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The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana

Stefan Heckmann, Inna Lermontova, Barbara Berckmans UGent, Lieven De Veylder UGent, Helmlut Bäumlein and Ingo Schubert (2011) PLANT JOURNAL. 68(4). p.646-656
abstract
To elucidate the epigenetic maintenance mechanism for functional plant centromeres, we studied transcriptional regulation of the centromere-specific histone H3 variant CENH3 in Arabidopsis thaliana. We focused on the structure and activity of the CENH3 promoter (CENH3pro) and its regulation by E2F transcription factors. Use of CENH3pro::GUS reporter gene constructs showed that CENH3pro is active in dividing tissues, and that full expression in root meristems depends on intragenic regulatory elements within the second intron. Chromatin immunoprecipitation identified CENH3 as an E2F target gene. Transient co-expression of a CENH3pro:: GUS reporter gene construct with various E2F transcription factors in A. thaliana protoplasts showed that E2Fa and E2Fb (preferentially with dimerization protein DPb) activate CENH3pro. Stable overexpression of E2Fa and E2Fb increased the CENH3 transcript level in planta, whereas over-expression of E2Fc decreased the CENH3 transcript level. Surprisingly, mutation of the two E2F binding sites of CENH3pro, in particular the more upstream one (E2F2), caused an increase in CENH3pro activity, indicating E2F-dependent transcriptional repression. CENH3pro repression may be triggered by the interplay of typical and atypical E2Fs in a cell cycle-dependent manner, and/or by interaction of typical E2Fs with retinoblastoma-related (RBR) protein. We speculate that E2Fs are involved in differential transcriptional regulation of CENH3 versus H3, as H3 promoters lack E2F binding motifs. E2F binding motifs are also present in human and Drosophila CENH3pro regions, thus cell cycle-dependent transcriptional regulation of CENH3 may be highly conserved.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
Arabidopsis thaliana, IME/intron, E2F/DP/RBR transcription factors, kinetochore, centromere, CENH3 promoter, DIVISION, GENE-EXPRESSION, CHROMATIN REQUIRES, FOLD DOMAIN, HISTONE H3 VARIANT, CENTROMERE-SPECIFIC HISTONE, RETINOBLASTOMA-RELATED PROTEIN, CELL-CYCLE, PLANTS, DROSOPHILA
journal title
PLANT JOURNAL
Plant J.
volume
68
issue
4
pages
646 - 656
Web of Science type
Article
Web of Science id
000297514900007
JCR category
PLANT SCIENCES
JCR impact factor
6.16 (2011)
JCR rank
8/189 (2011)
JCR quartile
1 (2011)
ISSN
0960-7412
DOI
10.1111/j.1365-313X.2011.04715.x
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1982079
handle
http://hdl.handle.net/1854/LU-1982079
date created
2012-01-10 16:27:58
date last changed
2012-01-13 14:38:09
@article{1982079,
  abstract     = {To elucidate the epigenetic maintenance mechanism for functional plant centromeres, we studied transcriptional regulation of the centromere-specific histone H3 variant CENH3 in Arabidopsis thaliana. We focused on the structure and activity of the CENH3 promoter (CENH3pro) and its regulation by E2F transcription factors. Use of CENH3pro::GUS reporter gene constructs showed that CENH3pro is active in dividing tissues, and that full expression in root meristems depends on intragenic regulatory elements within the second intron. Chromatin immunoprecipitation identified CENH3 as an E2F target gene. Transient co-expression of a CENH3pro:: GUS reporter gene construct with various E2F transcription factors in A. thaliana protoplasts showed that E2Fa and E2Fb (preferentially with dimerization protein DPb) activate CENH3pro. Stable overexpression of E2Fa and E2Fb increased the CENH3 transcript level in planta, whereas over-expression of E2Fc decreased the CENH3 transcript level. Surprisingly, mutation of the two E2F binding sites of CENH3pro, in particular the more upstream one (E2F2), caused an increase in CENH3pro activity, indicating E2F-dependent transcriptional repression. CENH3pro repression may be triggered by the interplay of typical and atypical E2Fs in a cell cycle-dependent manner, and/or by interaction of typical E2Fs with retinoblastoma-related (RBR) protein. We speculate that E2Fs are involved in differential transcriptional regulation of CENH3 versus H3, as H3 promoters lack E2F binding motifs. E2F binding motifs are also present in human and Drosophila CENH3pro regions, thus cell cycle-dependent transcriptional regulation of CENH3 may be highly conserved.},
  author       = {Heckmann, Stefan and Lermontova, Inna and Berckmans, Barbara and De Veylder, Lieven and B{\"a}umlein, Helmlut and Schubert, Ingo},
  issn         = {0960-7412},
  journal      = {PLANT JOURNAL},
  keyword      = {Arabidopsis thaliana,IME/intron,E2F/DP/RBR transcription factors,kinetochore,centromere,CENH3 promoter,DIVISION,GENE-EXPRESSION,CHROMATIN REQUIRES,FOLD DOMAIN,HISTONE H3 VARIANT,CENTROMERE-SPECIFIC HISTONE,RETINOBLASTOMA-RELATED PROTEIN,CELL-CYCLE,PLANTS,DROSOPHILA},
  language     = {eng},
  number       = {4},
  pages        = {646--656},
  title        = {The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana},
  url          = {http://dx.doi.org/10.1111/j.1365-313X.2011.04715.x},
  volume       = {68},
  year         = {2011},
}

Chicago
Heckmann, Stefan, Inna Lermontova, Barbara Berckmans, Lieven De Veylder, Helmlut Bäumlein, and Ingo Schubert. 2011. “The E2F Transcription Factor Family Regulates CENH3 Expression in Arabidopsis Thaliana.” Plant Journal 68 (4): 646–656.
APA
Heckmann, S., Lermontova, I., Berckmans, B., De Veylder, L., Bäumlein, H., & Schubert, I. (2011). The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. PLANT JOURNAL, 68(4), 646–656.
Vancouver
1.
Heckmann S, Lermontova I, Berckmans B, De Veylder L, Bäumlein H, Schubert I. The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. PLANT JOURNAL. 2011;68(4):646–56.
MLA
Heckmann, Stefan, Inna Lermontova, Barbara Berckmans, et al. “The E2F Transcription Factor Family Regulates CENH3 Expression in Arabidopsis Thaliana.” PLANT JOURNAL 68.4 (2011): 646–656. Print.