Hemera couples the proteolysis and transcriptional activity of phytochrome interacting actors in arabidopsis photomorphogenesis

Plant Cell

Volumn 27, Issue 5, 2015, Pages 1409-1427

  Qiu, Yongjian ^a   Li, Meina ^a   Pasoreck, Elise K ^a   Long, Lingyun ^a   Shi, Yiting ^a   Galvão, Rafaelo M ^a   Chou, Conrad L ^a   Wang, He ^a   Sun, Amanda Y ^a   Zhang, Yiyin C ^a   Jiang, Anna ^a   Chen, Meng ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HMR PROTEIN, ARABIDOPSIS; HYBRID PROTEIN; PHYTOCHROME; PIF1 PROTEIN, ARABIDOPSIS; PIF3 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

ARABIDOPSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYPOCOTYL; METABOLISM; MICROARRAY ANALYSIS; MUTATION; PROTEIN DEGRADATION; PROTEIN MOTIF; TRANSCRIPTION INITIATION; TWO HYBRID SYSTEM;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HYPOCOTYL; MICROARRAY ANALYSIS; MUTATION; PHYTOCHROME; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84930686610     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.136093     Document Type: Article

References (92)

1. Al-Sady, B., Kikis, E.A., Monte, E., and Quail, P.H. (2008). Mechanistic duality of transcription factor function in phytochrome signaling. Proc. Natl. Acad. Sci. USA 105: 2232–2237
2. Al-Sady, B., Ni, W., Kircher, S., Schäfer, E., and Quail, P.H. (2006). Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. Cell 23: 439–446
3. Bäckström, S., Elfving, N., Nilsson, R., Wingsle, G., and Björklund, S. (2007). Purification of a plant mediator from Arabidopsis thaliana identifies PFT1 as the Med25 subunit. Mol. Cell 26: 717–729
4. Bailey, P.C., Martin, C., Toledo-Ortiz, G., Quail, P.H., Huq, E., Heim, M.A., Jakoby, M., Werber, M., and Weisshaar, B. (2003). Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana. Plant Cell 15: 2497–2502
5. Bauer, D., Viczián, A., Kircher, S., Nobis, T., Nitschke, R., Kunkel, T., Panigrahi, K.C., Adám, E., Fejes, E., Schäfer, E., and Nagy, F. (2004). Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16: 1433–1445
6. Bernardo-García, S., de Lucas, M., Martínez, C., Espinosa-Ruiz, A., Davière, J.M., and Prat, S. (2014). BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth. Genes Dev. 28: 1681–1694
7. Borggrefe, T., and Yue, X. (2011). Interactions between subunits of the Mediator complex with gene-specific transcription factors. Semin. Cell Dev. Biol. 22: 759–768
8. Carey, M., Kakidani, H., Leatherwood, J., Mostashari, F., and Ptashne, M. (1989). An amino-terminal fragment of GAL4 binds DNA as a dimer. J. Mol. Biol. 209: 423–432
9. Cerdán, P.D., and Chory, J. (2003). Regulation of flowering time by light quality. Nature 423: 881–885
10. Chen, H., Huang, X., Gusmaroli, G., Terzaghi, W., Lau, O.S., Yanagawa, Y., Zhang, Y., Li, J., Lee, J.H., Zhu, D., and Deng, X.W. (2010a). Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1- SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 22: 108–123
11. Chen, M., and Chory, J. (2011). Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 21: 664–671
12. Chen, M., Schwab, R., and Chory, J. (2003). Characterization of the requirements for localization of phytochrome B to nuclear bodies. Proc. Natl. Acad. Sci. USA 100: 14493–14498
13. Chen, M., Galvão, R.M., Li, M., Burger, B., Bugea, J., Bolado, J., and Chory, J. (2010b). Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141: 1230–1240
