GC-Rich DNA Elements Enable Replication Origin Activity in the Methylotrophic Yeast Pichia pastoris

PLoS Genetics

Volumn 10, Issue 3, 2014, Pages

  Liachko, Ivan ^a   Youngblood, Rachel A ^a   Tsui, Kyle ^b   Bubb, Kerry L ^a   Queitsch, Christine ^a   Raghuraman, M K ^a   Nislow, Corey ^b,c   Brewer, Bonita J ^a   Dunham, Maitreya J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYSTEINE; GLYCINE; THREONINE; CHROMATIN; DNA; NUCLEOSOME;

ARTICLE; BUDDING; DNA REPLICATION ORIGIN; DNA SEQUENCE; FUNGAL GENOME; GENE MAPPING; GENETIC ASSOCIATION; GENETIC VARIABILITY; METHYLOTROPHIC YEAST; NONHUMAN; NUCLEOSOME; PICHIA PASTORIS; PROMOTER REGION; SCHIZOSACCHAROMYCES; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; CHROMATIN; DNA REPLICATION; GC RICH SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; PICHIA; TRANSCRIPTION INITIATION SITE;

CHROMATIN; DNA; DNA REPLICATION; GC RICH SEQUENCE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; NUCLEOSOMES; PICHIA; REPLICATION ORIGIN; TRANSCRIPTION INITIATION SITE;

EID: 84897385484     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004169     Document Type: Article

References (71)

