Genomewide characterization of the light-responsive and clock-controlled output pathways in Lotus japonicus with special emphasis of its uniqueness

Plant and Cell Physiology

Volumn 51, Issue 10, 2010, Pages 1800-1814

  Ono, Natsuko ^a   Ishida, Kai ^a   Yamashino, Takafumi ^a   Nakanishi, Hanayo ^a   Sato, Shusei ^b   Tabata, Satoshi ^b   Mizuno, Takeshi ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

Circadian clock; Flowering pathway; Light signaling; Lotus japonicus; Photomorphogenesis

Indexed keywords

ARABIDOPSIS; ARTICLE; CIRCADIAN RHYTHM; FLOWER; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; LOTUS; METABOLISM; PHOTOPERIODICITY; PLANT GENOME; RADIATION EXPOSURE; TRANSGENIC PLANT;

ARABIDOPSIS; CIRCADIAN CLOCKS; DATABASES, GENETIC; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; LIGHT; LOTUS; PHOTOPERIOD; PLANTS, GENETICALLY MODIFIED;

ARABIDOPSIS; ARABIDOPSIS THALIANA; LOTUS CORNICULATUS VAR. JAPONICUS;

EID: 77957957377     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcq140     Document Type: Article

References (100)

1. Achard, P., Renou, J.P., Berthome, R., Harberd, N.P. and Genschik, P. (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr. Biol. 6: 656-660.
2. Aguilar-Martínez, J.A., Poza-Carrión,C.and Cubas,P.(2007)Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19: 458-472.
3. Alabadí, D. and Blázquez, M.A. (2009) Molecular interactions between light and hormone signaling to control plant growth. Plant Mol. Biol. 69: 407-417.
4. Alabadí, D., Gallego-Bartolomé, J., Orlando, L., García-Cárcel, L., Rubio, V., Martínez, C., et al. (2008) Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J. 53: 324-335.
5. Alabadí, D., Oyama, T., Yanovsky, M.J., Harmon, F.G., Más, P. and Kay, S.A. (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293: 880-883.
6. Becker, A. and Theissen, G. (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29: 464-489.
7. Beveridge, C.A. and Kyozuka, J. (2010) New genes in the strigolactone-related shoot branching pathway. Curr. Opin. Plant Biol. 13: 34-39.
8. Breton, G. and Kay, S.A. (2007) Plant biology: time for growth. Nature 448: 265-266.
9. Castillon, A., Shen, H. and Huq, E. (2007) Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks. Trends Plant Sci. 12: 514-521.
10. Corbesier, L. and Coupland, G. (2006) The quest for florigen: a review of recent progress. J. Exp. Bot. 57: 3395-3403.
11. Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033.
12. Davière J.M., de Lucas, M. and Prat, S. (2008) Transcriptional factor interaction: a central step in DELLA function. Curr. Opin. Genet. Dev. 18: 295-303.
13. de Lucas, M., Davière, J.M., Rodríguez-Falcón, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., et al. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484.
14. de Montaigu, A., Tóth, R., and Coupland, G. (2010) Plant development goes like clockwork. Trends Genet. 26: 296-306.
15. Djakovic-Petrovic, T., de Wit, M., Voesenek, L.A. and Pierik, R. (2007) DELLA protein function in growth responses to canopy signals. Plant J. 51: 117-126.
16. Doebley, J., Stec A. and Hubbard L. (1997) The evolution of apical dominance in maize. Nature 386: 485-488.
17. Duek, P.D. and Fankhauser, C. (2005) bHLH class transcription factors take centre stage in phytochrome signalling. Trends Plant Sci. 1 0 : 51-54.
18. Feng, S., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J., Wang, F., et al. (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479.
19. Feng, X., Zhao, Z., Tian, Z., Xu, S., Luo, Y., Cai, Z., et al. (2006) Control of petal shape and floral zygomorphy in Lotus japonicus. Proc. Natl. Acad. Sci. USA 103: 4970-4975.
20. Finlayson, S.A., Krishnareddy, S.R., Kebrom, T.H. and Casal, J.J. (2010) Phytochrome regulation of branching in Arabidopsis. Plant Physiol. 152: 1914-1927.
21. Fornara, F., de Montaigu, A. and Coupland, G. (2010) SnapShot: control of flowering in Arabidopsis. Cell 141: 550.e1-2.
