The cyclophilin ROC1 links phytochrome and cryptochrome to brassinosteroid sensitivity

Plant Journal

Volumn 71, Issue 5, 2012, Pages 712-723

  Trupkin, Santiago A ^a   Mora García, Santiago ^b   Casal, Jorge J ^a,b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

Arabidopsis; brassinosteroid; cryptochrome; phytochrome; ROTAMASE CYCLOPHILIN 1

Indexed keywords

ARABIDOPSIS; BRASSINOSTEROIDS; CRYPTOCHROMES; CYCLOPHILIN; PHYTOCHROME;

PHOSPHORYLATION; PLANTS (BOTANY); TRANSCRIPTION FACTORS;

GENES;

ARABIDOPSIS PROTEIN; BES1 PROTEIN, ARABIDOPSIS; BRASSINOSTEROID; CRY1 PROTEIN, ARABIDOPSIS; CRYPTOCHROME; CYCLOPHILIN; NUCLEAR PROTEIN; PHYTOCHROME A; ROC1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; GENETICS; LIGHT; METABOLISM; MUTATION; PHENOTYPE; PHOSPHORYLATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; CRYPTOCHROMES; CYCLOPHILINS; LIGHT; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHORYLATION; PHYTOCHROME A;

ARABIDOPSIS;

EID: 84865497025     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05013.x     Document Type: Article

References (77)

