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

Volumn 24, Issue 4, 2012, Pages 1398-1419

  Leivar, Pablo ^a,b,c   Tepperman, James M ^a,b   Cohn, Megan M ^a,b   Monte, Elena ^c   Al Sady, Bassem ^a,b   Erickson, Erika ^a,b   Quail, Peter H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WESTERN REGIONAL RESEARCH CENTER   (United States)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84861403941     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.095711     Document Type: Article

References (83)

1. Al-Sady, B., Kikis, E.A., Monte, E., and Quail, P.H. (2008). Mechanistic duality of ranscription 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 egradation. Mol. Cell 23: 439-446.
3. Bae, G., and Choi, G. (2008). Decoding of light signals by plant phytochromes and their interacting proteins. Annu. Rev. Plant Biol. 59: 281-311.
4. 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.
5. Carabelli, M., Possenti, M., Sessa, G., Ciolfi, A., Sassi, M., Morelli, G., and Ruberti, I. (2007). Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev. 21: 1863-1868.
6. 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.
7. Chang, S., Puryear, J., and Cairney, J. (1993). A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11: 113-116.
8. Child, R., and Smith, H. (1987). Phytochrome action in light-grown mustard: Kinetics, fluence-rate compensation and ecological significance. Planta 172: 219-229.
9. Cole, B., Kay, S.A., and Chory, J. (2011). Automated analysis of hypocotyl growth dynamics during shade avoidance in Arabidopsis. Plant J. 65: 991-1000.
10. 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.
11. Devlin, P.F., Yanovsky, M.J., and Kay, S.A. (2003). A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol. 133: 1617-1629.
12. 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.
13. Edgar, R., Domrachev, M., and Lash, A.E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-210.
14. Feng, S., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479.
15. Franklin, K.A. (2008). Shade avoidance. New Phytol. 179: 930-944.
16. Franklin, K.A., Lee, S.H., Patel, D., Kumar, S.V., Spartz, A.K., Gu, C., Ye, S., Yu, P., Breen, G., Cohen, J.D., Wigge, P.A., and Gray, W.M. (2011). Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl. Acad. Sci. USA 108: 20231-20235.
17. Franklin, K.A., and Quail, P.H. (2010). Phytochrome functions in Arabidopsis development. J. Exp. Bot. 61: 11-24.
18. Friedrichsen, D.M., Nemhauser, J., Muramitsu, T., Maloof, J.N., Alonso, J., Ecker, J.R., Furuya, M., and Chory, J. (2002). Three redundant brassinosteroid early response genes encode putative bHLH transcription factors required for normal growth. Genetics 162: 1445-1456.
19. 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.
20. Grebe, M. (2011). Out of the shade and into the light. Nat. Cell Biol. 13: 347-349.
21. 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.
22. Hu, W., Su, Y.S., and Lagarias, J.C. (2009). A light-independent allele of phytochrome B faithfully recapitulates photomorphogenic transcriptional networks. Mol. Plant 2: 166-182.
23. 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.
24. 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.
25. Jiao, Y., Lau, O.S., and Deng, X.W. (2007). Light-regulated transcriptional networks in higher plants. Nat. Rev. Genet. 8: 217-230.
26. Keller, M.M., Jaillais, Y., Pedmale, U.V., Moreno, J.E., Chory, J., and Ballaré, C.L. (2011). Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. Plant J. 67: 195-207.
27. Keuskamp, D.H., Pollmann, S., Voesenek, L.A., Peeters, A.J., and Pierik, R. (2010). Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc. Natl. Acad. Sci. USA 107: 22740-22744.
28. Keuskamp, D.H., Sasidharan, R., Vos, I., Peeters, A.J., Voesenek, L.A., and Pierik, R. (2011). Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. Plant J. 67: 208-217.
29. Khanna, R., Shen, Y., Marion, C.M., Tsuchisaka, A., Theologis, A., Schäfer, E., and Quail, P.H. (2007). The basic helix-loop-helix transcription factor PIF5 acts on ethylene biosynthesis and phytochrome signaling by distinct mechanisms. Plant Cell 19: 3915-3929.
30. Kim, J., Yi, H., Choi, G., Shin, B., Song, P.S., and Choi, G. (2003). Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15: 2399-2407.
31. Koini, M.A., Alvey, L., Allen, T., Tilley, C.A., Harberd, N.P., Whitelam, G.C., and Franklin, K.A. (2009). High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19: 408-413.
