iSeq: A new double-barcode method for detecting dynamic genetic interactions in yeast

G3: Genes, Genomes, Genetics

Volumn 7, Issue 1, 2017, Pages 143-153

  Jaffe, Mia ^a   Sherlock, Gavin ^a   Levy, Sasha F ^b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

DNA barcoding; Genetic interactions; Saccharomyces cerevisiae; Systems biology; Whole genome sequencing

Indexed keywords

FUNGAL DNA; GENOMIC DNA;

ANEUPLOIDY; ARTICLE; CONTROLLED STUDY; DNA BARCODING; FUNGAL GENETICS; FUNGAL STRAIN; GENE DELETION; GENE INTERACTION; GENE MUTATION; GENE REPLICATION; GENETIC BACKGROUND; GENETIC ENGINEERING; GENETIC VARIATION; GENOTYPE; INTERACTION SEQUENCING PLATFORM; NONHUMAN; SEQUENCE ANALYSIS; DNA MICROARRAY; EPISTASIS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; MUTATION; PROCEDURES; SACCHAROMYCES CEREVISIAE; SYSTEMS BIOLOGY;

ANEUPLOIDY; EPISTASIS, GENETIC; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENE-ENVIRONMENT INTERACTION; GENOTYPE; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SACCHAROMYCES CEREVISIAE; SYSTEMS BIOLOGY;

EID: 85008429109     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.116.034207     Document Type: Article

References (75)

