time. Plant Physiology, (2005)139: 1557-1569
50. Kim WY, Geng R, Somers DE. Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome. PNAS (2003)100 (8): 4933-4938
51. Kiyosue T, Wada M. LKP1(LOV kelch proteinl):a factor involved in the regulation of flowering time in Arabidopsis.The Plant Journal, (2000)23(6):807-815
52. Klar T, Pokorny R, Moldt J, Batschauer A, Essen LO. Cryptochrome 3 from Structural Arabidopsis thaliana: Structural and Functional Analysis of its Complex with a Folate Light Antenna. J. Mol. Biol. (2007) 366,954-964
53. Kotera E, Tasaka M and Shikanai T. A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. NATURE, (2005)433:326-330
54. Lin C and Shalitin D. CRYPTOCHROME STRUCTURE AND SIGNAL TRANSDUCTION. Annu. Rev. Plant Biol. (2003)54,469-496
55. Lin C, Shalitin D. Cryptochrome structure and signal transduction. Annual Review of Plant Biology (2003) 54,469-496
56. Lin C, Yang H, Guo H, Mockler T, Chen.J and Cashmore A. Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. PNAS (1998) 95:2686-2690
57. Lin R, Wang H. Arabidopsis FHY3/FAR1 gene family and distinct roles of its members in light control of Arabidopsis development. Plant Physiol. (2004)136, 4010-4022
58. Liu XL, Covington MF, Fankhauser C, Chory J, Wagner DR. ELF3 Encodes a Circadian Clock-Regulated Nuclear Protein That Functions in an Arabidopsis PHYB Signal Transduction Pathway. The Plant Cell, (2001)13,1293-1304
59. Martin-Tryon E, Kreps J, and Harmer J. GIGANTEA Acts in Blue Light Signaling and Has Biochemically Separable Roles in Circadian Clock and Flowering Time Regulation.Plant Physiology,(2007) 143:473-486
60.Mas P,Alabadi D,Yanovsky MJ,Oyama T,Kay SA.Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis.Plant Cell (2003) 15:223-236
61.Mas P,Kim WY,Somers DE,Kay SA.Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana.NATURE,(2003)426:567-570
62.Matsushika A,Imamura A,Yamashino T,Mizuno T.Aberrant expression of the light-inducible and circadian-regulated APRR9 gene belonging to the circadian-associated TOC1 quintet results in the phenotype of early flowering inArabidopsis thaliana.Plant Cell Physiol(2002)43:833-843
63.Matsushika A,Kawamura M,Nakamura Y,Kato T,Murakami M,Yamashino T,Mizuno T.Characterization of circadian-associated pseudo-response regulators:Ⅱ.the function of PRR5 and its molecular dissection in Arabidopsis thaliana.Biosci.Biotechnol.Biochem,(2007)71(2):535-544
64.Matsushika A.,Makino S.,Kojima M.,and Mizuno T.Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana:Insight into the plant circadian clock.Plant Cell Physiol.(2000)41:1002-1012
65.Matsushita T.,Mochizuki N.,and Nagatani.Dimers of the N-terminal domain of phytochrome B are functional in the nucleus.Nature(2003)424,571-574.
66.Matsushika A,Imamura A,Yamashino T,Mizuno T.Discovery of Two Novel Radical S-Adenosylmethionine Proteins Required for the Assembly of an Active [Fe]Hydrogenase.THE JOURNAL OF BIOLOGICAL CHEMISTRY,(2004)279:25711-25720
67.McWatters HG,Bastow RM,Hall A,Millar AJ.The ELF3 zeitnehmer regulates light signaling to the circadian clock.Nature(2000)408,716-720.
68.McWatters.H,Kolmos.E,AnthonyHall,Doyle.M,RichardM.Amasino,Peter Gyula,Ferenc Nagy,Andrew J.Millar,and Seth J.Davis.ELF4 Is Required for Oscillatory Properties of the circadian Clock.Plant Physiology,(2007)144:491-401
69.Michael TP,Salome PA,Yu HJ,Spencer TR,Sharp EL,McPeek MA,Alonso JM,Ecker JR,McClung CR.Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science (2003)302, 1049-1053
70. Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song HR, Carre IA, Coupland G LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell (2002)2: 629-641.
71. Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J, Coupland G Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell (2005)17: 2255-2270
72. Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M,Song HR, Carre IA, Coupland G LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell (2002)2: 629-644
72. Mizuno T, Nakamichi N. Pseudo-Response Regulators (PRRs) or True Oscillator Components (TOCs). Plant Cell Physiol, (2005)46(5): 677-685
74. Mockler T, Yang H, Yu X, Parikh D, Cheng YC, Dolan S, Lin C. Regulation of flowering time by Arabidopsis photoreceptors. Science (1998)279:1360-1363.