14. Chi, Y., Huddleston, M.J., Zhang, X., Young, R.A., Annan, R.S., Carr, S.A., and Deshaies, R.J. (2001). Negative regulation of Gcn4 and Msn2 transcription factors by Srb10 cyclin-dependent kinase. Genes Dev. 15: 1078–1092
15. Christie, J.M., Arvai, A.S., Baxter, K.J., Heilmann, M., Pratt, A.J., O’Hara, A., Kelly, S.M., Hothorn, M., Smith, B.O., Hitomi, K., Jenkins, G.I., and Getzoff, E.D. (2012). Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335: 1492–1496
16. de Lucas, M., Davière, J.M., Rodríguez-Falcón, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blázquez, M.A., Titarenko, E., and Prat, S. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480–484
17. Franklin, K.A., and Quail, P.H. (2010). Phytochrome functions in Arabidopsis development. J. Exp. Bot. 61: 11–24
18. Fujimori, T., Yamashino, T., Kato, T., and Mizuno, T. (2004). Circadiancontrolled basic/helix-loop-helix factor, PIL6, implicated in light-signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 45: 1078–1086
19. Galvão, R.M., Li, M., Kothadia, S.M., Haskel, J.D., Decker, P.V., Van Buskirk, E.K., and Chen, M. (2012). Photoactivated phytochromes interact with HEMERA and promote its accumulation to establish photomorphogenesis in Arabidopsis. Genes Dev. 26: 1851–1863
20. Geng, F., and Tansey, W.P. (2012). Similar temporal and spatial recruitment of native 19S and 20S proteasome subunits to transcriptionally active chromatin. Proc. Natl. Acad. Sci. USA 109: 6060–6065
21. Hall, D.B., and Struhl, K. (2002). The VP16 activation domain interacts with multiple transcriptional components as determined by proteinprotein cross-linking in vivo. J. Biol. Chem. 277: 46043–46050
22. Heim, M.A., Jakoby, M., Werber, M., Martin, C., Weisshaar, B., and Bailey, P.C. (2003). The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 20: 735–747
23. 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
24. Hornitschek, P., Kohnen, M.V., Lorrain, S., Rougemont, J., Ljung, K., López-Vidriero, I., Franco-Zorrilla, J.M., Solano, R., Trevisan, M., Pradervand, S., Xenarios, I., and Fankhauser, C. (2012). Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 71: 699–711
25. Hu, W., Franklin, K.A., Sharrock, R.A., Jones, M.A., Harmer, S.L., and Lagarias, J.C. (2013). Unanticipated regulatory roles for Arabidopsis phytochromes revealed by null mutant analysis. Proc. Natl. Acad. Sci. USA 110: 1542–1547
26. 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
27. Huq, E., Al-Sady, B., Hudson, M., Kim, C., Apel, K., and Quail, P.H. (2004). Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305: 1937–1941
28. Iñigo, S., Giraldez, A.N., Chory, J., and Cerdán, P.D. (2012a). Proteasomemediated turnover of Arabidopsis MED25 is coupled to the activation of FLOWERING LOCUS T transcription. Plant Physiol. 160: 1662–1673
29. Iñigo, S., Alvarez, M.J., Strasser, B., Califano, A., and Cerdán, P.D. (2012b). PFT1, the MED25 subunit of the plant Mediator complex, promotes flowering through CONSTANS dependent and independent mechanisms in Arabidopsis. Plant J. 69: 601–612
30. Kami, C., Lorrain, S., Hornitschek, P., and Fankhauser, C. (2010). Lightregulated plant growth and development. Curr. Top. Dev. Biol. 91: 29–66
31. 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
32. Kim, J., Yi, H., Choi, G., Shin, B., Song, P.S., and Choi, G. (2003a). Functional characterization of phytochrome interacting factor 3 in phytochrome- mediated light signal transduction. Plant Cell 15: 2399–2407
33. Kim, S.Y., Herbst, A., Tworkowski, K.A., Salghetti, S.E., and Tansey, W.P. (2003b). Skp2 regulates Myc protein stability and activity. Mol. Cell 11: 1177–1188
