An inverse relationship to germline transcription defines centromeric chromatin in C. elegans
Reto Gassmann,Andreas Rechtsteiner,Karen W. Yuen,Karen W. Yuen,A. Muroyama,Thea A. Egelhofer,Laura J. Gaydos,Francie Barron,Francie Barron,Paul S. Maddox,Paul S. Maddox,Anthony Essex,Anthony Essex,Joost Monen,Joost Monen,Sevinc Ercan,Jason D. Lieb,Karen Oegema,Susan Strome,Arshad Desai +19 more
TLDR
It is proposed that germline transcription defines genomic regions that exclude CENP-A incorporation in progeny, and that zygotic transcription during early embryogenesis remodels and reinforces this basal pattern.Abstract:
Centromeres are chromosomal loci that direct segregation of the genome during cell division. The histone H3 variant CENP-A (also known as CenH3) defines centromeres in monocentric organisms, which confine centromere activity to a discrete chromosomal region, and holocentric organisms, which distribute centromere activity along the chromosome length. Because the highly repetitive DNA found at most centromeres is neither necessary nor sufficient for centromere function, stable inheritance of CENP-A nucleosomal chromatin is postulated to propagate centromere identity epigenetically. Here, we show that in the holocentric nematode Caenorhabditis elegans pre-existing CENP-A nucleosomes are not necessary to guide recruitment of new CENP-A nucleosomes. This is indicated by lack of CENP-A transmission by sperm during fertilization and by removal and subsequent reloading of CENP-A during oogenic meiotic prophase. Genome-wide mapping of CENP-A location in embryos and quantification of CENP-A molecules in nuclei revealed that CENP-A is incorporated at low density in domains that cumulatively encompass half the genome. Embryonic CENP-A domains are established in a pattern inverse to regions that are transcribed in the germline and early embryo, and ectopic transcription of genes in a mutant germline altered the pattern of CENP-A incorporation in embryos. Furthermore, regions transcribed in the germline but not embryos fail to incorporate CENP-A throughout embryogenesis. We propose that germline transcription defines genomic regions that exclude CENP-A incorporation in progeny, and that zygotic transcription during early embryogenesis remodels and reinforces this basal pattern. These findings link centromere identity to transcription and shed light on the evolutionary plasticity of centromeres.read more
Citations
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A Molecular View of Kinetochore Assembly and Function.
Andrea Musacchio,Arshad Desai +1 more
TL;DR: A broad summary of progress in the elucidation of the composition of the kinetochore and the identification of various physical and functional modules within its substructure has led to a much deeper molecular understanding of kinetchore organization and the origins of its functional output.
Journal ArticleDOI
The molecular basis for centromere identity and function
TL;DR: Ongoing work is providing important molecular insights into the central requirements for centromere identity and propagation, and the mechanisms by which centromeres recruit kinetochores to connect to spindle microtubules.
Journal ArticleDOI
Comparative analysis of metazoan chromatin organization
Joshua W. K. Ho,Joshua W. K. Ho,Youngsook L. Jung,Tao Liu,Tao Liu,Burak H. Alver,Soohyun Lee,Kohta Ikegami,Kohta Ikegami,Kyung-Ah Sohn,Kyung-Ah Sohn,Aki Minoda,Aki Minoda,Michael Y. Tolstorukov,Alex Appert,Stephen C. J. Parker,Tingting Gu,Anshul Kundaje,Anshul Kundaje,Anshul Kundaje,Nicole C. Riddle,Nicole C. Riddle,Eric Bishop,Eric Bishop,Thea A. Egelhofer,Sheng'en Shawn Hu,Artyom A. Alekseyenko,Andreas Rechtsteiner,Dalal Asker,Dalal Asker,Jason A. Belsky,Sarah K. Bowman,Q. Brent Chen,Ron A.-J. Chen,Daniel S. Day,Yan Dong,Andréa C. Dosé,Xikun Duan,Charles B. Epstein,Sevinc Ercan,Elise A. Feingold,Francesco Ferrari,Jacob M. Garrigues,Nils Gehlenborg,Nils Gehlenborg,Peter J. Good,Psalm Haseley,Daniel He,Moritz Herrmann,Michael M. Hoffman,Tess E. Jeffers,Tess E. Jeffers,Peter V. Kharchenko,P. Kolasinska-Zwierz,Chitra V. Kotwaliwale,Chitra V. Kotwaliwale,Nischay Kumar,Nischay Kumar,Sasha A. Langley,Sasha A. Langley,Erica Larschan,Isabel J. Latorre,Maxwell W. Libbrecht,Xueqiu Lin,Richard W. Park,Richard W. Park,Michael J. Pazin,Hoang N. Pham,Hoang N. Pham,Hoang N. Pham,Annette Plachetka,Bo Qin,Yuri B. Schwartz,Yuri B. Schwartz,Noam Shoresh,Przemyslaw Stempor,A. Vielle,Chengyang Wang,Christina M. Whittle,Christina M. Whittle,Huiling Xue,Robert E. Kingston,Ju Han Kim,Bradley E. Bernstein,Bradley E. Bernstein,Bradley E. Bernstein,Abby F. Dernburg,Abby F. Dernburg,Abby F. Dernburg,Vincenzo Pirrotta,Mitzi I. Kuroda,William Stafford Noble,Thomas D. Tullius,Manolis Kellis,Manolis Kellis,David M. MacAlpine,Susan Strome,Sarah C. R. Elgin,Xiaole Shirley Liu,Xiaole Shirley Liu,Jason D. Lieb,Julie Ahringer,Gary H. Karpen,Gary H. Karpen,Peter J. Park +104 more
TL;DR: Comparison of combinatorial patterns of histone modifications, nuclear lamina-associated domains, organization of large-scale topological domains, chromatin environment at promoters and enhancers, nucleosome positioning, and DNA replication patterns reveals many conserved features of chromatin organization among the three organisms.
Journal ArticleDOI
Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution.
Daniël P. Melters,Keith Bradnam,Hugh A. Young,Natalie Telis,Michael R. May,J. Graham Ruby,Robert Sebra,Paul Peluso,John Eid,David R. Rank,José Fernando Garcia,Joseph L. DeRisi,Joseph L. DeRisi,Timothy P. L. Smith,Christian M. Tobias,Jeffrey Ross-Ibarra,Ian F Korf,Simon W. L. Chan,Simon W. L. Chan +18 more
TL;DR: The results indicate that tandem repeats are highly prevalent at centromeres of both animal and plant genomes, which suggests a functional role for such repeats, perhaps in promoting concerted evolution of centromere DNA across chromosomes.
Journal ArticleDOI
The centromere: chromatin foundation for the kinetochore machinery.
TL;DR: This review of classic work and recent progress in studies of centromeric chromatin on vertebrates considers possible roles for repetitive DNA sequences found at most centromeres, chromatin factors and modifications that assemble and activate CENP-A chromatin for Kinetochore assembly, plus the use of artificial chromosomes and kinetochores to study centromere function.
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