Characterization of chromosomal architecture in Arabidopsis by chromosome conformation capture

BackgroundThe packaging of long chromatin fibers in the nucleus poses a major challenge, as it must fulfill both physical and functional requirements. Until recently, insights into the chromosomal architecture of plants were mainly provided by cytogenetic studies. Complementary to these analyses, chromosome conformation capture technologies promise to refine and improve our view on chromosomal architecture and to provide a more generalized description of nuclear organization.ResultsEmploying circular chromosome conformation capture, this study describes chromosomal architecture in Arabidopsis nuclei from a genome-wide perspective. Surprisingly, the linear organization of chromosomes is reflected in the genome-wide interactome. In addition, we study the interplay of the interactome and epigenetic marks and report that the heterochromatic knob on the short arm of chromosome 4 maintains a pericentromere-like interaction profile and interactome despite its euchromatic surrounding.ConclusionDespite the extreme condensation that is necessary to pack the chromosomes into the nucleus, the Arabidopsis genome appears to be packed in a predictive manner, according to the following criteria: heterochromatin and euchromatin represent two distinct interactomes; interactions between chromosomes correlate with the linear position on the chromosome arm; and distal chromosome regions have a higher potential to interact with other chromosomes.

[1]  Tanya Z. Berardini,et al.  The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools , 2011, Nucleic Acids Res..

[2]  A. Tanay,et al.  Three-Dimensional Folding and Functional Organization Principles of the Drosophila Genome , 2012, Cell.

[3]  L. Cour Heterochromatin and the organisation of nucleoli in plants , 1951, Heredity.

[4]  L. Deaven,et al.  Quantitative determination of nuclear pore complexes in cycling cells with differing DNA content , 1977, The Journal of cell biology.

[5]  Elzo de Wit,et al.  Determining long-range chromatin interactions for selected genomic sites using 4C-seq technology: from fixation to computation. , 2012, Methods.

[6]  William Stafford Noble,et al.  A Three-Dimensional Model of the Yeast Genome , 2010, Nature.

[7]  J. Fuchs,et al.  Centromere clustering is a major determinant of yeast interphase nuclear organization. , 2000, Journal of cell science.

[8]  B. van Steensel,et al.  Interactions among Polycomb Domains Are Guided by Chromosome Architecture , 2011, PLoS genetics.

[9]  J. Rougemont,et al.  The Dynamic Architecture of Hox Gene Clusters , 2011, Science.

[10]  F. Shibata,et al.  Differential localization of the centromere-specific proteins in the major centromeric satellite of Arabidopsis thaliana , 2004, Journal of Cell Science.

[11]  Ingo Schubert,et al.  Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[13]  L. F. La Cour Heterochromatin and the organization of nucleoli in plants. , 1951, Heredity.

[14]  J. Dekker,et al.  The active FMR1 promoter is associated with a large domain of altered chromatin conformation with embedded local histone modifications , 2006, Proceedings of the National Academy of Sciences.

[15]  G. H. Jones,et al.  Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. , 2001, Journal of cell science.

[16]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[17]  C. Dean,et al.  A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization , 2012, The EMBO journal.

[18]  Yuda Fang,et al.  Centromere positioning and dynamics in living Arabidopsis plants. , 2005, Molecular biology of the cell.

[19]  S. Henikoff,et al.  The Centromere Paradox: Stable Inheritance with Rapidly Evolving DNA , 2001, Science.

[20]  Wen Huang,et al.  The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant , 2001, Nucleic Acids Res..

[21]  W. de Laat,et al.  Tissue- and Expression Level–Specific Chromatin Looping at Maize b1 Epialleles[W] , 2009, The Plant Cell Online.

[22]  D W Hukins,et al.  Optimised parameters for A-DNA and B-DNA. , 1972, Biochemical and biophysical research communications.

[23]  Jiyong Wang,et al.  Csi1 links centromeres to the nuclear envelope for centromere clustering , 2012, The Journal of cell biology.

[24]  J. Wellink,et al.  Non-specific interactions are sufficient to explain the position of heterochromatic chromocenters and nucleoli in interphase nuclei , 2009, Nucleic acids research.

