Evolutionary Relationships Among Barley and Arabidopsis Core Circadian Clock and Clock-Associated Genes

Journal of Molecular Evolution

Volumn 80, Issue 2, 2015, Pages 108-119

  Calixto, Cristiane P G ^a   Waugh, Robbie ^a,b   Brown, John W S ^a,b  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Arabidopsis thaliana; Circadian clock; Homologue; Hordeum vulgare (barley); Reciprocal BLAST

Indexed keywords

ARABIDOPSIS; BRYOPSIDA; CIRCADIAN RHYTHM; GENETICS; HORDEUM; MOLECULAR EVOLUTION; PHYSIOLOGY; PLANT GENE; SOLANUM;

ARABIDOPSIS; BRYOPSIDA; CIRCADIAN CLOCKS; EVOLUTION, MOLECULAR; GENES, PLANT; HORDEUM; SOLANUM;

EID: 84925500275     PISSN: 00222844     EISSN: 14321432     Source Type: Journal    
DOI: 10.1007/s00239-015-9665-0     Document Type: Article

References (93)

1. Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
3. Boxall SF, Foster JM, Bohnert HJ, Cushman JC, Nimmo HG, Hartwell J (2005) Conservation and divergence of circadian clock operation in a stress-inducible Crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiol 137:969–982
4. Campoli C, Drosse B, Searle I, Coupland G, von Korff M (2012a) Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J 69:868–880
5. Campoli C, Shtaya M, Davis SJ, von Korff M (2012b) Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs. BMC Plant Biol 12:97
6. Campoli C, Pankin A, Drosse B, Casao CM, Davis SJ, von Korff M (2013) HvLUX1 is a candidate gene underlying the early maturity 10 locus in barley: phylogeny, diversity, and interactions with the circadian clock and photoperiodic pathways. New Phytol 199:1045–1059
7. Chaw SM, Chang CC, Chen HL, Li WH (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58:424–441
8. Chen Z, McKnight SL (2007) A conserved DNA damage response pathway responsible for coupling the cell division cycle to the circadian and metabolic cycles. Cell Cycle 6:2906–2912
9. Chow BY, Helfer A, Nusinow DA, Kay SA (2012) ELF3 recruitment to the PRR9 promoter requires other evening complex members in the Arabidopsis circadian clock. Plant Signal Behav 7:170–173
10. Cockram J, Thiel T, Steuernagel B, Stein N, Taudien S, Bailey PC, O’Sullivan DM (2012) Genome dynamics explain the evolution of flowering time CCT domain gene families in the Poaceae. PLoS One 7:e45307
11. Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:R130
12. Dodd AN et al (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633
13. Dunford RP, Griffiths S, Christodoulou V, Laurie DA (2005) Characterisation of a barley (Hordeum vulgare L.) homologue of the Arabidopsis flowering time regulator GIGANTEA. Theor Appl Genet 110:925–931
14. Endo M, Shimizu H, Nohales MA, Araki T, Kay SA (2014) Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515:419–422
15. Faure S, Higgins J, Turner A, Laurie DA (2007) The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 176:599–609
16. Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, Laurie DA (2012) Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proc Natl Acad Sci USA 109:8328–8333
17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
18. Fowler DB, Breton G, Limin AE, Mahfoozi S, Sarhan F (2001) Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley. Plant Physiol 127:1676–1681
19. Gallego M, Virshup DM (2007) Post-translational modifications regulate the ticking of the circadian clock. Nat Rev Mol Cell Biol 8:139–148
20. Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, Kay SA (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc Natl Acad Sci USA 109:3167–3172
21. Green RM, Tingay S, Wang ZY, Tobin EM (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129:576–584
22. Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 131:1855–1867
23. Harmer SL (2010) Plant biology in the fourth dimension. Plant Physiol 154:467–470
24. Harmer SL et al (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113
25. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722
26. Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AA (2013) Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502:689–692
27. Helfer A, Nusinow DA, Chow BY, Gehrke AR, Bulyk ML, Kay SA (2011) LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol 21:126–133
28. Higgins JA, Bailey PC, Laurie DA (2010) Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS One 5:e10065
29. Holm K, Källman T, Gyllenstrand N, Hedman H, Lagercrantz U (2010) Does the core circadian clock in the moss Physcomitrella patens (Bryophyta) comprise a single loop? BMC Plant Biol 10:109