1. Ahmad, M., and, Cashmore, A.R., (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature, 366, 162-166.
2. Arnold, H.K., Zhang, X., Daniel, C.J., Tibbitts, D., Escamilla-Powers, J., Farrell, A., Tokarz, S., Morgan, C., and, Sears, R.C., (2009) The Axin1 scaffold protein promotes formation of a degradation complex for c-Myc. EMBO J. 28, 500-512.
3. Asami, T., Min, Y.K., Nagata, N., Yamagishi, K., Takatsuto, S., Fujioka, S., Murofushi, N., Yamaguchi, I., and, Yoshida, S., (2000) Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor. Plant Physiol. 123, 93-100.
4. Bancos, S., Szatmari, A.-M., Castle, J., Kozma-Bognar, L., Shibata, K., Yokota, T., Bishop, G.J., Nagy, F., and, Szekeres, M., (2006) Diurnal regulation of the brassinosteroid-biosynthetic CPD gene in Arabidopsis. Plant Physiol. 141, 299-309.
5. Barnes, S.A., Nishizawa, N.K., Quaggio, R.B., Whitelam, G.C., and, Chua, N.-H., (1996) Far-red light blocks greening of Arabidopsis seedlings via a phytochrome A-mediated change in plastid development. Plant Cell, 8, 601-615.
6. Casal, J.J., and, Mazzella, M.A., (1998) Conditional synergism between cryptochrome 1 and phytochrome B is shown by the analysis of phyA, phyB, and hy4 single, double, and triple mutants in Arabidopsis. Plant Physiol. 118, 9-25.
7. Cashmore, A.R., Jarillo, J.A., Wu, Y.J., and, Liu, D., (1999) Cryptochromes: blue light receptors for plants and animals. Science, 284, 760-765.
8. Chen, M., Chory, J., and, Fankhauser, C., (2004) Light signal transduction in higher plants. Annu. Rev. Genet. 38, 87-117.
9. Chou, I.T., and, Gasser, C.S., (1997) Characterization of the cyclophilin gene family of Arabidopsis thaliana and phylogenetic analysis of known cyclophilin proteins. Plant Mol. Biol. 35, 873-892.
10. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
11. Clouse, S.D., (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell, 23, 1219-1230.
12. Coaker, G., Falick, A., and, Staskawicz, B., (2005) Activation of a phytopathogeneic bacterial effector protein by a eukaryotic cyclophilin. Science, 308, 506-508.
13. Coaker, G., Zhu, G., Ding, Z., Van Doren, S.R., and, Staskawicz, B., (2006) Eukaryotic cyclophilin as a molecular switch for effector activation. Mol. Microbiol. 61, 1485-1496.
14. Coenen, C., and, Lomax, T.L., (1998) The DIAGEOTROPICA gene differentially affects auxin and cytokinin responses throughout development in tomato (Lycopersicon esculentum Mill.). Plant Physiol. 117, 63-72.
15. Daniel, S.G., Rayle, D.L., and, Cleland, R.E., (1989) Auxin physiology of the tomato mutant diageotropica. Plant Physiol. 91, 804-807.
16. Duek, P.D., and, Fankhauser, C., (2003) HFR1, a putative bHLH transcription factor, mediates both phytochrome A and cryptochrome signaling. Plant J. 34, 827-836.
17. Goda, H., Shimada, Y., Asami, T., Fujioka, S., and, Yoshida, S., (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 130, 1319-1334.
18. 2+-binding protein involved in cryptochrome and phytochrome coaction. Science, 291, 487-490.
19. Hansen, H., and, Grossmann, K., (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol. 124, 1437-1448.
20. He, J.-X., Gendron, J.M., Yang, Y., Li, J., and, Wang, Z.Y., (2002) The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl Acad. Sci. USA, 99, 10185-10190.
21. Hoecker, U., Tepperman, J.M., and, Quail, P.H., (1999) SPA1, a WD-repeat protein specific to phytochrome A signal transduction. Science, 284, 496-499.
22. Hyun, Y., and, Lee, I., (2006) KIDARI, encoding a non-DNA binding bHLH protein, represses light signal transduction in Arabidopsis thaliana. Plant Mol. Biol. 61, 283-296.
23. Jiao, Y., Ma, L., Strickland, E., and, Deng, X.W., (2005) Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell, 17, 3239-3256.
24. Jiao, Y., Lau, O.S., and, Deng, X.W., (2007) Light-regulated transcriptional networks in higher plants. Nat. Rev. Genet. 8, 217-230.
25. Karimi, M., Inzé, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195.
26. Koncz, C., and, Schell, J., (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel Agrobacterium binary vector. Mol. Gen. Genet. 204, 383-396.