1. Albert, R., 2005 Scale-free networks in cell biology. J. Cell Sci. 118: 4947-4957.
2. Bandyopadhyay, S., M. Mehta, D. Kuo, M.-K. Sung, R. Chuang et al., 2010 Rewiring of genetic networks in response to DNA damage. Science 330: 1385-1389.
3. Baryshnikova, A., M. Costanzo, Y. Kim, H.Ding, J. Koh et al., 2010 Quantitative analysis of fitness and genetic interactions in yeast on a genome scale. Nat. Methods 7: 1017-1024.
4. Bender, A., and J. R. Pringle, 1991 Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 1295-1305.
5. Brachmann, C. B., A. Davies, G. J. Cost, E. Caputo, J. Li et al., 1998 Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
6. Breslow, D. K., D. M. Cameron, S. R. Collins, M. Schuldiner, J. Stewart-Ornstein et al., 2008 A comprehensive strategy enabling high-resolution functional analysis of the yeast genome. Nat. Methods 5: 711-718.
7. Collins, S. R., M. Schuldiner, N. J. Krogan, and J. S. Weissman, 2006 A strategy for extracting and analyzing large-scale quantitative epistatic interaction data. Genome Biol. 7: R63.
8. Collins, S. R., K. M. Miller, N. L. Maas, A. Roguev, J. Fillingham et al., 2007 Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446: 806-810.
9. Costanzo, M., A. Baryshnikova, J. Bellay, Y. Kim, E. D. Spear et al., 2010 The genetic landscape of a cell. Science 327: 425-431.
10. Costanzo, M., B. VanderSluis, E. N. Koch, A. Baryshnikova, C. Pons et al., 2016 A global genetic interaction network maps a wiring diagram of cellular function. Science 353: aaf1420.
11. Darby, M. M., L. Serebreni, X. Pan, J. D. Boeke, and J. L. Corden, 2012 The Saccharomyces cerevisiae Nrd1-Nab3 transcription termination pathway acts in opposition to Ras signaling and mediates response to nutrient depletion. Mol. Cell. Biol. 32: 1762-1775.
12. Davierwala, A. P., J. Haynes, Z. Li, R. L. Brost, M. D. Robinson et al., 2005 The synthetic genetic interaction spectrum of essential genes. Nat. Genet. 37: 1147-1152.
13. Decourty, L., C. Saveanu, K. Zemam, F. Hantraye, E. Frachon et al., 2008 Linking functionally related genes by sensitive and quantitative characterization of genetic interaction profiles. Proc. Natl. Acad. Sci. USA 105: 5821-5826.
14. Dodgson, S. E., S. Kim, M. Costanzo, A. Baryshnikova, D. L. Morse et al., 2016 Chromosome-specific and global effects of aneuploidy in Saccharomyces cerevisiae. Genetics 202: 1395-1409.
15. Dutkowski, J., M. Kramer, M. A. Surma, R. Balakrishnan, J. M. Cherry et al., 2013 A gene ontology inferred from molecular networks. Nat. Biotechnol. 31: 38-45.
16. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles et al., 2002 Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
17. Gilbert, L. A., M. H. Larson, L.Morsut, Z. Liu, G. A. Brar et al., 2013 CRISPRmediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154: 442-451.
18. Gresham, D., V. M. Boer, A. Caudy, N. Ziv, N. J. Brandt et al., 2011 Systemlevel analysis of genes and functions affecting survival during nutrient starvation in Saccharomyces cerevisiae. Genetics 187: 299-317.
19. Guénolé, A., R. Srivas, K. Vreeken, Z. Z. Wang, S. Wang et al., 2013 Dissection of DNA damage responses using multiconditional genetic interaction maps. Mol. Cell 49: 346-358.
20. Harrison, R., B. Papp, C. Pál, S. G. Oliver, and D. Delneri, 2007 Plasticity of genetic interactions in metabolic networks of yeast. Proc. Natl. Acad. Sci. USA 104: 2307-2312.
21. Herman, P. K., and J. Rine, 1997 Yeast spore germination: a requirement for Ras protein activity during re-entry into the cell cycle. EMBO J. 16: 6171-6181.
22. Hillenmeyer, M. E., E. Fung, J. Wildenhain, S. E. Pierce, S. Hoon et al., 2008 The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 320: 362-365.
23. Huang, Z., S. Srinivasan, J. Zhang, K. Chen, Y. Li et al., 2012 Discovering thiamine transporters as targets of chloroquine using a novel functional genomics strategy. PLoS Genet. 8: e1003083.
24. Hughes, T. R., C. J. Roberts, H. Dai, A. R. Jones, M. R. Meyer et al., 2000 Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25: 333-337.
25. Jasnos, L., and R. Korona, 2007 Epistatic buffering of fitness loss in yeast double deletion strains. Nat. Genet. 39: 550-554.
