Sequence analysis of origins of replication in the Saccharomyces cerevisiae genomes

DNA replication is a highly precise process that is initiated from origins of replication (ORIs) and is regulated by a set of regulatory proteins. The mining of DNA sequence information will be not only beneficial for understanding the regulatory mechanism of replication initiation but also for accurately identifying ORIs. In this study, the GC profile and GC skew were calculated to analyze the compositional bias in the Saccharomyces cerevisiae genome. We found that the GC profile in the region of ORIs is significantly lower than that in the flanking regions. By calculating the information redundancy, an estimation of the correlation of nucleotides, we found that the intensity of adjoining correlation in ORIs is dramatically higher than that in flanking regions. Furthermore, the relationships between ORIs and nucleosomes as well as transcription start sites were investigated. Results showed that ORIs are usually not occupied by nucleosomes. Finally, we calculated the distribution of ORIs in yeast chromosomes and found that most ORIs are in transcription terminal regions. We hope that these results will contribute to the identification of ORIs and the study of DNA replication mechanisms.

[1]  F. Antequera,et al.  Specification of DNA replication origins and genomic base composition in fission yeasts. , 2013, Journal of molecular biology.

[2]  François Jacob,et al.  On the Regulation of DNA Replication in Bacteria , 1963 .

[3]  Guo-qing Liu,et al.  An analysis and prediction of nucleosome positioning based on information content , 2013, Chromosome Research.

[4]  Ronald W. Davis,et al.  A high-resolution atlas of nucleosome occupancy in yeast , 2007, Nature Genetics.

[5]  J. Lobry,et al.  A new method for assessing the effect of replication on DNA base composition asymmetry. , 2007, Molecular biology and evolution.

[6]  David L. Wheeler,et al.  GenBank , 2015, Nucleic Acids Res..

[7]  Khalid Sayood,et al.  A divide-and-conquer approach to fragment assembly , 2003, Bioinform..

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

[9]  Joana Sequeira-Mendes,et al.  On the opportunistic nature of transcription and replication initiation in the metazoan genome , 2012, BioEssays : news and reviews in molecular, cellular and developmental biology.

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

[11]  J. Lobry.  Asymmetric substitution patterns in the two DNA strands of bacteria. , 1996, Molecular biology and evolution.

[12]  S. Kaul,et al.  Structure, replication efficiency and fragility of yeast ARS elements. , 2012, Research in microbiology.

[13]  J. Lobry,et al.  Origin of Replication of Mycoplasma genitalium , 1996, Science.

[14]  Zu-Guo Yu,et al.  Distance, correlation and mutual information among portraits of organisms based on complete genomes , 2001 .

[15]  Eduardo P C Rocha,et al.  The replication-related organization of bacterial genomes. , 2004, Microbiology.

[16]  Victor G. Levitsky,et al.  NPRD: Nucleosome Positioning Region Database , 2004, Nucleic Acids Res..

[17]  T. Kunkel,et al.  DNA-replication fidelity, mismatch repair and genome instability in cancer cells. , 1996, European journal of biochemistry.

[18]  Fu-Jung Chang,et al.  An ARS element inhibits DNA replication through a SIR2-dependent mechanism. , 2008, Molecular cell.

[19]  Feng Gao,et al.  Ori-Finder 2, an integrated tool to predict replication origins in the archaeal genomes , 2014, Front. Microbiol..

[20]  Jeremy Miller,et al.  High-resolution analysis of four efficient yeast replication origins reveals new insights into the ORC and putative MCM binding elements , 2011, Nucleic acids research.

[21]  K. H. Wolfe,et al.  Base Composition Skews, Replication Orientation, and Gene Orientation in 12 Prokaryote Genomes , 1998, Journal of Molecular Evolution.

[22]  R. Chuang,et al.  The fission yeast homologue of Orc4p binds to replication origin DNA via multiple AT-hooks. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Irene K. Moore,et al.  The DNA-encoded nucleosome organization of a eukaryotic genome , 2009, Nature.

[24]  Cheuk C. Siow,et al.  OriDB, the DNA replication origin database updated and extended , 2011, Nucleic Acids Res..

[25]  Liaofu Luo,et al.  STATISTICAL CORRELATION OF NUCLEOTIDES IN A DNA SEQUENCE , 1998 .

[26]  A. Wolffe,et al.  DNA methylation, nucleosomes and the inheritance of chromatin structure and function. , 1998, Novartis Foundation symposium.

[27]  Lu Cai,et al.  Genome-wide characterization and prediction of Arabidopsis thaliana replication origins , 2014, Biosyst..

[28]  Wei Chen,et al.  Prediction of replication origins by calculating DNA structural properties , 2012, FEBS letters.

[29]  Khalid Sayood,et al.  The Average Mutual Information Profile as a Genomic Signature , 2008, BMC Bioinformatics.

[30]  A. Wolffe,et al.  The structure of DNA in a nucleosome. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Kenta Nakai,et al.  Genome-wide characterization of transcriptional start sites in humans by integrative transcriptome analysis. , 2011, Genome research.

[32]  R. Reeves,et al.  HMGI/Y proteins: flexible regulators of transcription and chromatin structure. , 2001, Biochimica et biophysica acta.

[33]  T. Richmond,et al.  The structure of DNA in the nucleosome core , 2003, Nature.

[34]  E. Clercq.  Frontiers in Microbiology , 1987, New Perspectives in Clinical Microbiology.

[35]  S. Buldyrev,et al.  Species independence of mutual information in coding and noncoding DNA. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[36]  Zhiping Weng,et al.  Statistical analysis of the genomic distribution and correlation of regulatory elements in the ENCODE regions. , 2007, Genome research.

[37]  Tatsuro S. Takahashi,et al.  Multiple ORC‐binding sites are required for efficient MCM loading and origin firing in fission yeast , 2003, The EMBO journal.

[38]  Feng Gao,et al.  DoriC: a database of oriC regions in bacterial genomes , 2007, Bioinform..

[39]  A. Helmrich,et al.  Transcription-replication encounters, consequences and genomic instability , 2013, Nature Structural &Molecular Biology.

[40]  Feng Gao,et al.  Segmentation algorithm for DNA sequences. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  D. MacAlpine,et al.  DNA replication and transcription programs respond to the same chromatin cues , 2014, Genome research.

[42]  L. Duret,et al.  The relationship between DNA replication and human genome organization. , 2009, Molecular biology and evolution.

[43]  Noam Kaplan,et al.  New insights into replication origin characteristics in metazoans , 2012, Cell cycle.

[44]  Conrad A. Nieduszynski,et al.  Genome-wide identification of replication origins in yeast by comparative genomics. , 2006, Genes & development.

[45]  Xiangyin Kong,et al.  The impact of nucleosome positioning on the organization of replication origins in eukaryotes. , 2009, Biochemical and biophysical research communications.

[46]  Feng Gao,et al.  GC-Profile: a web-based tool for visualizing and analyzing the variation of GC content in genomic sequences , 2006, Nucleic Acids Res..

[47]  Charles Elkan,et al.  Fitting a Mixture Model By Expectation Maximization To Discover Motifs In Biopolymer , 1994, ISMB.

[48]  Feng Gao,et al.  DeOri: a database of eukaryotic DNA replication origins , 2012, Bioinform..

[49]  Lihong Wu,et al.  Mechanism of chromosomal DNA replication initiation and replication fork stabilization in eukaryotes , 2014, Science China Life Sciences.

[50]  J. Park,et al.  Characterization of nuclear factors binding to AT‐rich element in the rat p53 promoter , 2001, Journal of cellular biochemistry.