34. Kircher, S., Gil, P., Kozma-Bognár, L., Fejes, E., Speth, V., Husselstein-Muller, T., Bauer, D., Adám, E., Schäfer, E., and Nagy, F. (2002). Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14: 1541–1555
35. Klose, C., Büche, C., Fernandez, A.P., Schäfer, E., Zwick, E., and Kretsch, T. (2012). The mediator complex subunit PFT1 interferes with COP1 and HY5 in the regulation of Arabidopsis light signaling. Plant Physiol. 160: 289–307
36. Kobayashi, N., Boyer, T.G., and Berk, A.J. (1995). A class of activation domains interacts directly with TFIIA and stimulates TFIIATFIID- promoter complex assembly. Mol. Cell. Biol. 15: 6465–6473
37. Konieczny, A., and Ausubel, F.M. (1993). A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCRbased markers. Plant J. 4: 403–410
38. Langlois, C., Mas, C., Di Lello, P., Jenkins, L.M., Legault, P., and Omichinski, J.G. (2008). NMR structure of the complex between the Tfb1 subunit of TFIIH and the activation domain of VP16: structural similarities between VP16 and p53 J. Am. Chem. Soc. 130: 10596–10604
39. Leivar, P., and Quail, P.H. (2011). PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16: 19–28
40. 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 21: 3535–3553
41. Leivar, P., Tepperman, J.M., Cohn, M.M., Monte, E., Al-Sady, B., Erickson, E., and Quail, P.H. (2012). Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. Plant Cell 24: 1398–1419
42. Leivar, P., Monte, E., Al-Sady, B., Carle, C., Storer, A., Alonso, J.M., Ecker, J.R., and Quail, P.H. (2008a). The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 20: 337–352
43. Leivar, P., Monte, E., Oka, Y., Liu, T., Carle, C., Castillon, A., Huq, E., and Quail, P.H. (2008b). Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr. Biol. 18: 1815–1823
44. Li, L., et al. (2012). Linking photoreceptor excitation to changes in plant architecture. Genes Dev. 26: 785–790
45. Lipford, J.R., and Deshaies, R.J. (2003). Diverse roles for ubiquitin-dependent proteolysis in transcriptional activation. Nat. Cell Biol. 5: 845–850
46. Lipford, J.R., Smith, G.T., Chi, Y., and Deshaies, R.J. (2005). A putative stimulatory role for activator turnover in gene expression. Nature 438: 113–116
47. Lorrain, S., Trevisan, M., Pradervand, S., and Fankhauser, C. (2009). Phytochrome interacting factors 4 and 5 redundantly limit seedling deetiolation in continuous far-red light. Plant J. 60: 449–461
48. 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
49. Luo, Q., Lian, H.L., He, S.B., Li, L., Jia, K.P., and Yang, H.Q. (2014). COP1 and phyB physically Interact with PIL1 to Regulate Its Stability and Photomorphogenic Development in Arabidopsis. Plant Cell 26: 2441–2456
50. 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
51. Mitchell, P.J., and Tjian, R. (1989). Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245: 371–378
52. Moon, J., Zhu, L., Shen, H., and Huq, E. (2008). PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc. Natl. Acad. Sci. USA 105: 9433–9438
53. Muratani, M., and Tansey, W.P. (2003). How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4: 192–201
54. Murre, C., et al. (1989). Interactions between heterologous helixloop- helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58: 537–544
55. Nagatani, A. (2010). Phytochrome: structural basis for its functions. Curr. Opin. Plant Biol. 13: 565–570