26. Kao, K. C., and G. Sherlock, 2008 Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat. Genet. 40: 1499-1504.
27. Kelley, R., and T. Ideker, 2005 Systematic interpretation of genetic interactions using protein networks. Nat. Biotechnol. 23: 561-566.
28. Kryazhimskiy, S., D. P. Rice, E. R. Jerison, and M. M. Desai, 2014 Microbial evolution. Global epistasis makes adaptation predictable despite sequencelevel stochasticity. Science 344: 1519-1522.
29. Kumar, P., S. Henikoff, and P. C. Ng, 2009 Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4: 1073-1081.
30. Lehner, B., C. Crombie, J. Tischler, A. Fortunato, and A. G. Fraser, 2006 Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. Nat. Genet. 38: 896-903.
31. Levy, S. F., J. R. Blundell, S. Venkataram, D. A. Petrov, D. S. Fisher et al., 2015 Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature 519: 181-186.
32. Li, H., and R. Durbin, 2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
33. Li, H., B. Handsaker, A. Wysoker, T. Fennell, and J. Ruan 1000 Genome Project Data Processing Subgroup, 2009 The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
34. Li, Q.-R., A.-R.Carvunis, H. Yu, J.-D. J.Han, Q. Zhong et al., 2008 Revisiting the Saccharomyces cerevisiae predicted ORFeome. Genome Res. 18: 1294-1303.
35. Liu, G., M. Y. J. Yong, M. Yurieva, K. G. Srinivasan, J. Liu et al., 2015 Gene essentiality is a quantitative property linked to cellular evolvability. Cell 163: 1388-1399.
36. Mani, R., R. P. St Onge, J. L. Hartman, G. Giaever, and F. P. Roth, 2008 Defining genetic interaction. Proc. Natl. Acad. Sci. USA 105: 3461-3466.
37. Mans, R., H. M. van Rossum, M. Wijsman, A. Backx, N. G. A. Kuijpers et al., 2015 CRISPR/Cas9: a molecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae. FEMS Yeast Res. 15: pii: fov004.
38. Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader et al., 2005 Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
39. Martin, H., M. Shales, P. Fernandez-Piñar, P. Wei, M. Molina et al., 2015 Differential genetic interactions of yeast stress response MAPK pathways. Mol. Syst. Biol. 11: 800.
40. Martin, M., 2011 Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet.journal. 17: 10-12.
41. McKenna, A., M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis et al., 2010 The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20: 1297-1303.
42. Moriya, H., Y. Shimizu-Yoshida, and H. Kitano, 2006 In vivo robustness analysis of cell division cycle genes in Saccharomyces cerevisiae. PLoS Genet. 2: e111.
43. Musso, G., M. Costanzo, M. Huangfu, A. M. Smith, J. Paw et al., 2008 The extensive and condition-dependent nature of epistasis among wholegenome duplicates in yeast. Genome Res. 18: 1092-1099.
44. Ooi, S. L., D. D. Shoemaker, and J. D. Boeke, 2003 DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat. Genet. 35: 277-286.
45. Pan, X., D. S. Yuan, D.Xiang, X.Wang, S. Sookhai-Mahadeo et al., 2004 A robust toolkit for functional profiling of the yeast genome. Mol. Cell 16: 487-496.
46. Pan, X., P. Ye, D. S. Yuan, X. Wang, J. S. Bader et al., 2006 A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081.
47. Pavelka, N., G. Rancati, J. Zhu, W. D. Bradford, A. Saraf et al., 2010 Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468: 321-325.
48. Pelechano, V., W. Wei, and L. M. Steinmetz, 2013 Extensive transcriptional heterogeneity revealed by isoform profiling. Nature 497: 127-131.
49. Phillips, P. C., S. P. Otto, andM. C.Whitlock, 2000 Beyond the average. The evolutionary importance of gene interactions and variability of epistatic effects, pp. 20-38 in Epistasis and the Evolutionary Process, edited byWolf, J., E. Brodie, and M.Wade. Oxford University Press, New York.
50. Rattray, A., G. Santoyo, B. Shafer, and J. N. Strathern, 2015 Elevated mutation rate during meisosis in Saccharomyces cerevisiae. PLoS Genet. 11: e1004910.
51. Robinson, D. G., W. Chen, J. D. Storey, and D. Gresham, 2014 Design and analysis of Bar-seq experiments. G3 (Bethesda) 4: 11-18.