22. Fornara, F., Panigrahi, K.C., Gissot, L., Sauerbrunn, N., Rühl, M., Jarillo, J.A. et al. (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev. Cell 17: 75-86.
23. Frannklin, K.A. (2008) Shade avoidance. New Physiol. 179: 930-944.
24. Fujimori, T., Yamashino, T., Kato, T. and Mizuno, T. (2004) Circadian-controlled basic/helix-loop-helix factor, PIL6, implicated in light-signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 4 5 : 1078-1086.
25. Fujiwara, S., Oda, A., Yoshida, R., Niinuma, K., Miyata, K., Tomozoe, Y., et al. (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell 20: 2960-2971.
26. Gardner, M.J., Hubbard, K.E., Hotta, C.T., Dodd, A.N. and Webb, A.A. (2006) How plants tell the time. Biochem. J. 397: 15-24.
27. Guo, Z., Fujioka, S., Blancaflor, E.B., Miao, S., Gou, X. and Li, J. (2010) TCP1 modulates brassinosteroid biosynthesis by regulating the expression of the key biosynthetic gene DWARF4 in Arabidopsis thaliana. Plant Cell 22: 1161-1173.
28. Hecht, V., Foucher, F., Ferrándiz, C., Macknight, R., Navarro, C., Morin, J., et al. (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol. 137 : 1420-1434.
29. Hornitschek, P., Lorrain, S., Zoete, V., Michielin, O. and Fankhauser, C. (2009) Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J. 28: 3893-3902.
30. Hotta, C.T., Gardner, M.J., Hubbard, K.E., Baek, S.J., Dalchau, N, Suhita, D., et al. (2007) Modulation of environmental responses of plants by circadian clocks. Plant Cell Environ. 30: 333-349.
31. Huq, E. and Quail, P.H. (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 21: 2441-2450.
32. Huq, E., Tepperman, J.M. and Quail, P.H. (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 97: 9789-9794.
33. Imaizumi, T. (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr. Opin. Plant Biol. 13: 83-89.
34. Imaizumi, T. and Kay, S.A. (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci. 11: 550-558.
35. Imaizumi, T., Schultz, T.F., Harmon, F.G., Ho, L.A. and Kay, S.A. (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309: 293-297.
36. Imaizumi, T., Tran, H.G., Swartz, T.E., Briggs, W.R. and Kay, S.A. (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426: 302-306.
37. Itoh, H., Nonoue, Y., Yano, M. and Izawa, T. (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat. Genet. 42: 635-638.
38. Ishida, K., Niwa, Y., Yamashino, T. and Mizuno, T. (2009) A genome-wide compilation of the two-component systems in Lotus japonicus. DNA Res. 16: 237-247.
39. Jack, T. (2001) Plant development going MADS. Plant Mol. Biol. 4 6 : 515-520.
40. Jarillo, J.A., Piñeiro, M., Cubas, P. and Martínez-Zapater, J.M. (2009) Chromatin remodeling in plant development. Int. J. Dev. Biol. 5 3 : 581-596.
41. Jung, J.H., Seo, Y.H., Seo, P.J., Reyes, J.L., Yun, J., Chua, N.H. et al. (2007) The GIGANTEA-regulated MicroRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 1 9 : 2736-2748.
42. Khanna, R., Huq, E., Kikis, E.A., Al-Sady, B., Lanzatella, C. and Quail, P.H. (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.
43. Khanna, R., Kronmiller, B., Maszle, D.R., Coupland, G., Holm, M., Mizuno, T. et al. (2009) The Arabidopsis B-box zinc fi nger family. Plant Cell 21: 3416-3420.
44. Kim, W.Y., Fujiwara, S., Suh, S.S., Kim, J., Kim, Y., Han, L., et al. (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449: 356-360.
45. Kim, D.H., Doyle, M.R., Sung, S. and Amasino, R.M. (2009) Vernalization: winter and the timing of flowering in plants. Annu. Rev. Cell Dev. Biol. 25: 277-299.
46. Kobayashi, Y. and Weigel, D. (2007) Move on up, it's time for change\-mobile signals controlling photoperiod-dependent flowering. Genes Dev. 21: 2371-2384.
47. Kojima, S., Banno, H., Yoshioka, Y., Oka, A., Machida, C. and Machida, Y. (1999) A binary vector plasmid for gene expression in plant cells that is stably maintained in Agrobacterium cells. DNA Res. 6 : 407-410.
48. Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T., et al. (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43: 1096-1105.
