Heat shock-induced fluctuations in clock and light signaling enhance phytochrome B-mediated arabidopsis deetiolation

Plant Cell

Volumn 25, Issue 8, 2013, Pages 2892-2906

  Karayekov, Elizabeth ^a   Sellaro, Romina ^a   Legris, Martina ^b   Yanovsky, Marcelo J ^a,b   Casal, Jorge J ^a,b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; PHYB PROTEIN, ARABIDOPSIS; PHYTOCHROME B; TRANSCRIPTOME;

ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; CELL NUCLEUS; CIRCADIAN RHYTHM; DARKNESS; ETIOLATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; HEAT SHOCK RESPONSE; LIGHT; METABOLISM; PHYSIOLOGY; PLANT GROWTH; PROTEIN STABILITY; RADIATION EXPOSURE; SEEDLING; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; CIRCADIAN CLOCKS; DARKNESS; ETIOLATION; GENE EXPRESSION REGULATION, PLANT; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; HYPOCOTYL; LIGHT; MODELS, BIOLOGICAL; PHYTOCHROME B; PROTEIN STABILITY; SEEDLING; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84884677733     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.114306     Document Type: Article

References (66)

1. Abràmoff, M.D., Magalhàes, P.J., and Ram, S.J. (2004). Image processing with image. J. Biophotonics International 11: 36-41.
2. Anderson, S.L., Somers, D.E., Millar, A.J., Hanson, K., Chory, J., and Kay, S.A. (1997). Attenuation of phytochrome A and B signaling pathways by the Arabidopsis circadian clock. Plant Cell 9: 1727-1743.
3. Andronis, C., Barak, S., Knowles, S.M., Sugano, S., and Tobin, E.M. (2008). The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis. Mol. Plant 1: 58-67.
4. Bauer, D., Viczián, A., Kircher, S., Nobis, T., Nitschke, R., Kunkel, T., Panigrahi, K.C.S., Adám, E., Fejes, E., Schäfer, E., andNagy, 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. Beator, J., Pötter, E., and Kloppstech, K. (1992). The effect of heat shock on morphogenesis in barley: Coordinated circadian regulation of mRNA levels for light-regulated genes and of the capacity for accumulation of chlorophyll protein complexes. Plant Physiol. 100: 1780-1786.
6. Busch, W., Wunderlich, M., and Schöffl, F. (2005). Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J. 41: 1-14.
7. Casal, J.J. (1996). Phytochrome A enhances the promotion of hypocotyl growth caused by reductions in levels of phytochrome B in its far-redlight-absorbing form in light-grown Arabidopsis thaliana. Plant Physiol. 112: 965-973.
8. Catalá, R., Medina, J., and Salinas, J. (2011). Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc. Natl. Acad. Sci. USA 108: 16475-16480.
9. Chen, M., Chory, J., and Fankhauser, C. (2004). Light signal transduction in higher plants. Annu. Rev. Genet. 38: 87-117.
10. Dong, M.A., Farré, E.M., and Thomashow, M.F. (2011). Circadian clockassociated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA 108: 7241-7246.
11. Downs, R.J., Hendricks, S.B., and Borthwick, H.A. (1957). Photoreversible control of elongation of pinto beans and other plants under normal conditions of growth. Bot. Gaz. 118: 199-208.
12. Fankhauser, C., and Chory, J. (1997). Light control of plant development. Annu. Rev. Cell Dev. Biol. 13: 203-229.
13. Farré, E.M., Harmer, S.L., Harmon, F.G., Yanovsky, M.J., and Kay, S.A. (2005). Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. 15: 47-54.
14. Franklin, K.A. (2009). Light and temperature signal crosstalk in plant development. Curr. Opin. Plant Biol. 12: 63-68.
15. 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.
16. 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. 45: 1078-1086.
17. Gould, P.D., Locke, J.C.W., Larue, C., Southern, M.M., Davis, S.J., Hanano, S., Moyle, R., Milich, R., Putterill, J., Millar, A.J., and Hall, A. (2006). The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18: 1177-1187.
