Preferentially Quantized Linker DNA Lengths in Saccharomyces cerevisiae

The exact lengths of linker DNAs connecting adjacent nucleosomes specify the intrinsic three-dimensional structures of eukaryotic chromatin fibers. Some studies suggest that linker DNA lengths preferentially occur at certain quantized values, differing one from another by integral multiples of the DNA helical repeat, ∼10 bp; however, studies in the literature are inconsistent. Here, we investigate linker DNA length distributions in the yeast Saccharomyces cerevisiae genome, using two novel methods: a Fourier analysis of genomic dinucleotide periodicities adjacent to experimentally mapped nucleosomes and a duration hidden Markov model applied to experimentally defined dinucleosomes. Both methods reveal that linker DNA lengths in yeast are preferentially periodic at the DNA helical repeat (∼10 bp), obeying the forms 10n+5 bp (integer n). This 10 bp periodicity implies an ordered superhelical intrinsic structure for the average chromatin fiber in yeast.

[1]  W Hörz,et al.  Sequence specific cleavage of DNA by micrococcal nuclease. , 1981, Nucleic acids research.

[2]  Ryoiti Kiyama,et al.  Dinucleosome DNA of human K562 cells: experimental and computational characterizations. , 2003, Journal of molecular biology.

[3]  I. Albert,et al.  Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome , 2007, Nature.

[4]  N. Sonenberg,et al.  ATP/Mg++-dependent cross-linking of cap binding proteins to the 5' end of eukaryotic mRNA. , 1981, Nucleic acids research.

[5]  B. Silverman,et al.  Density Estimation for Statistics and Data Analysis , 1987 .

[6]  K. V. van Holde,et al.  Organization of spacer DNA in chromatin. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Irene K. Moore,et al.  A genomic code for nucleosome positioning , 2006, Nature.

[8]  Lani F. Wu,et al.  Genome-Scale Identification of Nucleosome Positions in S. cerevisiae , 2005, Science.

[9]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[10]  J. Widom,et al.  A relationship between the helical twist of DNA and the ordered positioning of nucleosomes in all eukaryotic cells. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Sean R. Eddy,et al.  Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids , 1998 .

[12]  A. Travers,et al.  Asymmetry and polarity of nucleosomes in chicken erythrocyte chromatin. , 1989, The EMBO journal.

[13]  P. J. Green,et al.  Density Estimation for Statistics and Data Analysis , 1987 .

[14]  C. Bustamante,et al.  Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Widom,et al.  Role of DNA sequence in nucleosome stability and dynamics , 2001, Quarterly Reviews of Biophysics.

[16]  F. Strauss,et al.  Organization of internucleosomal DNA in rat liver chromatin. , 1983, The EMBO journal.

[17]  Lawrence R. Rabiner,et al.  A tutorial on hidden Markov models and selected applications in speech recognition , 1989, Proc. IEEE.

[18]  Louise Fairall,et al.  EM measurements define the dimensions of the "30-nm" chromatin fiber: evidence for a compact, interdigitated structure. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Rubin,et al.  Maximum likelihood from incomplete data via the EM - algorithm plus discussions on the paper , 1977 .

[20]  Jonathan Widom,et al.  Improved alignment of nucleosome DNA sequences using a mixture model , 2005, Nucleic acids research.

[21]  Yechezkel Kashi,et al.  Three Sequence Rules for Chromatin , 2006, Journal of biomolecular structure & dynamics.

[22]  J. O. Thomas,et al.  Yeast chromatin structure , 1976, FEBS letters.

[23]  H. Drew,et al.  Sequence periodicities in chicken nucleosome core DNA. , 1986, Journal of molecular biology.

[24]  V. Zhurkin,et al.  DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Dominique Durand,et al.  Role of histone tails in the conformation and interactions of nucleosome core particles. , 2004, Biochemistry.

[26]  Yechezkel Kashi,et al.  Yeast Nucleosome DNA Pattern: Deconvolution from Genome Sequences of S. cerevisiae , 2005, Journal of biomolecular structure & dynamics.

[27]  T. Richmond,et al.  X-ray structure of a tetranucleosome and its implications for the chromatin fibre , 2005, Nature.

[28]  T. Richmond,et al.  DNA binding within the nucleosome core. , 1998, Current opinion in structural biology.

[29]  F Strauss,et al.  Nucleosome spacing in rat liver chromatin. A study with exonuclease III. , 1982, Nucleic acids research.