27. LeClere, S., and, Bartel, B., (2001) A library of Arabidopsis 35S-cDNA lines for identifying novel mutants. Plant Mol. Biol. 46, 695-703.
28. Li, J., (2010) Regulation of the nuclear activities of brassinosteroid signaling. Curr. Opin. Plant Biol. 13, 540-547.
29. Li, J., and, Nam, K.H., (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science, 295, 1299-1301.
30. Li, J.M., Nagpal, P., Vitart, V., McMorris, T.C., and, Chory, J., (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science, 272, 398-401.
31. Lian, H.-L., He, S.-B., Zhang, Y.-C., Zhu, D.-M., Zhang, J.-Y., Jia, K.-P., Sun, S.-X., Li, L., and, Yang, H.-Q., (2011) Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. Genes Dev. 25, 1023-1028.
32. Lin, C.T., Yang, H.Y., Guo, H.W., Mockler, T., Chen, J., and, Cashmore, A.R., (1998) Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc. Natl Acad. Sci. USA, 95, 2686-2690.
33. Liu, Y., Mitsukawa, N., Oosumi, T., and, Whittier, R.F., (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457-463.
34. Liu, B., Zuo, Z., Liu, H., Liu, X., and, Lin, C., (2011) Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev. 25, 1029-1034.
35. Luccioni, L.G., Oliverio, K.A., Yanovsky, M.J., Boccalandro, H.E., and, Casal, J.J., (2002) Brassinosteroid mutants uncover fine tuning of phytochrome signaling. Plant Physiol. 128, 173-181.
36. Luo, X.-M., Lin, W.-H., Zhu, S., et al. (2010) Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev. Cell, 19, 872-883.
37. Ma, L., Li, J., Qu, L., Hager, J., Chen, Z., Zhao, H., and, Deng, X.W., (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell, 13, 2589-2607.
38. Mallappa, C., Yadav, V., Negi, P., and, Chattopadhyay, S., (2006) A basic leucine zipper transcription factor, G-box-binding factor 1, regulates blue light-mediated photomorphogenic growth in Arabidopsis. J. Biol. Chem. 281, 22190-22199.
39. Mancinelli, A.L., Rossi, F., and, Moroni, A., (1991) Cryptochrome, phytochrome and anthocyanin production. Plant Physiol. 96, 1079-1085.
40. Mockler, T.C., Guo, H., Yang, H., Duong, H., and, Lin, C., (1999) Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development, 126, 2073-2082.
41. Moran, R., (1982) Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide. Plant Physiol. 69, 1376-1381.
42. Muday, G.K., Lomax, T.L., and, Rayle, D.L., (1995) Characterization of the growth and auxin physiology of roots of the tomato mutant diageotropica. Planta, 195, 548-553.
43. Nagatani, A., Reed, J.W., and, Chory, J., (1993) Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A. Plant Physiol. 102, 269-277.
44. Neff, M.M., and, Chory, J., (1998) Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol. 118, 27-35.
45. Neff, M.M., Nguyen, S.M., Malancharuvil, E.J., et al. (1999) BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc. Natl Acad. Sci. USA, 96, 15316-15323.
46. Oh, K., Ivanchenko, M.G., White, T.J., and, Lomax, T.L., (2006) The diageotropica gene of tomato encodes a cyclophilin: a novel player in auxin signaling. Planta, 224, 133-144.
47. Park, W.J., (1998) Effect of epibrassinolide on hypocotyl growth of the tomato mutant diageotropica. Planta, 207, 120-124.
48. Parks, B.M., and, Quail, P.H., (1993) hy8, a new class of Arabidopsis long hypocotyl mutants deficient in functional phytochrome A. Plant Cell, 5, 39-48.
49. Peng, P., Zhao, J., Zhu, Y., Asami, T., and, Li, J., (2010) A direct docking mechanism for a plant GSK3-like kinase to phosphorylate its substrates. J. Biol. Chem. 285, 24646-24653.
50. Poppe, C., Sweere, U., Drumm-Herrel, H., and, Schafer, E., (1998) The blue light receptor cryptochrome 1 can act independently of phytochrome A and B in Arabidopsis thaliana. Plant J. 16, 465-471.
51. Quail, P.H., (2005) Phytochrome overview. In Light Sensing in Plants (, Wada, M., Shimazaki, K., and, Lino, M., eds). Tokyo: Springer-Verlag, pp. 21-35.
52. Reed, J.W., Nagpal, P., Poole, D.S., Furuya, M., and, Chory, J., (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell, 5, 147-157.
53. Romano, P.G., Horton, P., and, Gray, J.E., (2004) The Arabidopsis cyclophilin gene family. Plant Physiol. 134, 1268-1282.