18. Gray, W.M., Östin, A., Sandberg, G., Romano, C.P., and Estelle, M. (1998). High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 7197-7202.
19. 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.
20. 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.
21. 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.
22. Ito, S., Nakamichi, N., Nakamura, Y., Niwa, Y., Kato, T., Murakami, M., Kita, M., Mizoguchi, T., Niinuma, K., Yamashino, T., and Mizuno, T. (2007). Genetic linkages between circadian clock-associated components and phytochrome-dependent red light signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 48: 971-983.
23. Kaczorowski, K.A., and Quail, P.H. (2003). Arabidopsis PSEUDORESPONSE REGULATOR7 is a signaling intermediate in phytochromeregulated seedling deetiolation and phasing of the circadian clock. Plant Cell 15: 2654-2665.
24. Kami, C., Lorrain, S., Hornitschek, P., and Fankhauser, C. (2010). Light-regulated plant growth and development. Curr. Top. Dev. Biol. 91: 29-66.
25. Kant, P., Gordon, M., Kant, S., Zolla, G., Davydov, O., Heimer, Y.M., Chalifa-Caspi, V., Shaked, R., and Barak, S. (2008). Functionalgenomics-based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses. Plant Cell Environ. 31: 697-714.
26. Keuskamp, D.H., Pollmann, S., Voesenek, L.A.C.J., Peeters, A.J.M., 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.
27. Kikis, E.A., Khanna, R., and Quail, P.H. (2005). ELF4 is a phytochromeregulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. Plant J. 44: 300-313.
28. 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.
29. Kloppstech, K., Otto, B., and Sierralta, W. (1991). Cyclic temperature treatments of dark-grown pea seedlings induce a rise in specific transcript levels of light-regulated genes related to photomorphogenesis. Mol. Gen. Genet. 225: 468-473.
30. Koini, M.A., Alvey, L., Allen, T., Tilley, C.A., Harberd, N.P., Whitelam, G.C., and Franklin, K.A. (2009). High temperaturemediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19: 408-413.
31. Larkindale, J., and Knight, M.R. (2002). Protection against heat stressinduced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128: 682-695.
32. Lau, O.S., and Deng, X.-W. (2012). The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci. 17: 584-593.
33. Lee, J., He, K., Stolc, V., Lee, H., Figueroa, P., Gao, Y., Tongprasit, W., Zhao, H., Lee, I., and Deng, X.-W. (2007). Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19: 731-749.
34. Leivar, P., and Quail, P.H. (2011). PIFs: Pivotal components in a cellular signaling hub. Trends Plant Sci. 16: 19-28.
35. Lu, S.X., Webb, C.J., Knowles, S.M., Kim, S.H.J., Wang, Z., and Tobin, E.M. (2012). CCA1 and ELF3 Interact in the control of hypocotyl length and flowering time in Arabidopsis. Plant Physiol. 158: 1079-1088.
36. Más, P., Alabadí, D., Yanovsky, M.J., Oyama, T., and Kay, S.A. (2003). Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell 15: 223-236.
37. McClung, C.R., and Davis, S.J. (2010). Ambient thermometers in plants: From physiological outputs towards mechanisms of thermal sensing. Curr. Biol. 20: R1086-R1092.
38. Michael, T.P., Salomé, P.A., and McClung, C.R. (2003). Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc. Natl. Acad. Sci. USA 100: 6878-6883.
39. Mullen, J.L., Weinig, C., and Hangarter, R.P. (2006). Shade avoidance and the regulation of leaf inclination in Arabidopsis. Plant Cell Environ. 29: 1099-1106.
40. Nakamichi, N., Kiba, T., Henriques, R., Mizuno, T., Chua, N.H., and Sakakibara, H. (2010). PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22: 594-605.
41. Niwa, Y., Yamashino, T., and Mizuno, T. (2009). The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant Cell Physiol. 50: 838-854.