30. Hotta CT et al (2007) Modulation of environmental responses of plants by circadian clocks. Plant Cell Environ 30:333–349
31. Huang W, Pérez-García P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336:75–79
32. Iwamoto M, Higo K, Takano M (2009) Circadian clock- and phytochrome-regulated Dof-like gene, Rdd1, is associated with grain size in rice. Plant Cell Environ 32:592–603
33. James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, Jenkins GI, Nimmo HG (2008) The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322:1832–1835
34. James AB et al (2012) Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24:961–981
35. Kim W-Y et al (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449:356–360
36. Klintenäs M, Pin PA, Benlloch R, Ingvarsson PK, Nilsson O (2012) Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytol 196:1260–1273
37. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962
38. Kolmos E et al (2009) Integrating ELF4 into the circadian system through combined structural and functional studies. HFSP Journal 3:350–366
39. Larkin MA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
40. Li C, Dubcovsky J (2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J 55:543–554
41. Lillo C (2006) Circadian rhythmicity of nitrate reductase activity in barley leaves. Physiol Plant 61:219–223
42. Locke JC et al (2006) Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol Syst Biol 2:59
43. Lou P, Wu J, Cheng F, Cressman LG, Wang X, McClung CR (2012) Preferential retention of circadian clock genes during diploidization following whole genome triplication in Brassica rapa. Plant Cell 24:2415–2426
44. Martínez M, Rubio-Somoza I, Carbonero P, Díaz I (2003) A cathepsin B-like cysteine protease gene from Hordeum vulgare (gene CatB) induced by GA in aleurone cells is under circadian control in leaves. J Exp Bot 54:951–959
45. Matos DA, Cole BJ, Whitney IP, MacKinnon KJ-M, Kay SA, Hazen SP (2014) Daily changes in temperature, not the circadian clock, regulate growth rate in Brachypodium distachyon. PLoS One 9:e100072
46. Matsumoto T et al (2011) Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol 156:20–28
47. Mayer KF et al (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716
48. McClung CR (2010) A modern circadian clock in the common angiosperm ancestor of monocots and eudicots. BMC Biol 8:55
49. McClung CR (2014) Wheels within wheels: new transcriptional feedback loops in the Arabidopsis circadian clock. F1000Prime Reports 6:2
50. Michael TP et al (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049–1053
51. Miller TA, Muslin EH, Dorweiler JE (2008) A maize CONSTANS-like gene, conz1, exhibits distinct diurnal expression patterns in varied photoperiods. Planta 227:1377–1388
52. Moore MJ, Bell CD, Soltis PS, Soltis DE (2007) Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci USA 104:19363–19368
53. Murakami M, Tago Y, Yamashino T, Mizuno T (2007) Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48:110–121
54. Nagasaka S, Takahashi M, Nakanishi-Itai R, Bashir K, Nakanishi H, Mori S, Nishizawa NK (2009) Time course analysis of gene expression over 24 hours in Fe-deficient barley roots. Plant Mol Biol 69:621–631
55. Nagel DH, Kay SA (2012) Complexity in the wiring and regulation of plant circadian networks. Curr Biol 22:R648–R657
56. Nakamichi N (2011) Molecular mechanisms underlying the Arabidopsis circadian clock. Plant Cell Physiol 52:1709–1718
57. Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22:594–605
58. Nitcher R, Distelfeld A, Tan C, Yan L, Dubcovsky J (2013) Increased copy number at the HvFT1 locus is associated with accelerated flowering time in barley. Mol Genet Genomics 288:261–275
59. Ogiso E, Takahashi Y, Sasaki T, Yano M, Izawa T (2010) The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiol 152:808–820
60. Okamura H (2004) Clock genes in cell clocks: roles, actions, and mysteries. J Biol Rhythms 19:388–399
61. Onai K, Ishiura M (2005) PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock. Genes Cells 10:963–972
62. Para A, Farré EM, Imaizumi T, Pruneda-Paz JL, Harmon FG, Kay SA (2007) PRR3 is a vascular regulator of TOC1 stability in the Arabidopsis circadian clock. Plant Cell 19:3462–3473
63. Paterson AH, Freeling M, Tang H, Wang X (2010) Insights from the comparison of plant genome sequences. Annu Rev Plant Biol 61:349–372