75. Monte E, Tepperman J, AlSady B, Kaczorowski K, Alonso J, Ecker J, Li X, Zhang Y, and Quail P.The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proc.Natl. Acad. Sci. (2004) 16: 16091-16098
76. Murakami M, Tago Y, Yamashino T, Mizuno T. Comparative Overviews of Clock-Associated Genes of Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol. (2007)48(1): 110-121.
77. Nakamichi N., Kita M., Ito S., Sato E., Yamashino T., and Mizuno T.. PSEUDO-RESPONSE REGULATORS, PRR9,PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol. (2005)46,686-698
78. Nelson D, Lasswell J, Rogg L, Cohen M and Bartel B. FKF1, a Clock-Controlled Gene that Regulates the Transition to Flowering in Arabidopsis. Cell, (2000) 101, 331-340
79. Niinuma.K, Nakagawa.M, Calvino.M, Mizoguchi.T. Dance of plants with circadian clock. Plant Biotechnology (2007)24, 87-97
80. Norihito N., Masanori K., Shogo I., Yamashino T. and Mizuno T. "PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana". Plan Cell Physiol. (2005)46:686-698
81. Oliverio KA, Crepy M, Martin-Tryon EL, Milich R, Harmer SL, Putterill J, Yanovsky MJ, Casal JJ. GIGANTEA regulates phytochrome A-mediated photomorphogenesis independently of its role in the circadian clock. Plant Physiology,(2007)144(1): 495-502
82. Onai K, Ishiura M. PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock. Genes to Cells (2005)10, 963-972
83. Para A, Farre EM, Imaizumi T, Pruneda-Paz JL, Harmon FG, Kay SA. PRR3 Is a Vascular Regulator of TOC1 Stability in the Arabidopsis Circadian Clock. Plant Cell,(2007) 19:3462-3473
84. Parks.B and Spalding.B. Sequential and coordinated action of phytochromes A and B during Arabidopsis stem growth revealed by kinetic analysis. Plant Biology, (1999)96,14142-14146.
85. Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science (1999)285,1579-1582
86. Pittendrigh C . On the temperature independence in the clock system controlling emergence time in Drosophila. Proc. Natl. Acad Sci. (1954)40, 1018-1029
87. Rutter.J. PAS Domains and Metabolic Status Signaling. Science, (2002) 298:1567-1568
88. SALOME P. A.; MCCLUNG C. R. What makes the Arabidopsis clock tick on time? A review on entrainment. Plant, Cell and Environment, (2005)28,21-38
89. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science (2000) 288: 1613-1616
90. Sawada Y, Aoki M, Nakaminami K, Mitsuhashi W, Tatematsu K, Kushiro T, Koshiba T, Kamiya Y, Inoue Y, Nambara E, Toyomasu T. Phytochrome- and Gibberellin-Mediated Regulation of Abscisic Acid Metabolism during Germination of Photoblastic Lettuce Seeds. Plant Physiology Preview, (2008)
91. Sawa M, Nusinow DA, Kay SA, Imaizumi T. FKF1 and GIGANTEA Complex Formation Is Required for Day-Length Measurement in Arabidopsis. Science (2007)318:261-265
92. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre IA, Coupland G. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering.Cell(1998)93:1219-1229
93.Schultz TF.and Kay S.A.Circadian clocks in daily and seasonal control of development.Science(2003) 301:326-328
94.Schultz TF,Kiyosue T,Yanovsky M,Wada M,Kay SA.A role for LKP2 in the circadian clock of Arabidopsis.The Plant Cell(2001) 13,2659-2670
95.Selby CP,Sancar A.A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity.PNAS(2006) 103:17696-17700.
96.Shalitin D,Yang H,Mockler T,Maymon M,Guo H,Whitelam G and Lin C.(2002)Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation.Nature 417:763-767.
97.Shalitin D,Yu X,Maymon M,Mockler T,and Lin C.Blue Light-Dependent in Vivo and in Vitro Phosphorylation of Arabidopsis Cryptochrome 1.The Plant Cell,(2003) 15,2421-2429
98.Smith T.F.,Gaitatzes C.,Saxena K.and Neer E.J..The WD repeat:a common architecture for diverse functions.Trends Biochem.Sci.(1999)24:181-185
99.Somers DE and Quail PH.Temporal and spatial expression patterns of PHYA and PHYB genes in Arabidopsis.Plant Journal.(1995)7,413-427
100.Somers D.Clock-associated genes in Arabidopsis:a family affair.Phil.Trans.R.Soc.Lond.B(2001)356:1745-1753
101.Somers DE,Webb AA,Pearson M,Kay SA.The short-period mutant,tocl-1,alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana.Development(1998) 125:485-494.
