Plant Cell Advance Online Publication Published on April 29, 2002; 10.1105/tpc.010425
Received October 1, 2001
Accepted February 24, 2002
Centromeric Localization and Adaptive Evolution of an Arabidopsis Histone H3 Variant
Paul B. Talbert 1, Ricardo Masuelli 2, Anand P. Tyagi 2, Luca Comai 2, and Steven Henikoff 1*
1
Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, 1100 Fairview
Avenue N, Seattle, Washington 98109-1024
2
Department of Botany, Box 355325, University of Washington, Seattle, Washington 98195
* To whom correspondence should be addressed. E-mail: steveh{at}fhcrc.org.
Centromeric H3-like histones, which replace histone H3 in the centromeric chromatin
of animals and fungi, have not been reported in plants. We identified a histone H3
variant from Arabidopsis thaliana that encodes a centromere-identifying
protein designated HTR12. By immunological detection, HTR12 localized at centromeres
in both mitotic and meiotic cells. HTR12 signal revealed tissue- and stage-specific
differences in centromere morphology, including a distended bead-like structure in
interphase root tip cells. The anti-HTR12 antibody also detected spherical organelles
in meiotic cells. Although the antibody does not label centromeres in the closely
related species Arabidopsis arenosa, HTR12 signal was found on all centromeres
in allopolyploids of these two species. Comparison of the HTR12 genes of
A. thaliana and A. arenosa revealed striking adaptive evolution
in the N-terminal tail of the protein, similar to the pattern seen in its counterpart
in Drosophila. This finding suggests that the same evolutionary forces shape
centromeric chromatin in both animals and plants.
This article has been cited by other articles:

|
 |

|
 |
 
L. Qi, B. Friebe, P. Zhang, and B. S. Gill
A Molecular-Cytogenetic Method for Locating Genes to Pericentromeric Regions Facilitates a Genomewide Comparison of Synteny Between the Centromeric Regions of Wheat and Rice
Genetics,
December 1, 2009;
183(4):
1235 - 1247.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. D. Hirsch, Y. Wu, H. Yan, and J. Jiang
Lineage-Specific Adaptive Evolution of the Centromeric Protein CENH3 in Diploid and Allotetraploid Oryza Species
Mol. Biol. Evol.,
December 1, 2009;
26(12):
2877 - 2885.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. N. Tenea, J. Spantzel, L.-Y. Lee, Y. Zhu, K. Lin, S. J. Johnson, and S. B. Gelvin
Overexpression of Several Arabidopsis Histone Genes Increases Agrobacterium-Mediated Transformation and Transgene Expression in Plants
PLANT CELL,
October 1, 2009;
21(10):
3350 - 3367.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Chen, S. Hafidh, S. H. Poh, D. Twell, and F. Berger
Proliferation and cell fate establishment during Arabidopsis male gametogenesis depends on the Retinoblastoma protein
PNAS,
April 28, 2009;
106(17):
7257 - 7262.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Murata, E. Yokota, F. Shibata, and K. Kashihara
Functional analysis of the Arabidopsis centromere by T-DNA insertion-induced centromere breakage
PNAS,
May 27, 2008;
105(21):
7511 - 7516.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Zhang, H.-R. Lee, D.-H. Koo, and J. Jiang
Epigenetic Modification of Centromeric Chromatin: Hypomethylation of DNA Sequences in the CENH3-Associated Chromatin in Arabidopsis thaliana and Maize
PLANT CELL,
January 1, 2008;
20(1):
25 - 34.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Balasubramanian, A. Karve, M. Kandasamy, R. B. Meagher, and B. d. Moore
A Role for F-Actin in Hexokinase-Mediated Glucose Signaling
Plant Physiology,
December 1, 2007;
145(4):
1423 - 1434.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Rossignol, S. Collier, M. Bush, P. Shaw, and J. H. Doonan
Arabidopsis POT1A interacts with TERT-V(I8), an N-terminal splicing variant of telomerase
J. Cell Sci.,
October 15, 2007;
120(20):