1. Méchali M, (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11: 728-738 doi:10.1038/nrm2976.
2. Eaton ML, Prinz JA, MacAlpine HK, Tretyakov G, Kharchenko PV, et al. (2011) Chromatin signatures of the Drosophila replication program. Genome Res 21: 164-174 doi:10.1101/gr.116038.110.
3. Dellino GI, Cittaro D, Piccioni R, Luzi L, Banfi S, et al. (2013) Genome-wide mapping of human DNA-replication origins: Levels of transcription at ORC1 sites regulate origin selection and replication timing. Genome Res 23: 1-11 doi:10.1101/gr.142331.112.
4. Costas C, la Paz Sanchez de M, Stroud H, Yu Y, Oliveros JC, et al. (2011) Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat Struct Mol Biol 18: 395-400 doi:10.1038/nsmb.1988.
5. Hansen RS, Thomas S, Sandstrom R, Canfield TK, Thurman RE, et al. (2010) Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc Natl Acad Sci USA 107: 139-144 doi:10.1073/pnas.0912402107.
6. Méchali M, Yoshida K, Coulombe P, Pasero P, (2013) Genetic and epigenetic determinants of DNA replication origins, position and activation. Curr Opin Genet Dev 23: 124-131 doi:10.1016/j.gde.2013.02.010.
7. Cayrou C, Coulombe P, Vigneron A, Stanojcic S, Ganier O, et al. (2011) Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res 21: 1438-1449 doi:10.1101/gr.121830.111.
8. Stinchcomb DT, Struhl K, Davis RW, (1979) Isolation and characterisation of a yeast chromosomal replicator. Nature 282: 39-43.
9. Bell SP, Dutta A, (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333-374 doi:10.1146/annurev.biochem.71.110601.135425.
10. Chang VK, Donato JJ, Chan CS, Tye BK, (2004) Mcm1 promotes replication initiation by binding specific elements at replication origins. Mol Cell Biol 24: 6514-6524 doi:10.1128/MCB.24.14.6514-6524.2004.
11. Walker SS, Francesconi SC, Tye BK, Eisenberg S, (1989) The OBF1 protein and its DNA-binding site are important for the function of an autonomously replicating sequence in Saccharomyces cerevisiae. Mol Cell Biol 9: 2914-2921.
12. Knott SRV, Peace JM, Ostrow AZ, Gan Y, Rex AE, et al. (2012) Forkhead Transcription Factors Establish Origin Timing and Long-Range Clustering in S. cerevisiae. Cell 148: 99-111 doi:10.1016/j.cell.2011.12.012.
13. Eaton ML, Galani K, Kang S, Bell SP, MacAlpine DM, (2010) Conserved nucleosome positioning defines replication origins. Genes Dev 24: 748-753 doi:10.1101/gad.1913210.
14. Berbenetz NM, Nislow C, Brown GW, (2010) Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure. PLoS Genet 6: e1001092 doi:10.1371/journal.pgen.1001092.
15. Lin S, Kowalski D, (1997) Functional equivalency and diversity of cis-acting elements among yeast replication origins. Mol Cell Biol 17: 5473-5484.
16. Donaldson AD, Raghuraman MK, Friedman KL, Cross FR, Brewer BJ, et al. (1998) CLB5-dependent activation of late replication origins in S. cerevisiae. Mol Cell 2: 173-182.
17. Koren A, Tsai H-J, Tirosh I, Burrack LS, Barkai N, et al. (2010) Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet 6: e1001068 doi:10.1371/journal.pgen.1001068.
18. Mantiero D, Mackenzie A, Donaldson A, Zegerman P, (2011) Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast. EMBO J 30: 4805-4814 doi:10.1038/emboj.2011.404.
19. Bechhoefer J, Rhind N, (2012) Replication timing and its emergence from stochastic processes. Trends Genet 28: 374-381 doi:10.1016/j.tig.2012.03.011.
20. de Moura APS, Retkute R, Hawkins M, Nieduszynski CA, (2010) Mathematical modelling of whole chromosome replication. Nucleic Acids Res 38: 5623-5633 doi:10.1093/nar/gkq343.
21. Chuang RY, Kelly TJ, (1999) The fission yeast homologue of Orc4p binds to replication origin DNA via multiple AT-hooks. Proc Natl Acad Sci USA 96: 2656-2661.
22. Dai J, Chuang R-Y, Kelly TJ, (2005) DNA replication origins in the Schizosaccharomyces pombe genome. Proc Natl Acad Sci USA 102: 337-342 doi:10.1073/pnas.0408811102.
23. Patel PK, Arcangioli B, Baker SP, Bensimon A, Rhind N, (2006) DNA replication origins fire stochastically in fission yeast. Mol Biol Cell 17: 308-316 doi:10.1091/mbc.E05-07-0657.
24. Ryba T, Hiratani I, Sasaki T, Battaglia D, Kulik M, et al. (2011) Replication timing: a fingerprint for cell identity and pluripotency. PLoS Comput Biol 7: e1002225 doi:10.1371/journal.pcbi.1002225.