42. 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.
43. Nusinow, D.A., Helfer, A., Hamilton, E.E., King, J.J., Imaizumi, T., Schultz, T.F., Farré, E.M., and Kay, S.A. (2011). The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475: 398-402.
44. O'Connor, T.R., Dyreson, C., and Wyrick, J.J. (2005). Athena: A resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21: 4411-4413.
45. Oravecz, A., Baumann, A., Máté, Z., Brzezinska, A., Molinier, J., Oakeley, E.J., Adám, E., Schäfer, E., Nagy, F., and Ulm, R. (2006). CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell 18: 1975-1990.
46. Osterlund, M.T., Hardtke, C.S., Wei, N., and Deng, X.W. (2000). Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462-466.
47. Otto, B., Ohad, I., and Kloppstech, K. (1992). Temperature treatments of dark-grown pea seedlings cause an accelerated greening in the light at different levels of gene expression. Plant Mol. Biol. 18: 887-896.
48. Pokhilko, A., Fernández, A.P., Edwards, K.D., Southern, M.M., Halliday, K.J., and Millar, A.J. (2012). The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol. Syst. Biol. 8: 574.
49. Salomé, P.A., and McClung, C.R. (2005). PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell 17: 791-803.
50. Salomé, P.A., Xie, Q., and McClung, C.R. (2008). Circadian timekeeping during early Arabidopsis development. Plant Physiol. 147: 1110-1125.
51. 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.
52. Somers, D.E., Webb, A.A.R., Pearson, M., and Kay, S.A. (1998). The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125: 485-494.
53. 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.
54. Storey, J.D., and Tibshirani, R. (2003). Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100: 9440-9445.
55. Tamaru, T., Hattori, M., Honda, K., Benjamin, I., Ozawa, T., and Takamatsu, K. (2011). Synchronization of circadian Per2 rhythms and HSF1-BMAL1:CLOCK interaction in mouse fibroblasts after short-term heat shock pulse. PLoS ONE 6: e24521.
56. 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.
57. 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.
58. Troein, C., Corellou, F., Dixon, L.E., van Ooijen, G., O'Neill, J.S., Bouget, F.Y., and Millar, A.J. (2011). Multiple light inputs to a simple clock circuit allow complex biological rhythms. Plant J. 66: 375-385.
59. Van Buskirk, E.K., Decker, P.V., and Chen, M. (2012). Photobodies in light signaling. Plant Physiol. 158: 52-60.
60. Vandenbussche, F., Vriezen, W.H., Smalle, J., Laarhoven, L.J.J., Harren, F.J.M., and Van Der Straeten, D. (2003). Ethylene and auxin control the Arabidopsis response to decreased light intensity. Plant Physiol. 133: 517-527.
61. van Zanten, M., Voesenek, L.A.C.J., Peeters, A.J.M., and Millenaar, F.F. (2009). Hormone-and light-mediated regulation of heat-induced differential petiole growth in Arabidopsis. Plant Physiol. 151: 1446-1458.
62. Wenden, B., Kozma-Bognár, L., Edwards, K.D., Hall, A.J.W., Locke, J.C.W., and Millar, A.J. (2011). Light inputs shape the Arabidopsis circadian system. Plant J. 66: 480-491.
63. Yamashino, T., Ito, S., Niwa, Y., Kunihiro, A., Nakamichi, N., and Mizuno, T. (2008). Involvement of Arabidopsis clock-associated pseudo-response regulators in diurnal oscillations of gene expression in the presence of environmental time cues. Plant Cell Physiol. 49: 1839-1850.
64. Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010). AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61: 672-685.
65. Zagotta, M.T., Hicks, K.A., Jacobs, C.I., Young, J.C., Hangarter, R.P., and Meeks-Wagner, D.R. (1996). The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J. 10: 691-702.
66. 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.