3678 - 3687.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Dalal, T. Furuyama, D. Vermaak, and S. Henikoff
Inaugural Article: Structure, dynamics, and evolution of centromeric nucleosomes
PNAS,
October 9, 2007;
104(41):
15974 - 15981.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. I. Lindhout, P. Fransz, F. Tessadori, T. Meckel, P. J.J. Hooykaas, and B. J. v. d. Zaal
Live cell imaging of repetitive DNA sequences via GFP-tagged polydactyl zinc finger proteins
Nucleic Acids Res.,
August 17, 2007;
(2007)
gkm618v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Villasante, J. P. Abad, and M. Mendez-Lago
Centromeres were derived from telomeres during the evolution of the eukaryotic chromosome
PNAS,
June 19, 2007;
104(25):
10542 - 10547.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. R. Woo, O. Pontes, C. S. Pikaard, and E. J. Richards
VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization
Genes & Dev.,
February 1, 2007;
21(3):
267 - 277.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. C. Presgraves and W. Stephan
Pervasive Adaptive Evolution among Interactors of the Drosophila Hybrid Inviability Gene, Nup96
Mol. Biol. Evol.,
January 1, 2007;
24(1):
306 - 314.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kawabe, S. Nasuda, and D. Charlesworth
Duplication of Centromeric Histone H3 (HTR12) Gene in Arabidopsis halleri and A. lyrata, Plant Species With Multiple Centromeric Satellite Sequences
Genetics,
December 1, 2006;
174(4):
2021 - 2032.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H.-R. Lee, P. Neumann, J. Macas, and J. Jiang
Transcription and Evolutionary Dynamics of the Centromeric Satellite Repeat CentO in Rice
Mol. Biol. Evol.,
December 1, 2006;
23(12):
2505 - 2520.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. E. Baker and K. Rogers
Phylogenetic Analysis of Fungal Centromere H3 Proteins
Genetics,
November 1, 2006;
174(3):
1481 - 1492.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Lermontova, V. Schubert, J. Fuchs, S. Klatte, J. Macas, and I. Schubert
Loading of Arabidopsis Centromeric Histone CENH3 Occurs Mainly during G2 and Requires the Presence of the Histone Fold Domain
PLANT CELL,
October 1, 2006;
18(10):
2443 - 2451.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Yi, N. Sardesai, T. Fujinuma, C.-W. Chan, Veena, and S. B. Gelvin
Constitutive Expression Exposes Functional Redundancy between the Arabidopsis Histone H2A Gene HTA1 and Other H2A Gene Family Members
PLANT CELL,
July 1, 2006;
18(7):
1575 - 1589.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. E. Hall, G. C. Kettler, and D. Preuss
Dynamic evolution at pericentromeres
Genome Res.,
March 1, 2006;
16(3):
355 - 364.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Ma and J. L. Bennetzen
Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice
PNAS,
January 10, 2006;
103(2):
383 - 388.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. D. Cervantes, X. Xi, D. Vermaak, M.-C. Yao, and H. S. Malik
The CNA1 Histone of the Ciliate Tetrahymena thermophila Is Essential for Chromosome Segregation in the Germline Micronucleus
Mol. Biol. Cell,
January 1, 2006;
17(1):
485 - 497.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. T. GRANT-DOWNTON and H. G. DICKINSON
Epigenetics and its Implications for Plant Biology. 1. The Epigenetic Network in Plants
Ann. Bot.,
December 1, 2005;
96(7):
1143 - 1164.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Fang and D. L. Spector
Centromere Positioning and Dynamics in Living Arabidopsis Plants
Mol. Biol. Cell,
December 1, 2005;
16(12):
5710 - 5718.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. A. Collins, A. R. Castillo, S. Y. Tatsutani, and S. Biggins
De Novo Kinetochore Assembly Requires the Centromeric Histone H3 Variant
Mol. Biol. Cell,
December 1, 2005;
16(12):
5649 - 5660.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Heeger, O. Leismann, R. Schittenhelm, O. Schraidt, S. Heidmann, and C. F. Lehner
