Functional analysis of COP1 and SPA orthologs from Physcomitrella and rice during photomorphogenesis of transgenic Arabidopsis reveals distinct evolutionary conservation

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Ranjan, Aashish ^a,c   Dickopf, Stephen ^a   Ullrich, Kristian K ^b   Rensing, Stefan A ^b   Hoecker, Ute ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arabidopsis; COP1; Evolution; Flowering time; Light signal transduction; Photomorphogenesis; Physcomitrella; Rice; SPA1

Indexed keywords

MESSENGER RNA; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; BRYOPSIDA; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MORPHOGENESIS; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PLANT GROWTH; PROTEIN TERTIARY STRUCTURE; RADIATION RESPONSE; RICE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRANSGENE; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; BRYOPSIDA; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; HYPOCOTYL; LIGHT; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MUTATION; ORYZA SATIVA; PHENOTYPE; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN STRUCTURE, TERTIARY; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANSGENES;

EID: 84903413244     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-178     Document Type: Article

References (74)

1. Kami C, Lorrain S, Hornitschek P, Fankhauser C. Light-regulated plant growth and development. Curr Top Dev Biol 2010, 91:29-66.
2. Whitelam GC, Halliday KJ. Light and plant development. Blackwell 2007, 30.
3. Demarsy E, Fankhauser C. Higher plants use LOV to perceive blue light. Curr Opin Plant Biol 2009, 12(1):69-74.
4. Nagatani A. Phytochrome: structural basis for its functions. Curr Opin Plant Biol 2010, 13(5):565-570.
5. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GT, Batschauer A, Ahmad M. The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 2011, 62:335-364.
6. Heijde M, Ulm R. UV-B photoreceptor-mediated signalling in plants. Trends Plant Sci 2012, 17(4):230-237.
7. Maier A, Schrader A, Kokkelink L, Falke C, Welter B, Iniesto E, Rubio V, Uhrig JF, Hulskamp M, Hoecker U. Light and the E3 ubiquitin ligase COP1/SPA control the protein stability of the MYB transcription factors PAP1 and PAP2 involved in anthocyanin accumulation in Arabidopsis. Plant J 2013, 74(4):638-651.
8. Weidler G, Zur Oven-Krockhaus S, Heunemann M, Orth C, Schleifenbaum F, Harter K, Hoecker U, Batschauer A. Degradation of Arabidopsis CRY2 is regulated by SPA proteins and phytochrome A. Plant Cell 2012, 24(6):2610-2623.
9. Li YY, Mao K, Zhao C, Zhao XY, Zhang HL, Shu HR, Hao YJ. MdCOP1 Ubiquitin E3 Ligases Interact with MdMYB1 to Regulate Light-Induced Anthocyanin Biosynthesis and Red Fruit Coloration in Apple. Plant Physiol 2012, 160(2):1011-1022.
10. Hoecker U. Regulated proteolysis in light signaling. Curr Opin Plant Biol 2005, 8(5):469-476.
11. Lau OS, Deng XW. The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci 2012, 17(10):584-593.
12. Deng X-W, Caspar T, Quail PH. cop1: A regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev 1991, 5:1172-1182.
13. Laubinger S, Fittinghoff K, Hoecker U. The SPA quartet: a family of WD-repeat proteins with a central role in suppression of photomorphogenesis in Arabidopsis. Plant Cell 2004, 16(9):2293-2306.
14. Rolauffs S, Fackendahl P, Sahm J, Fiene G, Hoecker U. Arabidopsis COP1 and SPA genes are essential for plant elongation but not for acceleration of flowering time in response to a low red light to far-red light ratio. Plant Physiol 2012, 160(4):2015-2027.
15. Laubinger S, Marchal V, Gentilhomme J, Wenkel S, Adrian J, Jang S, Kulajta C, Braun H, Coupland G, Hoecker U. Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development 2006, 133(16):3213-3222.
16. Jang S, Marchal V, Panigrahi KC, Wenkel S, Soppe W, Deng XW, Valverde F, Coupland G. Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. Embo J 2008, 27(8):1277-1288.
17. Liu LJ, Zhang YC, Li QH, Sang Y, Mao J, Lian HL, Wang L, Yang HQ. COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 2008, 20(2):292-306.
18. Crocco CD, Holm M, Yanovsky MJ, Botto JF. AtBBX21 and COP1 genetically interact in the regulation of shade avoidance. Plant J 2010, 64(4):551-562.
