The Plant Cell, Vol. 14, 1541-1555,
July 2002, Copyright © 2002,
American Society of Plant Biologists
Nucleocytoplasmic Partitioning of the Plant Photoreceptors Phytochrome A, B, C, D, and E Is Regulated Differentially by Light and Exhibits a Diurnal Rhythm
Stefan Kirchera,
Patricia Gila,
László Kozma-Bognárb,
Erzsébet Fejesb,
Volker Spetha,
Tania Husselstein-Mullera,
Diana Bauera,
Éva Ádámb,
Eberhard Schäfer1,a and
Ferenc Nagy1,a,b,c
a Albert-Ludwigs-Universität Freiburg, Institut für Biologie II/Botanik, Schänzlestrasse 1, 79104 Freiburg, Germany
b Institute of Plant Biology, Biological Research Centre, Temesvári krt 62, H-6726 Szeged, Hungary
c Institute of Plant Biology, Agricultural Biotechnological Centre, Szent-Gyorgyi A 4, H-2101 Godollo, Hungary
1 To whom correspondence should be addressed. E-mail schaegen{at}ruf.uni-freiburg.de; fax 49-761-2032629 or e-mail nagyf{at}nucleus.szbk.u-szeged.hu; fax 36-62-433434
The phytochrome family of plant photoreceptors has a central role in the adaptation of plant development to changes in ambient light conditions. The individual phytochrome species regulate different or partly overlapping physiological responses. We generated transgenic Arabidopsis plants expressing phytochrome A to E:green fluorescent protein (GFP) fusion proteins to assess the biological role of intracellular compartmentation of these photoreceptors in light-regulated signaling. We show that all phytochrome:GFP fusion proteins were imported into the nuclei. Translocation of these photoreceptors into the nuclei was regulated differentially by light. Light-induced accumulation of phytochrome species in the nuclei resulted in the formation of speckles. The appearance of these nuclear structures exhibited distinctly different kinetics, wavelengths, and fluence dependence and was regulated by a diurnal rhythm. Furthermore, we demonstrate that the import of mutant phytochrome B:GFP and phytochrome A:GFP fusion proteins, shown to be defective in signaling in vivo, is regulated by light but is not accompanied by the formation of speckles. These results suggest that (1) the differential regulation of the translocation of phytochrome A to E into nuclei plays a role in the specification of functions, and (2) the appearance of speckles is a functional feature of phytochrome-regulated signaling.
This article has been cited by other articles:

|
 |

|
 |
 
J. Kneissl, V. Wachtler, N.-H. Chua, and C. Bolle
OWL1: An Arabidopsis J-Domain Protein Involved in Perception of Very Low Light Fluences
PLANT CELL,
October 1, 2009;
21(10):
3212 - 3225.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Muller, A. P. Fernandez, A. Hiltbrunner, E. Schafer, and T. Kretsch
The Histidine Kinase-Related Domain of Arabidopsis Phytochrome A Controls the Spectral Sensitivity and the Subcellular Distribution of the Photoreceptor
Plant Physiology,
July 1, 2009;
150(3):
1297 - 1309.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Clack, A. Shokry, M. Moffet, P. Liu, M. Faul, and R. A. Sharrock
Obligate Heterodimerization of Arabidopsis Phytochromes C and E and Interaction with the PIF3 Basic Helix-Loop-Helix Transcription Factor
PLANT CELL,
March 1, 2009;
21(3):
786 - 799.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Mallappa, A. Singh, H. Ram, and S. Chattopadhyay
GBF1, a Transcription Factor of Blue Light Signaling in Arabidopsis, Is Degraded in the Dark by a Proteasome-mediated Pathway Independent of COP1 and SPA1
J. Biol. Chem.,
December 19, 2008;
283(51):
35772 - 35782.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. C. Wollenberg, B. Strasser, P. D. Cerdan, and R. M. Amasino
Acceleration of Flowering during Shade Avoidance in Arabidopsis Alters the Balance between FLOWERING LOCUS C-Mediated Repression and Photoperiodic Induction of Flowering
Plant Physiology,
November 1, 2008;
148(3):
1681 - 1694.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Lee, H.-S. Lee, J.-S. Lee, S.-K. Kim, and S.-H. Kim
Hormone- and light-regulated nucleocytoplasmic transport in plants: current status
J. Exp. Bot.,
September 1, 2008;
59(12):
3229 - 3245.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Shen, L. Zhu, A. Castillon, M. Majee, B. Downie, and E. Huq
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,
June 1, 2008;
20(6):
1586 - 1602.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. H. Kim, S. Yamaguchi, S. Lim, E. Oh, J. Park, A. Hanada, Y. Kamiya, and G. Choi
SOMNUS, a CCCH-Type Zinc Finger Protein in Arabidopsis, Negatively Regulates Light-Dependent Seed Germination Downstream of PIL5
PLANT CELL,
May 1, 2008;
20(5):
1260 - 1277.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Bhatia, S. N. Gangappa, R. Kushwaha, S. Kundu, and S. Chattopadhyay
SHORT HYPOCOTYL IN WHITE LIGHT1, a Serine-Arginine-Aspartate-Rich Protein in Arabidopsis, Acts as a Negative Regulator of Photomorphogenic Growth
Plant Physiology,
May 1, 2008;
147(1):
169 - 178.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-s. Hwang and P. H. Quail
Phytochrome-Regulated PIL1 Derepression is Developmentally Modulated
Plant Cell Physiol.,
April 1, 2008;
49(4):
501 - 511.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Leivar, E. Monte, B. Al-Sady, C. Carle, A. Storer, J. M. Alonso, J. R. Ecker, and P. H. Quail
The Arabidopsis Phytochrome-Interacting Factor PIF7, Together with PIF3 and PIF4, Regulates Responses to Prolonged Red Light by Modulating phyB Levels
PLANT CELL,
February 1, 2008;
20(2):
337 - 352.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Kevei, E. Schafer, and F. Nagy
Light-regulated nucleo-cytoplasmic partitioning of phytochromes
J. Exp. Bot.,
September 27, 2007;
(2007)
erm145v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Monte, B. Al-Sady, P. Leivar, and P. H. Quail
Out of the dark: how the PIFs are unmasking a dual temporal mechanism of phytochrome signalling
J. Exp. Bot.,
September 12, 2007;
(2007)
erm186v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. F. Devlin, J. M. Christie, and M. J. Terry
Many hands make light work
J. Exp. Bot.,
September 1, 2007;
58(12):
3071 - 3077.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Mira-Rodado, U. Sweere, C. Grefen, T. Kunkel, E. Fejes, F. Nagy, E. Schafer, and K. Harter
Functional cross-talk between two-component and phytochrome B signal transduction in Arabidopsis
J. Exp. Bot.,
July 1, 2007;
58(10):
2595 - 2607.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-s. Su and J. C. Lagarias
Light-Independent Phytochrome Signaling Mediated by Dominant GAF Domain Tyrosine Mutants of Arabidopsis Phytochromes in Transgenic Plants
PLANT CELL,
July 1, 2007;
19(7):
2124 - 2139.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. S. Ali and A. S. N. Reddy
ATP, phosphorylation and transcription regulate the mobility of plant splicing factors
J. Cell Sci.,
September 1, 2006;
119(17):
3527 - 3538.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Hiltbrunner, A. Tscheuschler, A. Viczian, T. Kunkel, S. Kircher, and E. Schafer
FHY1 and FHL Act Together to Mediate Nuclear Accumulation of the Phytochrome A Photoreceptor
Plant Cell Physiol.,
August 1, 2006;
47(8):
1023 - 1034.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Roig-Villanova, J. Bou, C. Sorin, P. F. Devlin, and J. F. Martinez-Garcia
Identification of Primary Target Genes of Phytochrome Signaling. Early Transcriptional Control during Shade Avoidance Responses in Arabidopsis
Plant Physiology,
May 1, 2006;
141(1):
85 - 96.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Datta, G.H.C.M. Hettiarachchi, X.-W. Deng, and M. Holm
Arabidopsis CONSTANS-LIKE3 Is a Positive Regulator of Red Light Signaling and Root Growth
PLANT CELL,
January 1, 2006;
18(1):
70 - 84.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. C. Froehlich, B. Noh, R. D. Vierstra, J. Loros, and J. C. Dunlap
Genetic and Molecular Analysis of Phytochromes from the Filamentous Fungus Neurospora crassa
Eukaryot. Cell,
December 1, 2005;
4(12):
2140 - 2152.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Shen, S. Feng, L. Ma, R. Lin, L.-J. Qu, Z. Chen, H. Wang, and X. W. Deng
Arabidopsis FHY1 Protein Stability Is Regulated by Light via Phytochrome A and 26S Proteasome
Plant Physiology,
November 1, 2005;
139(3):
1234 - 1243.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Fukamatsu, S. Mitsui, M. Yasuhara, Y. Tokioka, N. Ihara, S. Fujita, and T. Kiyosue
Identification of LOV KELCH PROTEIN2 (LKP2)-interacting Factors That Can Recruit LKP2 to Nuclear Bodies
Plant Cell Physiol.,
August 1, 2005;
46(8):
1340 - 1349.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. P. Fernandez, P. Gil, I. Valkai, F. Nagy, and E. Schafer
Analysis of the Function of the Photoreceptors Phytochrome B and Phytochrome D in Nicotiana plumbaginifolia and Arabidopsis thaliana
Plant Cell Physiol.,
May 1, 2005;
46(5):
790 - 796.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Shen, J.-I. Kim, and P.-S. Song
NDPK2 as a Signal Transducer in the Phytochrome-mediated Light Signaling
J. Biol. Chem.,
February 18, 2005;
280(7):
5740 - 5749.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. F. Pendle, G. P. Clark, R. Boon, D. Lewandowska, Y. W. Lam, J. Andersen, M. Mann, A. I. Lamond, J. W. S. Brown, and P. J. Shaw
Proteomic Analysis of the Arabidopsis Nucleolus Suggests Novel Nucleolar Functions
Mol. Biol. Cell,
January 1, 2005;
16(1):
260 - 269.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Khanna, E. Huq, E. A. Kikis, B. Al-Sady, C. Lanzatella, and P. H. Quail
A Novel Molecular Recognition Motif Necessary for Targeting Photoactivated Phytochrome Signaling to Specific Basic Helix-Loop-Helix Transcription Factors
PLANT CELL,
November 1, 2004;
16(11):
3033 - 3044.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Oh, J. Kim, E. Park, J.-I. Kim, C. Kang, and G. Choi
PIL5, a Phytochrome-Interacting Basic Helix-Loop-Helix Protein, Is a Key Negative Regulator of Seed Germination in Arabidopsis thaliana
PLANT CELL,
November 1, 2004;
16(11):
3045 - 3058.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Huq, B. Al-Sady, M. Hudson, C. Kim, K. Apel, and P. H. Quail
PHYTOCHROME-INTERACTING FACTOR 1 Is a Critical bHLH Regulator of Chlorophyll Biosynthesis
Science,
September 24, 2004;
305(5692):
1937 - 1941.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Mittmann, G. Brucker, M. Zeidler, A. Repp, T. Abts, E. Hartmann, and J. Hughes
Targeted knockout in Physcomitrella reveals direct actions of phytochrome in the cytoplasm
PNAS,
September 21, 2004;
101(38):
13939 - 13944.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Laubinger, K. Fittinghoff, and U. Hoecker
The SPA Quartet: A Family of WD-Repeat Proteins with a Central Role in Suppression of Photomorphogenesis in Arabidopsis
PLANT CELL,
September 1, 2004;
16(9):
2293 - 2306.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Park, J. Kim, Y. Lee, J. Shin, E. Oh, W.-I. Chung, J. R. Liu, and G. Choi
Degradation of Phytochrome Interacting Factor 3 in Phytochrome-Mediated Light Signaling
Plant Cell Physiol.,
August 15, 2004;
45(8):
968 - 975.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. Sharrock and T. Clack
Heterodimerization of type II phytochromes in Arabidopsis
PNAS,
August 3, 2004;
101(31):
11500 - 11505.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Oka, T. Matsushita, N. Mochizuki, T. Suzuki, S. Tokutomi, and A. Nagatani
Functional Analysis of a 450-Amino Acid N-Terminal Fragment of Phytochrome B in Arabidopsis
PLANT CELL,
August 1, 2004;
16(8):
2104 - 2116.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Sheehan, P. R. Farmer, and T. P. Brutnell
Structure and Expression of Maize Phytochrome Family Homeologs
Genetics,
July 1, 2004;
167(3):
1395 - 1405.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. M. Folta
Green Light Stimulates Early Stem Elongation, Antagonizing Light-Mediated Growth Inhibition
Plant Physiology,
July 1, 2004;
135(3):
1407 - 1416.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. K.-Y. Ng, T. Kinoshita, S. Pandey, K.-i. Shimazaki, and S. M. Assmann
Abscisic Acid Induces Rapid Subnuclear Reorganization in Guard Cells
Plant Physiology,
April 1, 2004;
134(4):
1327 - 1331.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. S. Seo, E. Watanabe, S. Tokutomi, A. Nagatani, and N.-H. Chua
Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling
Genes & Dev.,
March 15, 2004;
18(6):
617 - 622.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. M. Parks
The Red Side of Photomorphogenesis
Plant Physiology,
December 1, 2003;
133(4):
1437 - 1444.
[Full Text]
|
 |
|