64. Pin PA, Nilsson O (2012) The multifaceted roles of FLOWERING LOCUS T in plant development. Plant, Cell Environ 35:1742–1755
65. Poiré R, Wiese-Klinkenberg A, Parent B, Mielewczik M, Schurr U, Tardieu F, Walter A (2010) Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects. J Exp Bot 61:1751–1759
66. Pokhilko A et al (2010) Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model. Mol Syst Biol 6:416
67. Pokhilko A, Fernández AP, Edwards KD, Southern MM, Halliday KJ, Millar AJ (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 8:574
68. Prosdocimi F, Chisham B, Pontelli E, Thompson JD, Stoltzfus A (2009) Initial implementation of a comparative data analysis ontology. Evol Bioinform Online 5:47–66
69. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
70. Sanchez SE et al (2010) A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 468:112–116
71. Satbhai SB et al (2010) Pseudo-response regulator (PRR) homologues of the moss Physcomitrella patens: insights into the evolution of the PRR family in land plants. DNA Res 18:39–52
72. Schnable JC, Wang X, Pires JC, Freeling M (2012) Escape from preferential retention following repeated whole genome duplications in plants. Front Plant Sci 3:94
73. Serikawa M, Miwa K, Kondo T, Oyama T (2008) Functional conservation of clock-related genes in flowering plants: overexpression and RNA interference analyses of the circadian rhythm in the monocotyledon Lemna gibba. Plant Physiol 146:1952–1963
74. Shin BS, Lee JH, Lee JH, Jeong HJ, Yun CH, Kim JK (2004) Circadian regulation of rice (Oryza sativa L.) CONSTANS-like gene transcripts. Mol Cells 17:10–16
75. Song HR, Ito S, Imaizumi T (2010) Similarities in the circadian clock and photoperiodism in plants. Curr Opin Plant Biol 13:594–603
76. Stracke S, Haseneyer G, Veyrieras JB, Geiger HH, Sauer S, Graner A, Piepho HP (2009) Association mapping reveals gene action and interactions in the determination of flowering time in barley. Theor Appl Genet 118:259–273
77. Suetsugu N, Wada M (2013) Evolution of three LOV blue light receptor families in green plants and photosynthetic stramenopiles: phototropin, ZTL/FKF1/LKP2 and aureochrome. Plant Cell Physiol 54:8–23
78. Takata N, Saito S, Saito CT, Nanjo T, Shinohara K, Uemura M (2009) Molecular phylogeny and expression of poplar circadian clock genes, LHY1 and LHY2. New Phytol 181:808–819
79. Takata N, Saito S, Saito CT, Uemura M (2010) Phylogenetic footprint of the plant clock system in angiosperms: evolutionary processes of pseudo-response regulators. BMC Evol Biol 10:126
80. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035
81. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
82. Tauber E, Last KS, Olive PJW, Kyriacou CP (2004) Clock gene evolution and functional divergence. J Biol Rhythms 19:445–458
83. Troein C, Locke JC, Turner MS, Millar AJ (2009) Weather and seasons together demand complex biological clocks. Curr Biol 19:1961–1964
84. Turner A, Beales J, Faure S, Dunford RP, Laurie D (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034
85. Vallelian-Bindschedler L, Mösinger E, Métraux JP, Schweizer P (1998) Structure, expression and localization of a germin-like protein in barley (Hordeum vulgare L.) that is insolubilized in stressed leaves. Plant Mol Biol 37:297–308
86. Valverde F (2011) CONSTANS and the evolutionary origin of photoperiodic timing of flowering. J Exp Bot 62:2453–2463
87. Wang X et al (2011) Robust expression and association of ZmCCA1 with circadian rhythms in maize. Plant Cell Rep 30:1261–1272
88. Yon F, Seo PJ, Ryu JY, Park CM, Baldwin IT, Kim SG (2012) Identification and characterization of circadian clock genes in a native tobacco, Nicotiana attenuata. BMC Plant Biol 12:172
89. Yu B, Hinchcliffe M (2011) In silico tools for gene discovery. Methods in molecular biology, vol 760, 11th edn. Humana Press, New York. doi:10.1007/978-1-61779-176-5_2
90. Yu JW et al (2008) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell 32:617–630
91. Zakhrabekova S et al (2012) Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley. Proc Natl Acad Sci USA 109:4326–4331. doi:10.1073/pnas.1113009109
92. Zeilinger MN, Farré EM, Taylor SR, Kay SA, Doyle Jr F (2006) A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Mol Syst Biol 2:58
93. Zimmer A, Lang D, Richardt S, Frank W, Reski R, Rensing SA (2007) Dating the early evolution of plants: detection and molecular clock analyses of orthologs. Mol Genet Genomics 278:393–402