First published online February 18, 2004; 10.1105/tpc.018978
The Plant Cell 16:658-671 (2004)
© 2004 American Society of Plant Biologists
Type-A Arabidopsis Response Regulators Are Partially Redundant Negative Regulators of Cytokinin Signaling
Jennifer P.C. Toa,1,
Georg Haberera,1,2,
Fernando J. Ferreiraa,
Jean Deruèrea,
Michael G. Masonb,3,
G. Eric Schallerb,3,
Jose M. Alonsoc,4,
Joseph R. Eckerc and
Joseph J. Kiebera,5
a Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599
b Department of Biochemistry and Molecular Biology, University of New Hampshire, Durham, New Hampshire 03824
c Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, California 92037
5 To whom correspondence should be addressed. E-mail jkieber{at}unc.edu; fax 919-962-1625.
Type-A Arabidopsis (Arabidopsis thaliana) response regulators (ARRs) are a family of 10 genes that are rapidly induced by cytokinin and are highly similar to bacterial two-component response regulators. We have isolated T-DNA insertions in six of the type-A ARRs and constructed multiple insertional mutants, including the arr3,4,5,6,8,9 hextuple mutant. Single arr mutants were indistinguishable from the wild type in various cytokinin assays; double and higher order arr mutants showed progressively increasing sensitivity to cytokinin, indicating functional overlap among type-A ARRs and that these genes act as negative regulators of cytokinin responses. The induction of cytokinin primary response genes was amplified in arr mutants, indicating that the primary response to cytokinin is affected. Spatial patterns of ARR gene expression were consistent with partially redundant function of these genes in cytokinin signaling. The arr mutants show altered red light sensitivity, suggesting a general involvement of type-A ARRs in light signal transduction. Further, morphological phenotypes of some arr mutants suggest complex regulatory interactions and gene-specific functions among family members.
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|
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|
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|
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|
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|
 |
|

|
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|
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|
 |
|

|
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|
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|
 |
|

|
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|
 |
 
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|
 |
|

|
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|
 |
|

|
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|
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|
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|

|
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|
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|
 |
|

|
 |

|
 |
 
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(2007)
erm236v1.
[Abstract]
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|
 |
|

|
 |

|
 |
 
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Arabidopsis Cytokinin Signaling Pathway
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2007(407):
cm5 - cm5.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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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]
|
 |
|