|
 |

|
 |
 
P. Lariguet, H. E. Boccalandro, J. M. Alonso, J. R. Ecker, J. Chory, J. J. Casal, and C. Fankhauser
A Growth Regulatory Loop That Provides Homeostasis to Phytochrome A Signaling
PLANT CELL,
December 1, 2003;
15(12):
2966 - 2978.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Chen, R. Schwab, and J. Chory
Characterization of the requirements for localization of phytochrome B to nuclear bodies
PNAS,
November 25, 2003;
100(24):
14493 - 14498.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Monte, J. M. Alonso, J. R. Ecker, Y. Zhang, X. Li, J. Young, S. Austin-Phillips, and P. H. Quail
Isolation and Characterization of phyC Mutants in Arabidopsis Reveals Complex Crosstalk between Phytochrome Signaling Pathways
PLANT CELL,
September 1, 2003;
15(9):
1962 - 1980.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. J. Millar
A Suite of Photoreceptors Entrains the Plant Circadian Clock
J Biol Rhythms,
June 1, 2003;
18(3):
217 - 226.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Eriksson and A. J. Millar
The Circadian Clock. A Plant's Best Friend in a Spinning World
Plant Physiology,
June 1, 2003;
132(2):
732 - 738.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. J. Halliday and G. C. Whitelam
Changes in Photoperiod or Temperature Alter the Functional Relationships between Phytochromes and Reveal Roles for phyD and phyE
Plant Physiology,
April 1, 2003;
131(4):
1913 - 1920.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|