56. Ni, W., Xu, S.L., Chalkley, R.J., Pham, T.N., Guan, S., Maltby, D.A., Burlingame, A.L., Wang, Z.Y., and Quail, P.H. (2013). Multisite light-induced phosphorylation of the transcription factor PIF3 is necessary for both its rapid degradation and concomitant negative feedback modulation of photoreceptor phyB levels in Arabidopsis. Plant Cell 25: 2679–2698
57. Ni, W., Xu, S.L., Tepperman, J.M., Stanley, D.J., Maltby, D.A., Gross, J.D., Burlingame, A.L., Wang, Z.Y., and Quail, P.H. (2014). A mutually assured destruction mechanism attenuates light signaling in Arabidopsis. Science 344: 1160–1164
58. Oh, E., Zhu, J.Y., and Wang, Z.Y. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14: 802–809
59. Oh, E., Kim, J., Park, E., Kim, J.I., Kang, C., and Choi, G. (2004). PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16: 3045–3058
60. Oh, E., Kang, H., Yamaguchi, S., Park, J., Lee, D., Kamiya, Y., and Choi, G. (2009). Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21: 403–419
61. Park, E., Park, J., Kim, J., Nagatani, A., Lagarias, J.C., and Choi, G. (2012). Phytochrome B inhibits binding of phytochrome-interacting factors to their target promoters. Plant J. 72: 537–546
62. Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K.J., and Oelmüller, R. (2006). pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18: 176–197
63. Pfeiffer, A., Shi, H., Tepperman, J.M., Zhang, Y., and Quail, P.H. (2014). Combinatorial complexity in a transcriptionally centered signaling hub in Arabidopsis. Mol. Plant 7: 1598–1618
64. Piskacek, S., Gregor, M., Nemethova, M., Grabner, M., Kovarik, P., and Piskacek, M. (2007). Nine-amino-acid transactivation domain: establishment and prediction utilities. Genomics 89: 756–768
65. Ptashne, M. (1988). How eukaryotic transcriptional activators work. Nature 335: 683–689
66. Rausenberger, J., Hussong, A., Kircher, S., Kirchenbauer, D., Timmer, J., Nagy, F., Schäfer, E., and Fleck, C. (2010). An integrative model for phytochrome B mediated photomorphogenesis: from protein dynamics to physiology. PLoS ONE 5: e10721
67. Reid, G., Hübner, M.R., Métivier, R., Brand, H., Denger, S., Manu, D., Beaudouin, J., Ellenberg, J., and Gannon, F. (2003). Cyclic, proteasome-mediated turnover of unliganded and liganded ERalpha on responsive promoters is an integral feature of estrogen signaling. Mol. Cell 11: 695–707
68. Rizzini, L., Favory, J.J., Cloix, C., Faggionato, D., O’Hara, A., Kaiserli, E., Baumeister, R., Schäfer, E., Nagy, F., Jenkins, G.I., and Ulm, R. (2011). Perception of UV-B by the Arabidopsis UVR8 protein. Science 332: 103–106
69. Rockwell, N.C., Su, Y.S., and Lagarias, J.C. (2006). Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57: 837–858
70. Sadowski, I., Ma, J., Triezenberg, S., and Ptashne, M. (1988). GAL4-VP16 is an unusually potent transcriptional activator. Nature 335: 563–564
71. Salghetti, S.E., Caudy, A.A., Chenoweth, J.G., and Tansey, W.P. (2001). Regulation of transcriptional activation domain function by ubiquitin. Science 293: 1651–1653
72. Salghetti, S.E., Muratani, M., Wijnen, H., Futcher, B., and Tansey, W.P. (2000). Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis. Proc. Natl. Acad. Sci. USA 97: 3118–3123
73. Schwechheimer, C., Smith, C., and Bevan, M.W. (1998). The activities of acidic and glutamine-rich transcriptional activation domains in plant cells: design of modular transcription factors for high-level expression. Plant Mol. Biol. 36: 195–204
