Postembryonic Establishment of Megabase-Scale Gene Silencing in Nucleolar Dominance

被引:58
作者
Pontes, Olga [1 ,2 ]
Lawrence, Richard J. [2 ]
Silva, Manuela [1 ]
Preuss, Sasha [2 ]
Costa-Nunes, Pedro [1 ,2 ]
Earley, Keith [2 ]
Neves, Nuno [1 ,3 ]
Viegas, Wanda [1 ]
Pikaard, Craig S. [2 ]
机构
[1] Univ Tecn Lisboa, Inst Super Agron, Ctr Bot Aplicada & Agr, P-1100 Lisbon, Portugal
[2] Washington Univ, Dept Biol, St Louis, MO 63130 USA
[3] Univ Nova Lisboa, Fac Ciencias & Tecnol, Secc Autonoma Biotecnol, Caparica, Portugal
来源
PLOS ONE | 2007年 / 2卷 / 11期
基金
美国国家卫生研究院; 美国国家科学基金会;
关键词
D O I
10.1371/journal.pone.0001157
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Nucleolar dominance is an epigenetic phenomenon in plant and animal genetic hybrids that describes the expression of 45S ribosomal RNA genes (rRNA genes) inherited from only one progenitor due to the silencing of the other progenitor's rRNA genes. rRNA genes are tandemly arrayed at nucleolus organizer regions (NORs) that span millions of basepairs, thus gene silencing in nucleolar dominance occurs on a scale second only to X-chromosome inactivation in female mammals. In Arabidopsis suecica, the allotetraploid hybrid of A. thaliana and A. arenosa, the A. thaliana-derived rRNA genes are subjected to nucleolar dominance and are silenced via repressive chromatin modifications. However, the developmental stage at which nucleolar dominance is established in A. suecica is currently unknown. We show that nucleolar dominance is not apparent in seedling cotyledons formed during embryogenesis but becomes progressively established during early postembryonic development in tissues derived from both the shoot and root apical meristems. The progressive silencing of A. thaliana rRNA genes correlates with the transition of A. thaliana NORs from a decondensed euchromatic state associated with histone H3 that is trimethylated on lysine 4 (H3K4me3) to a highly condensed heterochromatic state in which the NORs are associated with H3K9me2 and 5-methylcytosine-enriched chromocenters. In RNAi-lines in which the histone deacetylases HDA6 and HDT1 are knocked down, the developmentally regulated condensation and inactivation of A. thaliana NORs is disrupted. Collectively, these data demonstrate that HDA6 and HDT1 function in the postembryonic establishment of nucleolar dominance, a process which recurs in each generation.
引用
收藏
页数:11
相关论文
共 33 条
[11]   Epigenetic silencing of RNA polymerase I transcription [J].
Grummt, I ;
Pikaard, CS .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2003, 4 (08) :641-649
[12]  
GUERCHE P, 1990, PLANT CELL, V2, P469, DOI 10.1105/tpc.2.5.469
[13]   A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance [J].
Lawrence, RJ ;
Earley, K ;
Pontes, O ;
Silva, M ;
Chen, ZJ ;
Neves, N ;
Viegas, W ;
Pikaard, CS .
MOLECULAR CELL, 2004, 13 (04) :599-609
[14]   SHOOT DEVELOPMENT IN PLANTS - TIME FOR A CHANGE [J].
LAWSON, EJR ;
POETHIG, RS .
TRENDS IN GENETICS, 1995, 11 (07) :263-268
[15]   Restricted chromosomal silencing in nucleolar dominance [J].
Lewis, MS ;
Pikaard, CS .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2001, 98 (25) :14536-14540
[16]   Cell cycle transition in early embryonic development of Xenopus laevis [J].
Masui, Y ;
Wang, P .
BIOLOGY OF THE CELL, 1998, 90 (08) :537-548
[17]   Changes in 5S rDNA chromatin organization and transcription during heterochromatin establishment in Arabidopsis [J].
Mathieu, O ;
Jasencakova, Z ;
Vaillant, I ;
Gendrel, AV ;
Colot, V ;
Schubert, I ;
Tourmente, S .
PLANT CELL, 2003, 15 (12) :2929-2939
[18]   Nucleolar dominance: a model for rRNA gene silencing [J].
McStay, B .
GENES & DEVELOPMENT, 2006, 20 (10) :1207-1214
[19]  
NAVASHIN M., 1934, CYTOLOGIA, V5, P169, DOI 10.1508/cytologia.5.169
[20]   RIBOSOMAL-RNA GENE ACTIVITY AND CONTROL OF EXPRESSION MEDIATED BY METHYLATION AND IMPRINTING DURING EMBRYO DEVELOPMENT IN WHEAT X RYE HYBRIDS [J].
NEVES, N ;
HESLOPHARRISON, JS ;
VIEGAS, W .
THEORETICAL AND APPLIED GENETICS, 1995, 91 (03) :529-533