[25]  B. Mcclintock CHROMOSOME MORPHOLOGY IN ZEA MAYS. , 1929, Science.

[26]  Pablo Tamayo,et al.  Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Henikoff,et al.  Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. , 2003, Genetics.

[28]  D. Wagner,et al.  Histone modifications and dynamic regulation of genome accessibility in plants. , 2007, Current opinion in plant biology.

[29]  Nicola J Stacey,et al.  LITTLE NUCLEI Genes Affecting Nuclear Morphology in Arabidopsis thaliana[W] , 2007, The Plant Cell Online.

[30]  Guillaume J. Filion,et al.  Systematic Protein Location Mapping Reveals Five Principal Chromatin Types in Drosophila Cells , 2010, Cell.

[31]  Christopher J. Hale,et al.  MORC Family ATPases Required for Heterochromatin Condensation and Gene Silencing , 2012, Science.

[32]  C. Dean,et al.  Integrated Cytogenetic Map of Chromosome Arm 4S of A. thaliana Structural Organization of Heterochromatic Knob and Centromere Region , 2000, Cell.

[33]  Stéphane Robin,et al.  Integrative epigenomic mapping defines four main chromatin states in Arabidopsis , 2011, The EMBO journal.

[34]  T. Michael,et al.  Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production. , 2013, The Plant journal : for cell and molecular biology.

[35]  William C. Nierman,et al.  Lin, X. et al. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402, 761-768 , 1999 .

[36]  M. Martí-Renom,et al.  Chromatin globules: a common motif of higher order chromosome structure? , 2011, Current opinion in cell biology.

[37]  Kevin L. Schneider,et al.  Maize Centromere Structure and Evolution: Sequence Analysis of Centromeres 2 and 5 Reveals Dynamic Loci Shaped Primarily by Retrotransposons , 2009, PLoS genetics.

[38]  Ulrich C. Klostermeier,et al.  A Powerful Method for Transcriptional Profiling of Specific Cell Types in Eukaryotes: Laser-Assisted Microdissection and RNA Sequencing , 2012, PloS one.

[39]  The Chinese Human Genome Sequencing Consortium,et al.  Sequence and analysis of chromosome 5 of the plant Arabidopsis thaliana , 2000, Nature.

[40]  K Mayer,et al.  Sequence and analysis of chromosome 5 of the plant Arabidopsis thaliana. , 2000, Nature.

[41]  A. Berr,et al.  Interphase chromatin organisation in Arabidopsis nuclei: constraints versus randomness , 2012, Chromosoma.

[42]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[43]  K. Sandhu,et al.  Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions , 2006, Nature Genetics.

[44]  S. Jacobsen,et al.  Comprehensive Analysis of Silencing Mutants Reveals Complex Regulation of the Arabidopsis Methylome , 2013, Cell.

[45]  S. Armstrong,et al.  Cytogenetics for the model system Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[46]  R. Wilson,et al.  The Complete Sequence of a Heterochromatic Island from a Higher Eukaryote , 2000, Cell.

[47]  G. Kreth,et al.  Chromosome arrangement and nuclear architecture but not centromeric sequences are conserved between Arabidopsis thaliana and Arabidopsis lyrata. , 2006, The Plant journal : for cell and molecular biology.

[48]  I. Amit,et al.  Comprehensive mapping of long range interactions reveals folding principles of the human genome , 2011 .

[49]  Jia Liu,et al.  Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. , 2003, Genetics.

[50]  W. D. Laat,et al.  A Decade of 3c Technologies: Insights into Nuclear Organization References , 2022 .

[51]  Alex E. Lash,et al.  Gene Expression Omnibus: NCBI gene expression and hybridization array data repository , 2002, Nucleic Acids Res..

[52]  J. Dekker,et al.  Capturing Chromosome Conformation , 2002, Science.

[53]  John A. Stamatoyannopoulos,et al.  Cell-type-specific long-range looping interactions identify distant regulatory elements of the CFTR gene , 2010, Nucleic acids research.

[54]  E. Lam,et al.  DNA hypomethylation reduces homologous pairing of inserted tandem repeat arrays in somatic nuclei of Arabidopsis thaliana. , 2005, The Plant journal : for cell and molecular biology.