74. Shen, H., Zhu, L., Castillon, A., Majee, M., Downie, B., and Huq, E. (2008). Light-induced phosphorylation and degradation of the negative regulator PHYTOCHROME-INTERACTING FACTOR1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. Plant Cell 20: 1586–1602
75. Shin, J., Kim, K., Kang, H., Zulfugarov, I.S., Bae, G., Lee, C.H., Lee, D., and Choi, G. (2009). Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors. Proc. Natl. Acad. Sci. USA 106: 7660–7665
76. Spoel, S.H., Mou, Z., Tada, Y., Spivey, N.W., Genschik, P., and Dong, X. (2009). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137: 860–872
77. Stephenson, P.G., Fankhauser, C., and Terry, M.J. (2009). PIF3 is a repressor of chloroplast development. Proc. Natl. Acad. Sci. USA 106: 7654–7659
78. 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 de-etiolation. Plant J. 48: 728–742
79. Till, B.J., et al. (2003). Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res. 13: 524–530
80. Toledo-Ortiz, G., Huq, E., and Quail, P.H. (2003). The Arabidopsis basic/ helix-loop-helix transcription factor family. Plant Cell 15: 1749–1770
81. Toledo-Ortiz, G., Huq, E., and Rodríguez-Concepción, M. (2010). Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc. Natl. Acad. Sci. USA 107: 11626–11631
82. Uesugi, M., Nyanguile, O., Lu, H., Levine, A.J., and Verdine, G.L. (1997). Induced alpha helix in the VP16 activation domain upon binding to a human TAF. Science 277: 1310–1313
83. Van Buskirk, E.K., Decker, P.V., and Chen, M. (2012). Photobodies in light signaling. Plant Physiol. 158: 52–60
84. Van Buskirk, E.K., Reddy, A.K., Nagatani, A., and Chen, M. (2014). Photobody localization of phytochrome B is tightly correlated with prolonged and light-dependent inhibition of hypocotyl elongation in the dark. Plant Physiol. 165: 595–607
85. Vojnic, E., Mourão, A., Seizl, M., Simon, B., Wenzeck, L., Larivière, L., Baumli, S., Baumgart, K., Meisterernst, M., Sattler, M., and Cramer, P. (2011). Structure and VP16 binding of the Mediator Med25 activator interaction domain. Nat. Struct. Mol. Biol. 18: 404–409
86. von der Lehr, N., et al. (2003). The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Mycregulated transcription. Mol. Cell 11: 1189–1200
87. Williams-Carrier, R., Zoschke, R., Belcher, S., Pfalz, J., and Barkan, A. (2014). A major role for the plastid-encoded RNA polymerase complex in the expression of plastid transfer RNAs. Plant Physiol. 164: 239–248
88. Wu, D., Hu, Q., Yan, Z., Chen, W., Yan, C., Huang, X., Zhang, J., Yang, P., Deng, H., Wang, J., Deng, X., and Shi, Y. (2012). Structural basis of ultraviolet-B perception by UVR8 Nature 484: 214–219
89. Xu, X., Paik, I., Zhu, L., Bu, Q., Huang, X., Deng, X.W., andHuq, E. (2014). PHYTOCHROME INTERACTING FACTOR1 enhances the E3 ligase activity of CONSTITUTIVE PHOTOMORPHOGENIC1 to synergistically repress photomorphogenesis in Arabidopsis. Plant Cell 26: 1992–2006
90. Yamaguchi, R., Nakamura, M., Mochizuki, N., Kay, S.A., and Nagatani, A. (1999). Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J. Cell Biol. 145: 437–445
91. Zhai, Q., Yan, L., Tan, D., Chen, R., Sun, J., Gao, L., Dong, M.Q., Wang, Y., and Li, C. (2013). Phosphorylation-coupled proteolysis of the transcription factor MYC2 is important for jasmonate-signaled plant immunity. PLoS Genet. 9: e1003422
92. Zhang, Y., Mayba, O., Pfeiffer, A., Shi, H., Tepperman, J.M., Speed, T.P., and Quail, P.H. (2013). A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genet. 9: e1003244.