32. Kozuka, T., Kobayashi, J., Horiguchi, G., Demura, T., Sakakibara, H., Tsukaya, H., and Nagatani, A. (2010). Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol. 153: 1608-1618.
33. Leivar, P., Monte, E., Al-Sady, B., Carle, C., Storer, A., Alonso, J.M., Ecker, J.R., and Quail, P.H. (2008b). 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.
34. Leivar, P., Monte, E., Cohn, M.M., and Quail, P.H. (April 5, 2012). Phytochrome signaling in green Arabidopsis seedlings: Impact assessment of a mutually-negative phyB-PIF feedback loop. Mol. Plant http://dx.doi.org/10.1093/mp/sss031.
35. Leivar, P., Monte, E., Oka, Y., Liu, T., Carle, C., Castillon, A., Huq, E., and Quail, P.H. (2008a). Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr. Biol. 18: 1815-1823.
36. Leivar, P., and Quail, P.H. (2011). PIFs: Pivotal components in a cellular signaling hub. Trends Plant Sci. 16: 19-28.
37. 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.
38. 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.
39. Lorrain, S., Trevisan, M., Pradervand, S., and Fankhauser, C. (2009). Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J. 60: 449-461.
40. Martínez-García, J.F., Huq, E., and Quail, P.H. (2000). Direct targeting of light signals to a promoter element-bound transcription factor. Science 288: 859-863.
41. Mockaitis, K., and Estelle, M. (2008). Auxin receptors and plant development: A new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24: 55-80.
42. Monte, E., Alonso, J.M., Ecker, J.R., Zhang, Y., Li, X., Young, J., Austin-Phillips, S., and Quail, P.H. (2003). Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell 15: 1962-1980.
43. 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.
44. Monte, E., Tepperman, J.M., Al-Sady, B., Kaczorowski, K.A., Alonso, J.M., Ecker, J.R., Li, X., Zhang, Y., and Quail, P.H. (2004). The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proc. Natl. Acad. Sci. USA 101: 16091-16098.
45. 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.
46. Nagatani, A. (2004). Light-regulated nuclear localization of phytochromes. Curr. Opin. Plant Biol. 7: 708-711.
47. Nozue, K., Covington, M.F., Duek, P.D., Lorrain, S., Fankhauser, C., Harmer, S.L., and Maloof, J.N. (2007). Rhythmic growth explained by coincidence between internal and external cues. Nature 448: 358-361.
48. Nozue, K., Harmer, S.L., and Maloof, J.N. (2011). Genomic analysis of circadian clock-, light-, and growth-correlated genes reveals PHYTOCHROME- INTERACTING FACTOR5 as a modulator of auxin signaling in Arabidopsis. Plant Physiol. 156: 357-372.
49. 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.
50. 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.
51. Oh, E., Yamaguchi, S., Hu, J., Yusuke, J., Jung, B., Paik, I., Lee, H.S., Sun, T.P., Kamiya, Y., and Choi, G. (2007). PIL5, a phytochromeinteracting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19: 1192-1208.
52. Oh, E., Yamaguchi, S., Kamiya, Y., Bae, G., Chung, W.I., and Choi, G. (2006). Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. Plant J. 47: 124-139.
53. Park, E., Kim, J., Lee, Y., Shin, J., Oh, E., Chung, W.I., Liu, J.R., and Choi, G. (2004). Degradation of phytochrome interacting factor 3 in phytochrome-mediated light signaling. Plant Cell Physiol. 45: 968-975.
54. Quail, P.H. (2010). Phytochromes. Curr. Biol. 20: R504-R507.
55. Rockwell, N.C., Su, Y.S., and Lagarias, J.C. (2006). Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57: 837-858.
56. Roig-Villanova, I., Bou, J., Sorin, C., Devlin, P.F., and Martínez-García, J.F. (2006). Identification of primary target genes of phytochrome signaling. Early transcriptional control during shade avoidance responses in Arabidopsis. Plant Physiol. 141: 85-96.
57. Roig-Villanova, I., Bou-Torrent, J., Galstyan, A., Carretero-Paulet, L., Portolés, S., Rodríguez-Concepción, M., and Martínez-García, J.F. (2007). Interaction of shade avoidance and auxin responses: A role for two novel atypical bHLH proteins. EMBO J. 26: 4756-4767.
58. Rose, J.K., Braam, J., Fry, S.C., and Nishitani, K. (2002). The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: Current perspectives and a new unifying nomenclature. Plant Cell Physiol. 43: 1421-1435.