19. Baumgardt RL, Oliverio KA, Casal JJ, Hoecker U. SPA1, a component of phytochrome A signal transduction, regulates the light signaling current. Planta 2002, 215(5):745-753.
20. Tilbrook K, Arongaus AB, Binkert M, Heijde M, Yin R, Ulm R. The UVR8 UV-B Photoreceptor: Perception. Signaling and Response. Arabidopsis Book 2013, 11:e0164.
21. Zhu D, Maier A, Lee JH, Laubinger S, Saijo Y, Wang H, Qu LJ, Hoecker U, Deng XW. Biochemical characterization of Arabidopsis complexes containing CONSTITUTIVELY PHOTOMORPHOGENIC1 and SUPPRESSOR OF PHYA proteins in light control of plant development. Plant Cell 2008, 20(9):2307-2323.
22. Hoecker U, Quail PH. The phytochrome A-specific signaling intermediate SPA1 interacts directly with COP1, a constitutive repressor of light signaling in Arabidopsis. J Biol Chem 2001, 276:38173-38178.
23. Saijo Y, Sullivan JA, Wang H, Yang J, Shen Y, Rubio V, Ma L, Hoecker U, Deng XW. The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev 2003, 17(21):2642-2647.
24. Laubinger S, Hoecker U. The SPA1-like proteins SPA3 and SPA4 repress photomorphogenesis in the light. Plant J 2003, 35(3):373-385.
25. Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH. COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 1992, 71(5):791-801.
26. Hoecker U, Tepperman JM, Quail PH. SPA1, a WD-repeat protein specific to phytochrome A signal transduction. Science 1999, 284:496-499.
27. Balcerowicz M, Fittinghoff K, Wirthmueller L, Maier A, Fackendahl P, Fiene G, Koncz C, Hoecker U. Light exposure of Arabidopsis seedlings causes rapid de-stabilization as well as selective post-translational inactivation of the repressor of photomorphogenesis SPA2. Plant J 2011, 65(5):712-723.
28. Pacin M, Legris M, Casal JJ. COP1 re-accumulates in the nucleus under shade. Plant J 2013, 75(4):631-641.
29. Von Arnim AG, Deng X-W. Light inactivation of arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 1994, 79:1035-1045.
30. Lian HL, He SB, Zhang YC, Zhu DM, Zhang JY, Jia KP, Sun SX, Li L, Yang HQ. Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. Genes Dev 2011, 25(10):1023-1028.
31. Liu B, Zuo Z, Liu H, Liu X, Lin C. Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev 2011, 25(10):1029-1034.
32. Zuo Z, Liu H, Liu B, Liu X, Lin C. Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr Biol 2011, 21(10):841-847.
33. Pacin M, Legris M, Casal JJ. Rapid decline in nuclear costitutive photomorphogenesis1 abundance anticipates the stabilization of its target elongated hypocotyl5 in the light. Plant Physiol 2014, 164(3):1134-1138.
34. Fittinghoff K, Laubinger S, Nixdorf M, Fackendahl P, Baumgardt RL, Batschauer A, Hoecker U. Functional and expression analysis of Arabidopsis SPA genes during seedling photomorphogenesis and adult growth. Plant J 2006, 47(4):577-590.
35. Tanaka N, Itoh H, Sentoku N, Kojima M, Sakakibara H, Izawa T, Itoh J, Nagato Y. The COP1 ortholog PPS regulates the juvenile-adult and vegetative-reproductive phase changes in rice. Plant Cell 2011, 23(6):2143-2154.
36. Sullivan JA, Gray JC. The pea light-independent photomorphogenesis1 mutant results from partial duplication of COP1 generating an internal promoter and producing two distinct transcripts. Plant Cell 2000, 12(10):1927-1938.
37. Weller JL, Hecht V, Vander Schoor JK, Davidson SE, Ross JJ. Light regulation of gibberellin biosynthesis in pea is mediated through the COP1/HY5 pathway. Plant Cell 2009, 21(3):800-813.
38. Marine JC. Spotlight on the role of COP1 in tumorigenesis. Nat Rev Cancer 2012, 12(7):455-464.
39. Lamparter T. Photomorphogenesis of mosses 2006, Dordrecht, The Netherlands: Springer, 3.
40. Wolf L, Rizzini L, Stracke R, Ulm R, Rensing SA. The molecular and physiological responses of Physcomitrella patens to ultraviolet-B radiation. Plant Physiol 2010, 153(3):1123-1134.
41. Richardt S, Lang D, Reski R, Frank W, Rensing SA. PlanTAPDB, a phylogeny-based resource of plant transcription-associated proteins. Plant Physiol 2007, 143(4):1452-1466.
42. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin-I T, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 2008, 319(5859):64-69.
43. International rice genome sequencing project The map-based sequence of the rice genome. Nature 2005, 436(7052):793-800. International rice genome sequencing project.
