First published online January 11, 2006; 10.1104/pp.105.073783
Plant Physiology 140:411-432 (2006)
© 2006 American Society of Plant Biologists
GENOME ANALYSIS
Genome-Wide Analysis of the ERF Gene Family in Arabidopsis and Rice[W]
Toshitsugu Nakano1,
Kaoru Suzuki1,
Tatsuhito Fujimura and
Hideaki Shinshi*
Molecular and Cellular Breeding Research Group, Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki 3058566, Japan (T.N., K.S., H.S.); and Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 3058672, Japan (T.N., T.F.)
Genes in the ERF family encode transcriptional regulators with a variety of functions involved in the developmental and physiological processes in plants. In this study, a comprehensive computational analysis identified 122 and 139 ERF family genes in Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa L. subsp. japonica), respectively. A complete overview of this gene family in Arabidopsis is presented, including the gene structures, phylogeny, chromosome locations, and conserved motifs. In addition, a comparative analysis between these genes in Arabidopsis and rice was performed. As a result of these analyses, the ERF families in Arabidopsis and rice were divided into 12 and 15 groups, respectively, and several of these groups were further divided into subgroups. Based on the observation that 11 of these groups were present in both Arabidopsis and rice, it was concluded that the major functional diversification within the ERF family predated the monocot/dicot divergence. In contrast, some groups/subgroups are species specific. We discuss the relationship between the structure and function of the ERF family proteins based on these results and published information. It was further concluded that the expansion of the ERF family in plants might have been due to chromosomal/segmental duplication and tandem duplication, as well as more ancient transposition and homing. These results will be useful for future functional analyses of the ERF family genes.
1 These authors contributed equally to the paper.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Hideaki Shinshi (h.shinshi{at}aist.go.jp).
[W] The online version of this article contains Web-only data.
www.plantphysiol.org/cgi/doi/10.1104/pp.105.073783.
* Corresponding author; e-mail h.shinshi{at}aist.go.jp; fax 81298616090.
Received November 7, 2005;
returned for revision December 5, 2005;
accepted December 14, 2005.
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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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April 1, 2008;
146(4):
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|
 |
|

|
 |

|
 |
 
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March 11, 2008;
105(10):
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[Full Text]
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|
 |
|

|
 |

|
 |
 
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March 1, 2008;
59(4):
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[Full Text]
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|
 |
|

|
 |

|
 |
 
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March 1, 2008;
146(3):
1305 - 1321.
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|
 |
|

|
 |

|
 |
 
R.-C. Lin, H.-J. Park, and H.-Y. Wang
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January 1, 2008;
1(1):
42 - 57.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Gong, K. He, M. Covington, S. P. Dinesh-Kumar, M. Snyder, S. L. Harmer, Y.-X. Zhu, and X. W. Deng
The Development of Protein Microarrays and Their Applications in DNA-Protein and Protein-Protein Interaction Analyses of Arabidopsis Transcription Factors
Mol Plant,
January 1, 2008;
1(1):
27 - 41.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Rohde, T. Ruttink, V. Hostyn, L. Sterck, K. Van Driessche, and W. Boerjan
Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar
J. Exp. Bot.,
December 1, 2007;
58(15-16):
4047 - 4060.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Wang, D. Tan, A. Takahashi, T. Zhong Li, and T. Harada
MdERFs, two ethylene-response factors involved in apple fruit ripening
J. Exp. Bot.,
October 1, 2007;
58(13):
3743 - 3748.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Karaba, S. Dixit, R. Greco, A. Aharoni, K. R. Trijatmiko, N. Marsch-Martinez, A. Krishnan, K. N. Nataraja, M. Udayakumar, and A. Pereira
Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene
PNAS,
September 25, 2007;
104(39):
15270 - 15275.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Andriankaja, A. Boisson-Dernier, L. Frances, L. Sauviac, A. Jauneau, D. G. Barker, and F. de Carvalho-Niebel
AP2-ERF Transcription Factors Mediate Nod Factor Dependent Mt ENOD11 Activation in Root Hairs via a Novel cis-Regulatory Motif
PLANT CELL,
September 1, 2007;
19(9):
2866 - 2885.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Ruttink, M. Arend, K. Morreel, V. Storme, S. Rombauts, J. Fromm, R. P. Bhalerao, W. Boerjan, and A. Rohde
A Molecular Timetable for Apical Bud Formation and Dormancy Induction in Poplar
PLANT CELL,
August 1, 2007;
19(8):
2370 - 2390.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Lasanthi-Kudahettige, L. Magneschi, E. Loreti, S. Gonzali, F. Licausi, G. Novi, O. Beretta, F. Vitulli, A. Alpi, and P. Perata
Transcript Profiling of the Anoxic Rice Coleoptile
Plant Physiology,
May 1, 2007;
144(1):
218 - 231.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Kannangara, C. Branigan, Y. Liu, T. Penfield, V. Rao, G. Mouille, H. Hofte, M. Pauly, J. L. Riechmann, and P. Broun
The Transcription Factor WIN1/SHN1 Regulates Cutin Biosynthesis in Arabidopsis thaliana
PLANT CELL,
April 1, 2007;
19(4):
1278 - 1294.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. H. Middleton, J. Jakab, R. V. Penmetsa, C. G. Starker, J. Doll, P. Kalo, R. Prabhu, J. F. Marsh, R. M. Mitra, A. Kereszt, et al.
An ERF Transcription Factor in Medicago truncatula That Is Essential for Nod Factor Signal Transduction
PLANT CELL,
April 1, 2007;
19(4):
1221 - 1234.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Cavalcante, C Vargas, E. Nogueira, F Vinagre, K Schwarcz, J. Baldani, P. Ferreira, and A. Hemerly
Members of the ethylene signalling pathway are regulated in sugarcane during the association with nitrogen-fixing endophytic bacteria
J. Exp. Bot.,
February 1, 2007;
58(3):
673 - 686.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Onate-Sanchez, J. P. Anderson, J. Young, and K. B. Singh
AtERF14, a Member of the ERF Family of Transcription Factors, Plays a Nonredundant Role in Plant Defense
Plant Physiology,
January 1, 2007;
143(1):
400 - 409.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. Kellogg
Progress and challenges in studies of the evolution of development
J. Exp. Bot.,
October 1, 2006;
57(13):
3505 - 3516.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. A. Tuskan, S. DiFazio, S. Jansson, J. Bohlmann, I. Grigoriev, U. Hellsten, N. Putnam, S. Ralph, S. Rombauts, A. Salamov, et al.
The genome of black cottonwood, Populus trichocarpa (Torr. & Gray).
Science,
September 15, 2006;
313(5793):
1596 - 1604.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. Li, X. Duan, H. Jiang, Y. Sun, Y. Tang, Z. Yuan, J. Guo, W. Liang, L. Chen, J. Yin, et al.
Genome-Wide Analysis of Basic/Helix-Loop-Helix Transcription Factor Family in Rice and Arabidopsis
Plant Physiology,
August 1, 2006;
141(4):
1167 - 1184.
[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]
|
 |
|
|
|