49. Kumagai, T., Ito, S., Nakamichi, N., Niwa, Y., Murakami, M., Yamashino, T. et al. (2008) The common function of a novel subfamily of B-box zinc fi nger proteins with reference to circadian-associated events in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 72: 1539-1545.
50. Ledger, S., Strayer, C., Ashton, F., Kay, S.A. and Putterill J. (2001) Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J. 26: 15-22.
51. Leivar, P., Tepperman, J.M., Monte, E., Calderon, R.H., Liu, T.L. and Quail, P.H. (2009) Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 2 1 : 3535-3553.
52. Liew, L.C., Hecht, V., Laurie, R.E., Knowles, C.L., Vander-Schoor, J.K., Macknight, R.C., et al. (2009) DIE NEUTRALIS and LATE BLOOMER 1 contribute to regulation of the pea circadian clock. Plant Cell 2 1 : 3198-3211.
53. Lin, C. and Shalitin, D. (2003) Cryptochrome structure and signal transduction. Annu. Rev. Plant Biol. 54: 469-496.
54. Liu, C., Thong,Z.and Yu,H.(2009) Coming into bloom: the specification of floral meristems. Development 136: 3379-3391.
55. Locke, J.C., Kozma-Bognár, L., Gould, P.D., Fehér, B., Kevei, E., Nagy, F., et al. (2006) Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol. Syst. Biol. 2: 59.
56. Lorrain, S., Allen, T., Duek, P.D., Whitelam, G.C. and Fankhauser, C. (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 53: 312-323.
57. Luo, D., Carpenter, R., Copsey, L., Vincent, C., Clark, J. and Coen, E. (1999) Control of organ asymmetry in flowers of Antirrhinum. Cell 99: 367-376.
58. Makino, S., Kiba, T., Imamura, A., Hanaki, N., Nakamura, A., Suzuki, T., et al. (2000) Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol. 41: 791-803.
59. Martín-Trillo, M. and Cubas, P. (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci. 5: 31-39.
60. Matsushika, A., Makino, S., Kojima, M. and Mizuno, T. (2000) 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. 41: 1002-1012.
61. McClung, C.R. (2006) Plant circadian rhythms. Plant Cell 18: 792-803.
62. McClung, C.R. (2008) Comes a time. Curr. Opin. Plant Biol. 1 1 : 514-520.
63. McClung, C.R. (2010) A modern circadian clock in the common angiosperm ancestor of monocots and eudicots. BMC Biol. 8: 55.
64. Mizoguchi, T., Wheatley, K., Hanzawa, Y., Wright, L., Mizoguchi, M., Song, H.R., et al. (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev. Cell 5 : 629-641.
65. Mizoguchi, T., Wright, L., Fujiwara, S., Cremer, F., Lee, K., Onouchi, H., et al. (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 1 7 : 2255-2270.
66. Mizuno, T. (1998) His-Asp phosphotransfer signal transduction. J. Biochem. (Tokyo) 123: 555-563.
67. Mizuno, T. (2004) Plant response regulators implicated in signal trans-duction and circadian rhythm. Curr. Opin. Plant Biol. 7: 499-505.
68. Mizuno, T. (2005) Two-component phosphorelay signal transduction systems in plants: from hormone responses to circadian rhythms. Biosci. Biotechnol. Biochem. 69: 2263-2276.
69. Mizuno, T. and Nakamichi, N. (2005) Pseudo-response regulators (PRRs) or true oscillator components (TOCs). Plant Cell Physiol. 4 6 :677-685.
70. Monte, E., Al-Sady, B., Leivar, P. and Quail, P.H. (2007) Out of the dark: how the PIFs are unmasking a dual temporal mechanism of phytochrome signalling. J. Exp. Bot. 58: 3125-3133.
71. Nakamichi, N., Kita, M., Niinuma, K., Ito, S., Yamashino, T., Mizoguchi, T. et al. (2007) Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol. 48: 822-832.
72. Nemhauser, J.L. (2008) Dawning of a new era: photomorphogenesis as an integrated molecular network. Curr. Opin. Plant Biol. 11: 4-8.
73. Nishimura, R., Ohmori, M., Fujita, H. and Kawaguchi, M. (2002) A Lotus basic leucine zipper protein with a RING-fi nger motif negatively regulates the developmental program of nodulation. Proc. Natl. Acad. Sci. USA 99: 15206-15210.
74. Niwa, Y., Ito, S., Nakamichi, N., Mizoguchi, T., Niinuma, K., Yamashino, T., et al. (2007) Genetic linkages of the circadian clock-associated genes, TOC1, CCA1 and LHY, in the photoperiodic control of flowering time in Arabidopsis thaliana. Plant Cell Physiol. 48 : 925-937.