52. Roguev, A., S. Bandyopadhyay, M. Zofall, K. Zhang, T. Fischer et al., 2008 Conservation and rewiring of functional modules revealed by an epistasis map in fission yeast. Science 322: 405-410.
53. Schuldiner, M., S. R. Collins, N. J. Thompson, V. Denic, A. Bhamidipati et al., 2005 Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123: 507-519.
54. Schuldiner, M., S.R.Collins, J. S. Weissman, andN. J.Krogan, 2006 Quantitative genetic analysis in Saccharomyces cerevisiae using epistatic miniarray profiles (E-MAPs) and its application to chromatin functions. Methods 40: 344-352.
55. Segrè, D., A. Deluna, G. M. Church, and R. Kishony, 2005 Modular epistasis in yeast metabolism. Nat. Genet. 37: 77-83.
56. Senturk, S., N. H. Shirole, D.D.Nowak, V. Corbo, A. Vaughan et al., 2015 A rapid and tunable method to temporally control Cas9 expression enables the identification of essential genes and the interrogation of functional gene interactions in vitro and in vivo. bioRxiv. Available at: http://dx.doi.org/10.1101/023366.
57. Smith, A. M., L. E. Heisler, J. Mellor, F. Kaper, M. J. Thompson et al., 2009 Quantitative phenotyping via deep barcode sequencing. Genome Res. 19: 1836-1842.
58. Smith, J. D., S. Suresh, U. Schlecht, M.Wu, O. Wagih et al., 2016 Quantitative CRISPR interference screens in yeast identify chemical-genetic interactions and new rules for guide RNA design. Genome Biol. 17: 45.
59. Stark, C., B.-J. Breitkreutz, T. Reguly, L. Boucher, A. Breitkreutz et al., 2006 BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34: D535-D539.
60. St Onge, R. P., R. Mani, J. Oh, M. Proctor, E. Fung et al., 2007 Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nat. Genet. 39: 199-206.
61. Szamecz, B., G. Boross, D. Kalapis, K. Kovács, G. Fekete et al., 2014 The genomic landscape of compensatory evolution. PLoS Biol. 12: e1001935.
62. Teng, X., M. Dayhoff-Brannigan, W.-C. Cheng, C. E. Gilbert, C. N. Sing et al., 2013 Genome-wide consequences of deleting any single gene. Mol. Cell 52: 485-494.
63. Tong, A. H. Y., and C. Boone, 2007 High-throughput strain construction and systematic synthetic lethal screening in Saccharomyces cerevisiae. Methods Microbiol. 36: 369-707.
64. Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Bader et al., 2001 Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
65. Tong, A. H. Y., G. Lesage, G. D. Bader, H. Ding, H. Xu et al., 2004 Global mapping of the yeast genetic interaction network. Science 303: 808-813.
66. Vernon, M., K. Lobachev, and T. D. Petes, 2008 High rates of "unselected" aneuploidy and chromosome rearrangements in tel1 mec1 haploid yeast strains. Genetics 179: 237-247.
67. Wahba, L., J. D. Amon, D. Koshland, and M. Vuica-Ross, 2011 RNase H and multiple RNA biogenesis factors cooperate to prevent RNA:DNA hybrids from generating genome instability. Mol. Cell 44: 978-988.
68. Williams, R., S. G. Peisajovich, O. J. Miller, S. Magdassi, D. S. Tawfik et al., 2006 Amplification of complex gene libraries by emulsion PCR. Nat. Methods 3: 545-550.
69. Winzeler, E. A., D. D. Shoemaker, A. Astromoff, H. Liang, K. Anderson et al., 1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
70. Wong, S. L., L. V. Zhang, A. H. Y. Tong, Z. Li, D. S. Goldberg et al., 2004 Combining biological networks to predict genetic interactions. Proc. Natl. Acad. Sci. USA 101: 15682-15687.
71. Xie, C., and M. T. Tammi, 2009 CNV-seq, a new method to detect copy number variation using high-throughput sequencing. BMC Bioinformatics 10: 80.
72. Ye, P., B. D. Peyser, X. Pan, J. D. Boeke, F. A. Spencer et al., 2005 Gene function prediction from congruent synthetic lethal interactions in yeast. Mol. Syst. Biol. 1: 2005.0026.
73. Yona, A. H., Y. S. Manor, R. H. Herbst, G. H. Romano, A. Mitchell et al., 2012 Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl. Acad. Sci. USA 109: 21010-21015.
74. Yu, H., L. Tardivo, S. Tam, E. Weiner, F. Gebreab et al., 2011 Next-generation sequencing to generate interactome datasets. Nat. Methods 8: 478-480.
75. Zuk, O., E. Hechter, S. R. Sunyaev, and E. S. Lander, 2012 The mystery of missing heritability: genetic interactions create phantom heritability. Proc. Natl. Acad. Sci. USA 109: 1193-1198.