Abstract
Layered on top of information conveyed by DNA sequence and chromatin are higher order structures that encompass portions of chromosomes, entire chromosomes, and even whole genomes. Interphase chromosomes are not positioned randomly within the nucleus, but instead adopt preferred conformations. Disparate DNA elements co-localize into functionally defined aggregates or 'factories' for transcription and DNA replication. In budding yeast, Drosophila and many other eukaryotes, chromosomes adopt a Rabl configuration, with arms extending from centromeres adjacent to the spindle pole body to telomeres that abut the nuclear envelope. Nonetheless, the topologies and spatial relationships of chromosomes remain poorly understood. Here we developed a method to globally capture intra- and inter-chromosomal interactions, and applied it to generate a map at kilobase resolution of the haploid genome of Saccharomyces cerevisiae. The map recapitulates known features of genome organization, thereby validating the method, and identifies new features. Extensive regional and higher order folding of individual chromosomes is observed. Chromosome XII exhibits a striking conformation that implicates the nucleolus as a formidable barrier to interaction between DNA sequences at either end. Inter-chromosomal contacts are anchored by centromeres and include interactions among transfer RNA genes, among origins of early DNA replication and among sites where chromosomal breakpoints occur. Finally, we constructed a three-dimensional model of the yeast genome. Our findings provide a glimpse of the interface between the form and function of a eukaryotic genome.
MeSH Terms
Cell Nucleolus/genetics,metabolism
Cell Nucleus/genetics,metabolism
Centromere/genetics,metabolism
Chromosome Breakpoints
Chromosome Positioning/physiology
Chromosomes, Fungal/genetics,metabolism
DNA Replication
Genome, Fungal
Haploidy
Imaging, Three-Dimensional
Intranuclear Space/metabolism
RNA, Transfer/genetics
Replication Origin/genetics
Saccharomyces cerevisiae/cytology,genetics
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Duan Zhijun
Institute for Stem Cell and Regenerative Medicine, University of Washington, Seattle, Washington 98195-8056, USA.
Andronescu Mirela
Schutz Kevin
McIlwain Sean
Kim Yoo Jung
Lee Choli
Shendure Jay
Fields Stanley
Blau C Anthony
Noble William S
References (30)
30 references, click to expand
-
Comprehensive mapping of long-range interactions reveals folding principles of the human genome.
Science. 2009 Oct 9;326(5950):289-93
PMID: 19815776
-
Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops.
Nat Genet. 2004 Aug;36(8):889-93
PMID: 15273689
-
Nucleolar clustering of dispersed tRNA genes.
Science. 2003 Nov 21;302(5649):1399-401
PMID: 14631041
-
High-resolution statistical mapping reveals gene territories in live yeast.
Nat Methods. 2008 Dec;5(12):1031-7
PMID: 18978785
-
Long-range compaction and flexibility of interphase chromatin in budding yeast analyzed by high-resolution imaging techniques.
Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16495-500
PMID: 15545610
-
Active genes dynamically colocalize to shared sites of ongoing transcription.
Nat Genet. 2004 Oct;36(10):1065-71
PMID: 15361872
-
MAP kinase signaling induces nuclear reorganization in budding yeast.
Curr Biol. 2000 Apr 6;10(7):373-82
PMID: 10753745
-
Interchromosomal associations between alternatively expressed loci.
Nature. 2005 Jun 2;435(7042):637-45
PMID: 15880101
-
ChIP-based methods for the identification of long-range chromatin interactions.
J Cell Biochem. 2009 May 1;107(1):30-9
PMID: 19247990
-
Spatial organisation and behaviour of the parental chromosome sets in the nuclei of Saccharomyces cerevisiae x S. paradoxus hybrids.
J Cell Sci. 2002 Oct 1;115(Pt 19):3829-35
PMID: 12235293
-
Ribosome synthesis in Saccharomyces cerevisiae.
Annu Rev Genet. 1999;33:261-311
PMID: 10690410
-
Fragile genomic sites are associated with origins of replication.
Genome Biol Evol. 2009 Sep 09;1:350-63
PMID: 20333204
-
Developmentally induced changes in transcriptional program alter spatial organization across chromosomes.
Genes Dev. 2005 May 15;19(10):1188-98
PMID: 15905407
-
Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase.
J Cell Biol. 1998 Apr 6;141(1):21-9
PMID: 9531545
-
Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes.
Genes Dev. 2008 Aug 15;22(16):2204-14
PMID: 18708579
-
Controlled exchange of chromosomal arms reveals principles driving telomere interactions in yeast.
Genome Res. 2008 Feb;18(2):261-71
PMID: 18096749
-
Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C).
Nat Genet. 2006 Nov;38(11):1348-54
PMID: 17033623
-
Chromosome looping in yeast: telomere pairing and coordinated movement reflect anchoring efficiency and territorial organization.
J Cell Biol. 2005 Jan 31;168(3):375-87
PMID: 15684028
-
Lack of chromosome territoriality in yeast: promiscuous rejoining of broken chromosome ends.
Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13949-54
PMID: 8943041
-
Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories.
Cell. 2006 Jun 30;125(7):1297-308
PMID: 16814716
-
Visualizing chromatin dynamics in interphase nuclei.
Science. 2002 May 24;296(5572):1412-6
PMID: 12029120
-
An oestrogen-receptor-alpha-bound human chromatin interactome.
Nature. 2009 Nov 5;462(7269):58-64
PMID: 19890323
-
Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions.
Nat Rev Genet. 2007 Feb;8(2):104-15
PMID: 17230197
-
Capturing chromosome conformation.
Science. 2002 Feb 15;295(5558):1306-11
PMID: 11847345
-
Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions.
Nat Genet. 2006 Nov;38(11):1341-7
PMID: 17033624
-
Nuclear neighborhoods and gene expression.
Curr Opin Genet Dev. 2009 Apr;19(2):172-9
PMID: 19339170
-
Chromosome dynamics in the yeast interphase nucleus.
Science. 2001 Dec 7;294(5549):2181-6
PMID: 11739961
-
Beyond the sequence: cellular organization of genome function.
Cell. 2007 Feb 23;128(4):787-800
PMID: 17320514
-
An evaluation of 3C-based methods to capture DNA interactions.
Nat Methods. 2007 Nov;4(11):895-901
PMID: 17971780
-
The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae.
J Cell Biol. 1996 Sep;134(6):1349-63
PMID: 8830766