75. Niwa, Y., Yamashino, T. and Mizuno, T. (2009) Circadian clock regulates photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant Cell Physiol. 50: 838-854.
76. Nozue, K. and Maloof, J.N. (2006) Diurnal regulation of plant growth. Plant Cell Environ. 29: 396-408.
77. Nozue, K., Covington, M.F., Duek, P.D., Lorrain, S., Fankhauser, C., Harmer, S.L. et al. (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448: 358-361.
78. Putterill, J., Robson, F., Lee, K., Simon, R. and Coupland, G. (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc fi nger transcription factors. Cell 80: 847-857.
79. Quail, P.H. (2002) Photosensory perception and signalling in plant cells: new paradigms? Curr. Opin. Cell Biol. 14: 180-188.
80. Robles, P. and Pelaz, S. (2005) Flower and fruit development in Arabidopsis thaliana. Int. J. Dev. Biol. 49: 633-643.
81. Salazar, J.D., Saithong, T., Brown, P.E., Foreman, J., Locke, J.C., Halliday, K.J., et al. (2009) Prediction of photoperiodic regulators from quantitative gene circuit models. Cell 139: 1170-1179.
82. Sato, S., Isobe, S. and Tabata, S. (2010) Structural analyses of the genomes in legumes. Curr. Opin. Plant Biol. 13: 146-152.
83. Sato, S., Nakamura, Y., Kaneko, T., Asamizu, E., Kato, T., Nakao, M., et al. (2008) Genome structure of the legume, Lotus japonicus. DNA Res. 15: 227-239.
84. Sato, S. and Tabata, S. (2005) Lotus japonicus as a platform for legume research. Curr. Opin. Plant Biol. 9: 128-132.
85. Sawa, M., Nusinow, D.A., Kay, S.A. and Imaizumi, T. (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318: 261-265.
86. Schaffer, R., Ramsay, N., Samach, A., Corden, S., Putterill, J., Carré, I.A., et al. (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93: 1219-1229.
87. Strayer, C., Oyama, T., Schultz, T.F., Raman, R., Somers, D.E., Más, P., et al. (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289: 768-771.
88. Szczyglowski, K. and Stougaard, J. (2008) Lotus genome: pod of gold for legume research. Trends Plant Sci. 13: 515-517.
89. Takada, S. and Goto, K. (2003) TERMINAL FLOWER2, an Arabidopsis homolog of HETEROCHROMATIN PROTEIN1, counteracts the activation of FLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time. Plant Cell 1 5 : 2856-2865.
90. Thakare, D., Kumudini, S. and Dinkins, R.D. (2010) Expression of flowering-time genes in soybean E1 near-isogenic lines under short and long day conditions. Planta 231: 951-963.
91. Town, C.D. (2006) Annotating the genome of Medicago truncatula. Curr. Opin. Plant Biol. 9: 122-127.
92. Vandenbussche, F., Verbelen, J.P. and Van Der Straeten, D. (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. Bioessays 27: 275-284.
93. Waldie, T., Hayward, A. and Beveridge, C.A. (2010) Axillary bud outgrowth in herbaceous shoots: how do strigolactones fi t into the picture? Plant Mol. Biol. 73: 27-36.
94. Wang, Z.Y. and Tobin, E.M. (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93: 1207-1217.
95. Weller, J.L., Hecht, V., Liew, L.C., Sussmilch, F.C., Wenden, B., Knowles, C.L., et al. (2009) Update on the genetic control of flowering in garden pea. J. Exp. Bot. 60: 2493-2499.
96. Weller, J.L., Hecht, V., Vander-Schoor, J.K., Davidson, S.E. and Ross, J.J. (2009) Light regulation of gibberellin biosynthesis in pea is mediated through the COP1/HY5 pathway. Plant Cell 21: 800-813.
97. Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M. and Araki, T. (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol. 46: 1175-1189.
98. Yamashino, T., Matsushika, A., Fujimori, T., Sato, S., Kato, T., Tabata, S., et al. (2003) A link between circadian-controlled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 44: 619-629.
99. Yanovsky, M.J. and Kay, S.A. (2003) Living by the calendar: how plants know when to flower. Nat. Rev. Mol. Cell Biol. 4: 265-275.
100. Zeilinger, M.N., Farré, E.M., Taylor, S.R., Kay, S.A. and Doyle, F.J. III (2006) A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Mol. Syst. Biol. 2 : 58-64.