44. Possart A, Hiltbrunner A. An evolutionarily conserved signaling mechanism mediates far-red light responses in land plants. Plant Cell 2013, 25(1):102-114.
45. Chen YR, Su YS, Tu SL. Distinct phytochrome actions in nonvascular plants revealed by targeted inactivation of phytobilin biosynthesis. Proc Natl Acad Sci U S A 2012, 109(21):8310-8315.
46. Jaedicke K, Lichtenthaler AL, Meyberg R, Zeidler M, Hughes J. A phytochrome-phototropin light signaling complex at the plasma membrane. Proc Natl Acad Sci U S A 2012, 109(30):12231-12236.
47. Riese M, Zobell O, Saedler H, Huijser P. SBP-domain transcription factors as possible effectors of cryptochrome-mediated blue light signalling in the moss Physcomitrella patens. Planta 2008, 227(2):505-515.
48. Zimmer AD, Lang D, Buchta K, Rombauts S, Nishiyama T, Hasebe M, Van de Peer Y, Rensing SA, Reski R. Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions. BMC Genomics 2013, 14:498.
49. Gruber H, Heijde M, Heller W, Albert A, Seidlitz HK, Ulm R. Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. Proc Natl Acad Sci U S A 2010, 107(46):20132-20137.
50. Heijde M, Ulm R. Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state. Proc Natl Acad Sci U S A 2013, 110(3):1113-1118.
51. McNellis TW, Von Arnim AG, Araki T, Komeda Y, Miséra S, Deng X-W. Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell 1994, 6:487-500.
52. Ranjan A, Fiene G, Fackendahl P, Hoecker U. The Arabidopsis repressor of light signaling SPA1 acts in the phloem to regulate seedling de-etiolation, leaf expansion and flowering time. Development 2011, 138(9):1851-1862.
53. Yang J, Wang H. The central coiled-coil domain and carboxyl-terminal WD-repeat domain of Arabidopsis SPA1 are responsible for mediating repression of light signaling. Plant J 2006, 47(4):564-576.
54. Rensing SA. Gene duplication as a driver of plant morphogenetic evolution. Curr Opin Plant Biol 2014, 17C:43-48.
55. Hoecker U, Xu Y, Quail PH. SPA1: A new genetic locus involved in phytochrome A-specific signal transduction. Plant Cell 1998, 10:19-33.
56. Zobell O, Coupland G, Reiss B. The family of CONSTANS-like genes in Physcomitrella patens. Plant Biol (Stuttg) 2005, 7(3):266-275.
57. Shimizu M, Ichikawa K, Aoki S. Photoperiod-regulated expression of the PpCOL1 gene encoding a homolog of CO/COL proteins in the moss Physcomitrella patens. Biochem Bioph Res Co 2004, 324(4):1296-1301.
58. Yamawaki S, Yamashino T, Nakanishi H, Mizuno T. Functional characterization of HY5 homolog genes involved in early light-signaling in Physcomitrella patens. Biosci Biotechnol Biochem 2011, 75(8):1533-1539.
59. Lamesch P, Berardini TZ, Li DH, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 2012, 40(D1):D1202-D1210.
60. Kawahara Y, De La Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice (New York, NY) 2013, 6(1):4.
61. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinform 2009, 10:421.
62. Rost B. Twilight zone of protein sequence alignments. Protein Eng 1999, 12(2):85-94.
63. Lechner M, Findeiss S, Steiner L, Marz M, Stadler PF, Prohaska SJ. Proteinortho: Detection of (Co-)orthologs in large-scale analysis. Bmc Bioinform 2011, 12:124.
64. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S. InterProScan 5: genome-scale protein function classification. Bioinform 2014, 30:1236-1240.
65. Lupas A, Vandyke M, Stock J. PREDICTING COILED COILS FROM PROTEIN SEQUENCES. Science 1991, 252(5009):1162-1164.
66. Katoh K, Standley DM. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol Biol Evol 2013, 30(4):772-780.
67. Do CB, Mahabhashyam MSP, Brudno M, Batzoglou S. ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res 2005, 15(2):330-340.
68. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
69. Notredame C, Higgins DG, Heringa J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000, 302(1):205-217.
70. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinform 2009, 25(9):1189-1191.
71. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinform 2011, 27(8):1164-1165.
72. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinform 2003, 19(12):1572-1574.
73. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinform 2014, 30(9):1312-1313.
74. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 2007, 104(1):34-41.