|
 |

|
 |
 
N. Hirose, N. Makita, M. Kojima, T. Kamada-Nobusada, and H. Sakakibara
Overexpression of a Type-A Response Regulator Alters Rice Morphology and Cytokinin Metabolism
Plant Cell Physiol.,
March 1, 2007;
48(3):
523 - 539.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Taniguchi, N. Sasaki, T. Tsuge, T. Aoyama, and A. Oka
ARR1 Directly Activates Cytokinin Response Genes that Encode Proteins with Diverse Regulatory Functions
Plant Cell Physiol.,
February 1, 2007;
48(2):
263 - 277.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Yokoyama, T. Yamashino, Y.-I. Amano, Y. Tajima, A. Imamura, H. Sakakibara, and T. Mizuno
Type-B ARR Transcription Factors, ARR10 and ARR12, are Implicated in Cytokinin-Mediated Regulation of Protoxylem Differentiation in Roots of Arabidopsis thaliana
Plant Cell Physiol.,
January 1, 2007;
48(1):
84 - 96.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Hanano, M. A. Domagalska, F. Nagy, and S. J. Davis
Multiple phytohormones influence distinct parameters of the plant circadian clock
Genes Cells,
December 1, 2006;
11(12):
1381 - 1392.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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November 1, 2006;
47(11):
1443 - 1456.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. E. Hutchison, J. Li, C. Argueso, M. Gonzalez, E. Lee, M. W. Lewis, B. B. Maxwell, T. D. Perdue, G. E. Schaller, J. M. Alonso, et al.
The Arabidopsis Histidine Phosphotransfer Proteins Are Redundant Positive Regulators of Cytokinin Signaling
PLANT CELL,
November 1, 2006;
18(11):
3073 - 3087.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Gonzalez-Rizzo, M. Crespi, and F. Frugier
The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti
PLANT CELL,
October 1, 2006;
18(10):
2680 - 2693.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Sakamoto, H. Sakakibara, M. Kojima, Y. Yamamoto, H. Nagasaki, Y. Inukai, Y. Sato, and M. Matsuoka
Ectopic Expression of KNOTTED1-Like Homeobox Protein Induces Expression of Cytokinin Biosynthesis Genes in Rice
Plant Physiology,
September 1, 2006;
142(1):
54 - 62.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Rashotte, M. G. Mason, C. E. Hutchison, F. J. Ferreira, G. E. Schaller, and J. J. Kieber
A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway
PNAS,
July 18, 2006;
103(29):
11081 - 11085.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Che, S. Lall, D. Nettleton, and S. H. Howell
Gene Expression Programs during Shoot, Root, and Callus Development in Arabidopsis Tissue Culture
Plant Physiology,
June 1, 2006;
141(2):
620 - 637.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. S. Pischke, E. L. Huttlin, A. D. Hegeman, and M. R. Sussman
A Transcriptome-Based Characterization of Habituation in Plant Tissue Culture
Plant Physiology,
April 1, 2006;
140(4):
1255 - 1278.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. J. Kim, H. Ryu, S. H. Hong, H. R. Woo, P. O. Lim, I. C. Lee, J. Sheen, H. G. Nam, and I. Hwang
Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis
PNAS,
January 17, 2006;
103(3):
814 - 819.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. A. Salome, J. P.C. To, J. J. Kieber, and C. R. McClung
Arabidopsis Response Regulators ARR3 and ARR4 Play Cytokinin-Independent Roles in the Control of Circadian Period
PLANT CELL,
January 1, 2006;
18(1):
55 - 69.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Riefler, O. Novak, M. Strnad, and T. Schmulling
Arabidopsis Cytokinin Receptor Mutants Reveal Functions in Shoot Growth, Leaf Senescence, Seed Size, Germination, Root Development, and Cytokinin Metabolism
PLANT CELL,
January 1, 2006;
18(1):
40 - 54.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. G. Mason, D. E. Mathews, D. A. Argyros, B. B. Maxwell, J. J. Kieber, J. M. Alonso, J. R. Ecker, and G. E. Schaller
Multiple Type-B Response Regulators Mediate Cytokinin Signal Transduction in Arabidopsis
PLANT CELL,
November 1, 2005;
17(11):
3007 - 3018.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. M. Ellis, P. Nagpal, J. C. Young, G. Hagen, T. J. Guilfoyle, and J. W. Reed
AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana
Development,
October 15, 2005;
132(20):
4563 - 4574.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Cutler and P. McCourt
Dude, Where's My Phenotype? Dealing with Redundancy in Signaling Networks
Plant Physiology,
June 1, 2005;
138(2):
558 - 559.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Franco-Zorrilla, A. C. Martin, A. Leyva, and J. Paz-Ares
Interaction between Phosphate-Starvation, Sugar, and Cytokinin Signaling in Arabidopsis and the Roles of Cytokinin Receptors CRE1/AHK4 and AHK3
Plant Physiology,
June 1, 2005;
138(2):
847 - 857.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Kiba, T. Naitou, N. Koizumi, T. Yamashino, H. Sakakibara, and T. Mizuno
Combinatorial Microarray Analysis Revealing Arabidopsis Genes Implicated in Cytokinin Responses through the His->Asp Phosphorelay Circuitry
Plant Cell Physiol.,
February 1, 2005;
46(2):
339 - 355.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Greenboim-Wainberg, I. Maymon, R. Borochov, J. Alvarez, N. Olszewski, N. Ori, Y. Eshed, and D. Weiss
Cross Talk between Gibberellin and Cytokinin: The Arabidopsis GA Response Inhibitor SPINDLY Plays a Positive Role in Cytokinin Signaling
PLANT CELL,
January 1, 2005;
17(1):
92 - 102.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Kiba, K. Aoki, H. Sakakibara, and T. Mizuno
Arabidopsis Response Regulator, ARR22, Ectopic Expression of Which Results in Phenotypes Similar to the wol Cytokinin-Receptor Mutant
Plant Cell Physiol.,
August 15, 2004;
45(8):
1063 - 1077.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Higuchi, M. S. Pischke, A. P. Mahonen, K. Miyawaki, Y. Hashimoto, M. Seki, M. Kobayashi, K. Shinozaki, T. Kato, S. Tabata, et al.
In planta functions of the Arabidopsis cytokinin receptor family
PNAS,
June 8, 2004;
101(23):
8821 - 8826.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|