Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion genetics

Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions. State‐of‐the‐art yeast genetic interaction mapping, which relies on robotic manipulation of arrays of double‐mutant strains, does not scale readily to mu...

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Published inMolecular systems biology Vol. 14; no. 5; pp. e7985 - n/a
Main Authors Díaz‐Mejía, J Javier, Celaj, Albi, Mellor, Joseph C, Coté, Atina, Balint, Attila, Ho, Brandon, Bansal, Pritpal, Shaeri, Fatemeh, Gebbia, Marinella, Weile, Jochen, Verby, Marta, Karkhanina, Anna, Zhang, YiFan, Wong, Cassandra, Rich, Justin, Prendergast, D'Arcy, Gupta, Gaurav, Öztürk, Sedide, Durocher, Daniel, Brown, Grant W, Roth, Frederick P
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.05.2018
EMBO Press
John Wiley and Sons Inc
Springer Nature
Subjects
Bar codes
Bleomycin
Chromosome Mapping
condition‐dependent
Damage
Deoxyribonucleic acid
DNA
DNA barcode
DNA Barcoding, Taxonomic
DNA Damage
DNA Repair
DNA sequencing
EMBO17
EMBO22
EMBO26
en masse
Epistasis, Genetic
Gene Deletion
Gene mapping
Genes
Genetic engineering
genetic interaction
Genetic Loci
Genetics
Growth conditions
High-Throughput Nucleotide Sequencing
Kinases
Mapping
Mating
Method
Methods
Methyl Methanesulfonate
Models, Theoretical
Mutants
Promoter Regions, Genetic
Protein kinase
Proteins
Recombination
Repair
Reproducibility of Results
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae Proteins - genetics
sequencing
Yeast
condition‐dependent
DNA barcode
genetic interaction
sequencing
en masse
Online AccessGet full text