25. Delgado S, Gómez M, Bird A, Antequera F, (1998) Initiation of DNA replication at CpG islands in mammalian chromosomes. EMBO J 17: 2426-2435 doi:10.1093/emboj/17.8.2426.
26. MacAlpine HK, Gordân R, Powell SK, Hartemink AJ, MacAlpine DM, (2010) Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res 20: 201-211 doi:10.1101/gr.097873.109.
27. Liachko I, Bhaskar A, Lee C, Chung SCC, Tye B-K, et al. (2010) A comprehensive genome-wide map of autonomously replicating sequences in a naive genome. PLoS Genet 6: e1000946 doi:10.1371/journal.pgen.1000946.
28. Liachko I, Tanaka E, Cox K, Chung SCC, Yang L, et al. (2011) Novel features of ARS selection in budding yeast Lachancea kluyveri. BMC Genomics 12: 633 doi:10.1186/1471-2164-12-633.
29. Di Rienzi SC, Lindstrom KC, Mann T, Noble WS, Raghuraman MK, et al. (2012) Maintaining replication origins in the face of genomic change. Genome Res 22: 1940-1952 doi:10.1101/gr.138248.112.
30. Xu J, Yanagisawa Y, Tsankov AM, Hart C, Aoki K, et al. (2012) Genome-wide identification and characterization of replication origins by deep sequencing. Genome Biol 13: R27 doi:10.1186/gb-2012-13-4-r27.
31. De Schutter K, Lin Y-C, Tiels P, Van Hecke A, Glinka S, et al. (2009) Genome sequence of the recombinant protein production host Pichia pastoris. Nat Biotechnol 27: 561-566 doi:10.1038/nbt.1544.
32. Kurtzman CP, (2009) Biotechnological strains of Komagataella (Pichia) pastoris are Komagataella phaffii as determined from multigene sequence analysis. J Ind Microbiol Biotechnol 36: 1435-1438 doi:10.1007/s10295-009-0638-4.
33. Macauley-Patrick S, Fazenda ML, McNeil B, Harvey LM, (2005) Heterologous protein production using the Pichia pastoris expression system. Yeast 22: 249-270 doi:10.1002/yea.1208.
34. Anckar J, Sistonen L, (2011) Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 80: 1089-1115 doi:10.1146/annurev-biochem-060809-095203.
35. Chan CS, Tye BK, (1980) Autonomously replicating sequences in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 77: 6329-6333.
36. Tanaka S, Tanaka Y, Isono K, (1996) Systematic mapping of autonomously replicating sequences on chromosome V of Saccharomyces cerevisiae using a novel strategy. Yeast 12: 101-113 doi:;10.1002/(SICI)1097-0061(199602)12:2<101::AID-YEA885>3.0.CO;2-2.
37. Cregg JM, Barringer KJ, Hessler AY, Madden KR, (1985) Pichia pastoris as a host system for transformations. Mol Cell Biol 5: 3376-3385.
38. Liachko I, Youngblood RA, Keich U, Dunham MJ, (2013) High-resolution mapping, characterization, and optimization of autonomously replicating sequences in yeast. Genome Res 23: 698-704 doi:10.1101/gr.144659.112.
39. Keich U, Gao H, Garretson JS, Bhaskar A, Liachko I, et al. (2008) Computational detection of significant variation in binding affinity across two sets of sequences with application to the analysis of replication origins in yeast. BMC Bioinformatics 9: 372 doi:10.1186/1471-2105-9-372.
40. Ng P, Keich U, (2008) GIMSAN: a Gibbs motif finder with significance analysis. Bioinformatics 24: 2256-2257 doi:10.1093/bioinformatics/btn408.
41. Breier AM, Chatterji S, Cozzarelli NR, (2004) Prediction of Saccharomyces cerevisiae replication origins. Genome Biol 5: R22 doi:10.1186/gb-2004-5-4-r22.
42. Nieduszynski CA, Knox Y, Donaldson AD, (2006) Genome-wide identification of replication origins in yeast by comparative genomics. Genes Dev 20: 1874-1879 doi:10.1101/gad.385306.
43. Bhaskar A, Keich U, (2010) Confidently estimating the number of DNA replication origins. Stat Appl Genet Mol Biol 9: Article28 doi:10.2202/1544-6115.1544.
44. Bailey TL, Elkan C, (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
45. Brewer BJ, Fangman WL, (1987) The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51: 463-471.
46. Fowler DM, Araya CL, Fleishman SJ, Kellogg EH, Stephany JJ, et al. (2010) High-resolution mapping of protein sequence-function relationships. Nat Methods 7: 741-746 doi:10.1038/nmeth.1492.
47. Patwardhan RP, Lee C, Litvin O, Young DL, Pe'er D, et al. (2009) High-resolution analysis of DNA regulatory elements by synthetic saturation mutagenesis. Nat Biotechnol 27: 1173-1175 doi:10.1038/nbt.1589.