59. Salter, M.G., Franklin, K.A., and Whitelam, G.C. (2003). Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426: 680-683.
60. Sasidharan, R., Chinnappa, C.C., Staal, M., Elzenga, J.T., Yokoyama, R., Nishitani, K., Voesenek, L.A., and Pierik, R. (2010). Light qualitymediated petiole elongation in Arabidopsis during shade avoidance involves cell wall modification by xyloglucan endotransglucosylase/ hydrolases. Plant Physiol. 154: 978-990.
61. Schafer, E., and Nagy, F. (2006). Photomorphogenesis in Plants and Bacteria. (Dordrecht, The Netherlands: Springer).
62. Sentandreu, M., Martín, G., González-Schain, N., Leivar, P., Soy, J., Tepperman, J.M., Quail, P.H., and Monte, E. (2011). Functional profiling identifies genes involved in organ-specific branches of the PIF3 regulatory network in Arabidopsis. Plant Cell 23: 3974-3991.
63. Sessa, G., Carabelli, M., Sassi, M., Ciolfi, A., Possenti, M., Mittempergher, F., Becker, J., Morelli, G., and Ruberti, I. (2005). A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev. 19: 2811-2815.
64. Shen, H., Moon, J., and Huq, E. (2005). PIF1 is regulated by lightmediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J. 44: 1023-1035.
65. 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.
66. Shen, Y., Khanna, R., Carle, C.M., and Quail, P.H. (2007). Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol. 145: 1043-1051.
67. 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.
68. Shin, J., Park, E., and Choi, G. (2007). PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J. 49: 981-994.
69. Smith, H., and Whitelam, G.C. (1997). The shade avoidance syndrome: Multiple responses mediated by multiple phytochromes. Plant Cell Environ. 20: 840-844.
70. Smyth, G.K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3: Article 3.
71. Sorin, C., Salla-Martret, M., Bou-Torrent, J., Roig-Villanova, I., and Martínez-García, J.F. (2009). ATHB4, a regulator of shade avoidance, modulates hormone response in Arabidopsis seedlings. Plant J. 59: 266-277.
72. Soy, J., Leivar, P., González-Schain, N., Sentandreu, M., Prat, S., Quail, P.H., and Monte, E. (March 12, 2012). Phytochrome-imposed oscillations in PIF3-protein abundance regulate hypocotyl growth under diurnal light-dark conditions in Arabidopsis. Plant J. http://dx.doi.org/10.1111/j.1365-313X.2012.04992.x.
73. Stamm, P., and Kumar, P.P. (2010). The phytohormone signal network regulating elongation growth during shade avoidance. J. Exp. Bot. 61: 2889-2903.
74. Stavang, J.A., Gallego-Bartolomé, J., Gómez, M.D., Yoshida, S., Asami, T., Olsen, J.E., García-Martínez, J.L., Alabadí, D., and Blázquez, M.A. (2009). Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60: 589-601.
75. Steindler, C., Matteucci, A., Sessa, G., Weimar, T., Ohgishi, M., Aoyama, T., Morelli, G., and Ruberti, I. (1999). Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development 126: 4235-4245.
76. 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.
77. Strasser, B., Sánchez-Lamas, M., Yanovsky, M.J., Casal, J.J., and Cerdán, P.D. (2010). Arabidopsis thaliana life without phytochromes. Proc. Natl. Acad. Sci. USA 107: 4776-4781.
78. Tanaka, S., Nakamura, S., Mochizuki, N., and Nagatani, A. (2002). Phytochrome in cotyledons regulates the expression of genes in the hypocotyl through auxin-dependent and -independent pathways. Plant Cell Physiol. 43: 1171-1181.
79. Tao, Y., et al. (2008). Rapid synthesis of auxin via a new tryptophandependent pathway is required for shade avoidance in plants. Cell 133: 164-176.
80. 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 redlight- regulated gene expression during seedling de-etiolation. Plant J. 38: 725-739.
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. Vandenbussche, F., Vriezen, W.H., Smalle, J., Laarhoven, L.J., Harren, F.J., and Van Der Straeten, D. (2003). Ethylene and auxin control the Arabidopsis response to decreased light intensity. Plant Physiol. 133: 517-527.
83. Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., and Chory, J. (2005). A new class of transcription factors mediates brassinosteroid- regulated gene expression in Arabidopsis. Cell 120: 249-259.