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The Arabidopsis CBF Gene Family Is Composed of Three
Genes Encoding AP2 Domain-Containing Proteins Whose Expression Is
Regulated by Low Temperature but Not by Abscisic Acid or
Dehydration1
Joaquín Medina,
Mónica Bargues,
Javier Terol,
Manuel Pérez-Alonso, and
Julio Salinas*
Departamento de Mejora Genética y Biotecnología,
Instituto Nacional de Investigaciones Agrarias y Alimentarias,
Carretera de la Coruña, Km. 7, 28040 Madrid, Spain (J.M., J.S.); and Departamento de Genética, Universidad de Valencia, 46100 Burjasot, Spain (M.B., J.T., M.P.-A.)
We have identified two genes from
Arabidopsis that show high similarity with
CBF1, a gene encoding an AP2 domain-containing transcriptional activator that binds to the low-temperature-responsive element CCGAC and induces the expression of some cold-regulated genes,
increasing plant freezing tolerance. These two genes, which we have
named CBF2 and CBF3, also encode proteins
containing AP2 DNA-binding motifs. Furthermore, like CBF1, CBF2 and
CBF3 proteins also include putative nuclear-localization signals and
potential acidic activation domains. The CBF2 and
CBF3 genes are linked to CBF1,
constituting a cluster on the bottom arm of chromosome IV. The high
level of similarity among the three CBF genes, their tandem organization, and the fact that they have the same
transcriptional orientation all suggest a common origin.
CBF1, CBF2, and CBF3 show
identical expression patterns, being induced very rapidly by
low-temperature treatment. However, in contrast to most of the
cold-induced plant genes characterized, they are not responsive to
abscisic acid or dehydration. Taken together, all of these data suggest
that CBF2 and CBF3 may function as
transcriptional activators, controlling the level of low-temperature
gene expression and promoting freezing tolerance through an abscisic
acid-independent pathway.
1
This work was supported by research contract no.
BIO-CT96-0101 from the European Union to J.S.
*
Corresponding author; e-mail salinas{at}inia.es; fax
34-91- 357-3107.
Plant Physiol. (1999) 119: 463-470
Copyright Clearance Center: 0032-0889/99/119//08
© 1999 American Society of Plant Physiologists
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|
 |
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[Full Text]
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
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|
 |
 
H. Lee, L. Xiong, Z. Gong, M. Ishitani, B. Stevenson, and J.-K. Zhu
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[Abstract]
[Full Text]
|
 |
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|
 |

|
 |
 
J. Medina, R. Catalá, and J. Salinas
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Plant Physiology,
April 1, 2001;
125(4):
1655 - 1666.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
S. Y. Fujimoto, M. Ohta, A. Usui, H. Shinshi, and M. Ohme-Takagi
Arabidopsis Ethylene-Responsive Element Binding Factors Act as Transcriptional Activators or Repressors of GCC Box-Mediated Gene Expression
PLANT CELL,
March 1, 2000;
12(3):
393 - 404.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
E. Kanaya, N. Nakajima, K. Morikawa, K. Okada, and Y. Shimura
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J. Biol. Chem.,
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274(23):
16068 - 16076.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|