48. Müller CA, Nieduszynski CA, (2012) Conservation of replication timing reveals global and local regulation of replication origin activity. Genome Res doi:10.1101/gr.139477.112.
49. Müller CA, Hawkins M, Retkute R, Malla S, Wilson R, et al. (2013) The dynamics of genome replication using deep sequencing. Nucleic Acids Res doi:10.1093/nar/gkt878.
50. Müller P, Park S, Shor E, Huebert DJ, Warren CL, et al. (2010) The conserved bromo-adjacent homology domain of yeast Orc1 functions in the selection of DNA replication origins within chromatin. Genes Dev 24: 1418-1433 doi:10.1101/gad.1906410.
51. Lantermann AB, Straub T, Strålfors A, Yuan G-C, Ekwall K, et al. (2010) Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae. Nat Struct Mol Biol 17: 251-257 doi:10.1038/nsmb.1741.
52. Lubelsky Y, Sasaki T, Kuipers MA, Lucas I, Le Beau MM, et al. (2011) Pre-replication complex proteins assemble at regions of low nucleosome occupancy within the Chinese hamster dihydrofolate reductase initiation zone. Nucleic Acids Res 39: 3141-3155 doi:10.1093/nar/gkq1276.
53. Lee W, Tillo D, Bray N, Morse RH, Davis RW, et al. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39: 1235-1244 doi:10.1038/ng2117.
54. Tsankov AM, Thompson DA, Socha A, Regev A, Rando OJ, (2010) The role of nucleosome positioning in the evolution of gene regulation. PLoS Biol 8: e1000414 doi:10.1371/journal.pbio.1000414.
55. Liang S, Wang B, Pan L, Ye Y, He M, et al. (2012) Comprehensive structural annotation of Pichia pastoris transcriptome and the response to various carbon sources using deep paired-end RNA sequencing. BMC Genomics 13: 738 doi:10.1186/1471-2164-13-738.
56. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, et al. (2012) Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res 22: 1798-1812 doi:10.1101/gr.139105.112.
57. Yuan G-C, Liu Y-J, Dion MF, Slack MD, Wu LF, et al. (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309: 626-630 doi:10.1126/science.1112178.
58. Hahn J-S, Hu Z, Thiele DJ, Iyer VR, (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24: 5249-5256 doi:10.1128/MCB.24.12.5249-5256.2004.
59. Trinklein ND, Murray JI, Hartman SJ, Botstein D, Myers RM, (2004) The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response. Mol Biol Cell 15: 1254-1261 doi:10.1091/mbc.E03-10-0738.
60. Shirahige K, Iwasaki T, Rashid MB, Ogasawara N, Yoshikawa H, (1993) Location and characterization of autonomously replicating sequences from chromosome VI of Saccharomyces cerevisiae. Mol Cell Biol 13: 5043-5056.
61. Dujon B, (2010) Yeast evolutionary genomics. Nat Rev Genet 11: 512-524 doi:10.1038/nrg2811.
62. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104 doi:10.1038/nature02800.
63. Gasser B, Maurer M, Rautio J, Sauer M, Bhattacharyya A, et al. (2007) Monitoring of transcriptional regulation in Pichia pastoris under protein production conditions. BMC Genomics 8: 179 doi:10.1186/1471-2164-8-179.
64. Liachko I, Dunham MJ, (2013) An autonomously replicating sequence for use in a wide range of budding yeasts. FEMS Yeast Res doi:10.1111/1567-1364.12123.
65. Lee CC, Williams TG, Wong DWS, Robertson GH, (2005) An episomal expression vector for screening mutant gene libraries in Pichia pastoris. Plasmid 54: 80-85 doi:10.1016/j.plasmid.2004.12.001.
66. Fowler DM, Araya CL, Gerard W, Fields S, (2011) Enrich: Software for Analysis of Protein Function by Enrichment and Depletion of Variants. Bioinformatics doi:10.1093/bioinformatics/btr577.
67. Crooks GE, Hon G, Chandonia J-M, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190 doi:10.1101/gr.849004.
68. Bailey TL, Gribskov M, (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14: 48-54.
69. Grant CE, Bailey TL, Noble WS, (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27: 1017-1018 doi:10.1093/bioinformatics/btr064.
70. Huberman JA, (1997) Mapping replication origins, pause sites, and termini by neutral/alkaline two-dimensional gel electrophoresis. Methods 13: 247-257 doi:10.1006/meth.1997.0524.
71. Adey A, Morrison HG, Asan, Xun X, Kitzman JO, et al. (2010) Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome Biol 11: R119 doi:10.1186/gb-2010-11-12-r119.