54. Savaldi-Goldstein, S., Baiga, T.J., Pojer, F., et al. (2008) New auxin analogs with growth-promoting effects in intact plants reveal a chemical strategy to improve hormone delivery. Proc. Natl Acad. Sci. USA, 105, 15190-15195.
55. Sellaro, R., Hoecker, U., Yanovsky, M., Chory, J., and, Casal, J.J., (2009) Synergism of red and blue light in the control of Arabidopsis gene expression and development. Curr. Biol. 19, 1216-1220.
56. Sellaro, R., Crepy, M., Trupkin, S.A., Karayekov, E., Buchovsky, A.S., Rossi, C., and, Casal, J.J., (2010) Cryptochrome as a sensor of the blue/green ratio of natural radiation in Arabidopsis. Plant Physiol. 154, 401-409.
57. Shi, Q.-M., Yang, X., Song, L., and, Xue, H.-W., (2011) Arabidopsis MSBP1 is activated by HY5 and HYH and is involved in photomorphogenesis and brassinosteroid sensitivity regulation. Mol. Plant, 4, 1092-1104.
58. Sun, Y., Fan, X.-Y., Cao, D.-M., et al. (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell, 19 (5), 765-777.
59. Symons, G., and, Reid, J.B., (2008) Brassinosteroids, de-etiolation and the re-emerging art of plant hormone quantification. Plant Signal. Behav. 3 (10), 868-870.
60. Symons, G.M., Smith, J.J., Nomura, T., Davies, N.W., Yokota, T., and, Reid, J.B., (2008) The hormonal regulation of de-etiolation. Planta, 227, 1115-1125.
61. Tang, W., Yuan, M., Wang, R., et al. (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13, 124-131.
62. Tepperman, J.M., Hudson, M.E., Khanna, R., Zhu, T., Chang, S.H., Wang, X., and, Quail, P.H., (2004) Expression profiling of phyB mutant demonstrates substantial contribution of other phytochromes to red-light-regulated gene expression during seedling de-etiolation. Plant J. 38, 725-739.
63. Tepperman, J.M., Hwang, Y.S., and, Quail, P.H., (2006) phyA dominates in transduction of red-light signals to rapidly-responding genes at the initiation of Arabidopsis seedling deetiolation. Plant J. 48, 728-742.
64. Turk, E.M., Fujioka, S., Seto, H., Shimada, Y., Takatsuto, S., Yoshida, S., Denzel, M.A., Torres, Q.I., and, Neff, M.M., (2003) CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol. 133, 1643-1653.
65. Turk, E.M., Fujioka, S., Seto, H., et al. (2005) Bas1 and Sob7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J. 42, 23-34.
66. Vandenbussche, F., Habricot, Y., Condiff, A.S., Maldiney, R., Van der Straeten, D., and, Ahmad, M., (2007) HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J. 49, 428-441.
67. Vert, G., and, Chory, J., (2006) Downstream nuclear events in brassinosteroid signalling. Nature, 441, 96-100.
68. Wang, H., Ma, L., Habashi, J., Li, J., Zhao, H., and, Deng, X.W., (2002a) Analysis of far-red light-regulated genome expression profiles of phytochrome A pathway mutants in Arabidopsis. Plant J. 32, 723-733.
69. Wang, Z.-Y., Nakano, T., Gendron, J., et al. (2002b) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell, 2, 505-513.
70. Wang, Y., Liu, C., Yang, D., Yu, H., and, Liou, Y.C., (2010) Pin1At encoding a peptidyl-prolyl cis/trans isomerase regulates flowering time in Arabidopsis. Mol. Cell, 37, 112-122.
71. Xu, W., Huang, J., Li, B., Li, J., and, Wang, Y., (2008) Is kinase activity essential for biological functions of BRI1? Cell Res. 18, 472-478.
72. Yadav, V., Mallappa, C., Gangappa, S.N., Bhatia, S., and, Chattopadhyay, S., (2005) A basic helix-loop-helix transcription factor in Arabidopsis, MYC2, acts as a repressor of blue light-mediated photomorphogenic growth. Plant Cell, 17, 1953-1966.
73. Yang, X.H., Xu, Z.H., and, Xue, H.W., (2005) Arabidopsis membrane steroid-binding protein 1 is involved in inhibition of cell elongation. Plant Cell, 17, 116-131.
74. Yi, C., and, Deng, X.W., (2005) COP1 - from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol. 15, 618-625.
75. Yin, Y.H., Wang, Z.Y., Mora-Garcia, S., Li, J.M., Yoshida, S., Asami, T., and, Chory, J., (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell, 109, 181-191.
76. Yu, X., Li, L., Zola, J., et al. (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65, 634-646.
77. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and, Gruissem, W., (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.