Genetic interactions of separase regulatory subunits reveal the diverged Drosophila Cenp-C homolog
Genes & Dev.,
September 1, 2005;
19(17):
2041 - 2053.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Zhang, C. Yi, W. Bao, B. Liu, J. Cui, H. Yu, X. Cao, M. Gu, M. Liu, and Z. Cheng
The Transcribed 165-bp CentO Satellite Is the Major Functional Centromeric Element in the Wild Rice Species Oryza punctata
Plant Physiology,
September 1, 2005;
139(1):
306 - 315.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H.-R. Lee, W. Zhang, T. Langdon, W. Jin, H. Yan, Z. Cheng, and J. Jiang
From The Cover: Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species
PNAS,
August 16, 2005;
102(33):
11793 - 11798.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. E. Hall, S. Luo, A. E. Hall, and D. Preuss
Differential Rates of Local and Global Homogenization in Centromere Satellites From Arabidopsis Relatives
Genetics,
August 1, 2005;
170(4):
1913 - 1927.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Nagaki, K. Kashihara, and M. Murata
Visualization of Diffuse Centromeres with Centromere-Specific Histone H3 in the Holocentric Plant Luzula nivea
PLANT CELL,
July 1, 2005;
17(7):
1886 - 1893.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Jin, J. C. Lamb, J. M. Vega, R. K. Dawe, J. A. Birchler, and J. Jiang
Molecular and Functional Dissection of the Maize B Chromosome Centromere
PLANT CELL,
May 1, 2005;
17(5):
1412 - 1423.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. J. O'Neill, M. D. B. Eldridge, and C. J. Metcalfe
Centromere Dynamics and Chromosome Evolution in Marsupials
J. Hered.,
September 1, 2004;
95(5):
375 - 381.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. L. Cooper and S. Henikoff
Adaptive Evolution of the Histone Fold Domain in Centromeric Histones
Mol. Biol. Evol.,
September 1, 2004;
21(9):
1712 - 1718.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Shibata and M. Murata
Differential localization of the centromere-specific proteins in the major centromeric satellite of Arabidopsis thaliana
J. Cell Sci.,
June 15, 2004;
117(14):
2963 - 2970.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Jin, J. R. Melo, K. Nagaki, P. B. Talbert, S. Henikoff, R. K. Dawe, and J. Jiang
Maize Centromeres: Organization and Functional Adaptation in the Genetic Background of Oat
PLANT CELL,
March 1, 2004;
16(3):
571 - 581.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Nagaki, P. B. Talbert, C. X. Zhong, R. K. Dawe, S. Henikoff, and J. Jiang
Chromatin Immunoprecipitation Reveals That the 180-bp Satellite Repeat Is the Key Functional DNA Element of Arabidopsis thaliana Centromeres
Genetics,
March 1, 2003;
163(3):
1221 - 1225.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Nagaki, J. Song, R. M. Stupar, A. S. Parokonny, Q. Yuan, S. Ouyang, J. Liu, J. Hsiao, K. M. Jones, R. K. Dawe, et al.
Molecular and Cytological Analyses of Large Tracks of Centromeric DNA Reveal the Structure and Evolutionary Dynamics of Maize Centromeres
Genetics,
February 1, 2003;
163(2):
759 - 770.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. E. Hall, G. Kettler, and D. Preuss
Centromere Satellites From Arabidopsis Populations: Maintenance of Conserved and Variable Domains
Genome Res.,
February 1, 2003;
13(2):
195 - 205.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Vermaak, H. S. Hayden, and S. Henikoff
Centromere Targeting Element within the Histone Fold Domain of Cid
Mol. Cell. Biol.,
November 1, 2002;
22(21):
7553 - 7561.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. X. Zhong, J. B. Marshall, C. Topp, R. Mroczek, A. Kato, K. Nagaki, J. A. Birchler, J. Jiang, and R. K. Dawe
Centromeric Retroelements and Satellites Interact with Maize Kinetochore Protein CENH3
PLANT CELL,
November 1, 2002;
14(11):
2825 - 2836.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|