102.Sofia.H,Chen.G,Hetzler.B,Reyes-Spindola.J and Miller.N.Radical SAM,a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanism:functional characterization using new analysis and information visualization methods.Nucleic Acids Research,(2001)29:1097-1106
103.Somers D,Devlin P,Kay S.Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock.Science(1998)282:1488-1490.
104.Somers.D,Kim.W,and Geng.R.The F-Box Protein ZEITLUPE Confers Dosage-Dependent Control on the Circadian Clock,Photomorphogenesis,and Flowering Time.The Plant Cell,(2004)16:769-782
105.Somers D,Schultz T,Milnamow M,and Kay S.ZEITLUPE Encodes a Novel Clock-Associated PAS Protein from Arabidopsis.Cell,(2000) 101:319-329
106. 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: 768-771
107. Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature (2001) 410: 1116-1120
108. Sugano S., Andronis C, Green R. M., Wang Z. Y., and Tobin E. M. Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein. Proc. Natl. Acad. Sci. (1998)95:11020-11025
109. Taylor BL, Zhulin IB. PAS Domains: Internal Sensors of Oxygen, Redox Potential, and Light. Microbiol Mol Biol Rev, (1999)63: 479-506
110. Tseng TS, Salome PA, McClung CR, Olszewski NE. SPINDLY and GIGANTEA interact and act in Arabidopsis thaliana pathways involved in light responses,flowering and rhythms in leaf movements. Plant Cell (2004)16, 1550-1563
111. Vierstra RD. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. (2003)8,135-142
112. Vreede J, van der Horst MA, Hellingwerf KJ, Crielaard W, van Aalten DM. PAS Domains. Common structure and common flexibility .The Journal of Biological Chemistry, (2003) 278: 18434-18439
113. Wagner D., Fairchild C.D., Kuhn R.M., and Quail P.H. Chromophore-bearing NH-terminal domains of 2 phytochromes A and B determine their photosensory specificity and differential light lability. Proc. Natl. Acad. Sci. (1996)93, 4011-4015.
114. Wang.H, Ma.L, Li.J, Zhao.H, Deng.X.Direct Interaction of Arabidopsis Cryptochromes with COP1 in Mediation of Photomorphogenic Development. Science(2001) 294:154-158
115. Wang.H and Deng.X. Phytochrome signaling mechanism. In: The Arabidopsis Book (eds CR. Somerville & E.M. Mey-erowitz), American Society of Plant Biologists, Rock ville MD, USA. (2002)1-28
116. Whitelam GC, Johnson E., Peng, J., Carol P., Anderson M.L., Cowl J.S., and Harberd N.P.. Phytochrome A null mutants ofArabidopsis display a wild-type phenotype in white light. Plant Cell (1993)5,757-768
117. Winston JT, Koepp DM, Zhu C, Elledge SJ, Harper JW. A family of mammalian F-box proteins.Current Biology(1999)9,1180-1182
118.Xiao W,Jang JC.F-box proteins in Arabidopsis.Trends in Plant Science(2000)5,454-457
119.Yang HQ,Tang RH,Cashmore AR..The Signaling Mechanism of Arabidopsis CRY1 Involves Direct Interaction with COP1.Plant Cell(2001) 13,2573-2587
120 Yamamoto Y,Sato E,Shimizu T,Nakamich N,Sato S,Kato T,Tabata S,Nagatani A,Yamashino T,Mizuno T.Comparative Genetic Studies on the APRR5 and APRR7 Genes Belonging to the APRR1/TOC1 Quintet Implicated in Circadian Rhythm,Control of Flowering Time,and Early Photomorphogenesis.Plant Cell Physiol,(2003)44(11):1119-1130
121.Yanovsky MJ,Kay SA.Living by the calender:how plants know when to flower.Nat.Rev.Mol.Cell.Biol.(2003)4:265-275
122.Yasuhara M,Mitsui S,Hirano H,Takanabe R,Tokioka Y,Ihara N,Komatsu A,Seki M,Shinozaki K,Kiyosue T.Identification of ASK and clock-associated proteins as molecular partners of LKP2(LOV kelch protein 2) in Arabidopsis.Journal of Experimental Botany,(2004)55:2015-2027
123.Yu L.,Gaitatzes C.,Neer E.and Smith TF.Thirty-plus functional families from a single motif.Protein Sci.(2000)9:2470-2476