Cover

Abstract Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions. State‐of‐the‐art yeast genetic interaction mapping, which relies on robotic manipulation of arrays of double‐mutant strains, does not scale readily to multi‐condition studies. Here, we describe barcode fusion genetics to map genetic interactions (BFG‐GI), by which double‐mutant strains generated via en masse “party” mating can also be monitored en masse for growth to detect genetic interactions. By using site‐specific recombination to fuse two DNA barcodes, each representing a specific gene deletion, BFG‐GI enables multiplexed quantitative tracking of double mutants via next‐generation sequencing. We applied BFG‐GI to a matrix of DNA repair genes under nine different conditions, including methyl methanesulfonate (MMS), 4‐nitroquinoline 1‐oxide (4NQO), bleomycin, zeocin, and three other DNA‐damaging environments. BFG‐GI recapitulated known genetic interactions and yielded new condition‐dependent genetic interactions. We validated and further explored a subnetwork of condition‐dependent genetic interactions involving MAG1 , SLX4, and genes encoding the Shu complex, and inferred that loss of the Shu complex leads to an increase in the activation of the checkpoint protein kinase Rad53. Synopsis A new method, Barcode Fusion Genetics to Map Genetic Interactions (BFG‐GI) allows generating double mutants and measuring condition‐dependent genetic interactions en masse . Application of BFG‐GI to DNA repair genes reveals a new function for the Shu complex. BFG‐GI involves generating double‐mutant‐specific fused barcodes, enabling to measure the abundance of double mutants en masse by next generation sequencing. Once a double mutant BFG‐GI pool has been generated genetic interactions can be tested in new growth conditions. BFG‐GI is applied to 26 genes related to DNA damage repair in nine different conditions, including seven DNA‐damaging agents. A novel relationship is reported between the Shu complex and the checkpoint protein kinase Rad53. Graphical Abstract A new method, Barcode Fusion Genetics to Map Genetic Interactions (BFG‐GI) allows generating double mutants and measuring condition‐dependent genetic interactions en masse . Application of BFG‐GI to DNA repair genes reveals a new function for the Shu complex.
AbstractList Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions. State‐of‐the‐art yeast genetic interaction mapping, which relies on robotic manipulation of arrays of double‐mutant strains, does not scale readily to multi‐condition studies. Here, we describe barcode fusion genetics to map genetic interactions ( BFG ‐ GI ), by which double‐mutant strains generated via en masse “party” mating can also be monitored en masse for growth to detect genetic interactions. By using site‐specific recombination to fuse two DNA barcodes, each representing a specific gene deletion, BFG ‐ GI enables multiplexed quantitative tracking of double mutants via next‐generation sequencing. We applied BFG ‐ GI to a matrix of DNA repair genes under nine different conditions, including methyl methanesulfonate ( MMS ), 4‐nitroquinoline 1‐oxide (4 NQO ), bleomycin, zeocin, and three other DNA ‐damaging environments. BFG ‐ GI recapitulated known genetic interactions and yielded new condition‐dependent genetic interactions. We validated and further explored a subnetwork of condition‐dependent genetic interactions involving MAG 1 , SLX 4, and genes encoding the Shu complex, and inferred that loss of the Shu complex leads to an increase in the activation of the checkpoint protein kinase Rad53.
Abstract Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions. State‐of‐the‐art yeast genetic interaction mapping, which relies on robotic manipulation of arrays of double‐mutant strains, does not scale readily to multi‐condition studies. Here, we describe barcode fusion genetics to map genetic interactions (BFG‐GI), by which double‐mutant strains generated via en masse “party” mating can also be monitored en masse for growth to detect genetic interactions. By using site‐specific recombination to fuse two DNA barcodes, each representing a specific gene deletion, BFG‐GI enables multiplexed quantitative tracking of double mutants via next‐generation sequencing. We applied BFG‐GI to a matrix of DNA repair genes under nine different conditions, including methyl methanesulfonate (MMS), 4‐nitroquinoline 1‐oxide (4NQO), bleomycin, zeocin, and three other DNA‐damaging environments. BFG‐GI recapitulated known genetic interactions and yielded new condition‐dependent genetic interactions. We validated and further explored a subnetwork of condition‐dependent genetic interactions involving MAG1, SLX4, and genes encoding the Shu complex, and inferred that loss of the Shu complex leads to an increase in the activation of the checkpoint protein kinase Rad53.
Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions. State‐of‐the‐art yeast genetic interaction mapping, which relies on robotic manipulation of arrays of double‐mutant strains, does not scale readily to multi‐condition studies. Here, we describe barcode fusion genetics to map genetic interactions (BFG‐GI), by which double‐mutant strains generated via en masse “party” mating can also be monitored en masse for growth to detect genetic interactions. By using site‐specific recombination to fuse two DNA barcodes, each representing a specific gene deletion, BFG‐GI enables multiplexed quantitative tracking of double mutants via next‐generation sequencing. We applied BFG‐GI to a matrix of DNA repair genes under nine different conditions, including methyl methanesulfonate (MMS), 4‐nitroquinoline 1‐oxide (4NQO), bleomycin, zeocin, and three other DNA‐damaging environments. BFG‐GI recapitulated known genetic interactions and yielded new condition‐dependent genetic interactions. We validated and further explored a subnetwork of condition‐dependent genetic interactions involving MAG1, SLX4, and genes encoding the Shu complex, and inferred that loss of the Shu complex leads to an increase in the activation of the checkpoint protein kinase Rad53.
Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions. State‐of‐the‐art yeast genetic interaction mapping, which relies on robotic manipulation of arrays of double‐mutant strains, does not scale readily to multi‐condition studies. Here, we describe barcode fusion genetics to map genetic interactions (BFG‐GI), by which double‐mutant strains generated via en masse “party” mating can also be monitored en masse for growth to detect genetic interactions. By using site‐specific recombination to fuse two DNA barcodes, each representing a specific gene deletion, BFG‐GI enables multiplexed quantitative tracking of double mutants via next‐generation sequencing. We applied BFG‐GI to a matrix of DNA repair genes under nine different conditions, including methyl methanesulfonate (MMS), 4‐nitroquinoline 1‐oxide (4NQO), bleomycin, zeocin, and three other DNA‐damaging environments. BFG‐GI recapitulated known genetic interactions and yielded new condition‐dependent genetic interactions. We validated and further explored a subnetwork of condition‐dependent genetic interactions involving MAG1, SLX4, and genes encoding the Shu complex, and inferred that loss of the Shu complex leads to an increase in the activation of the checkpoint protein kinase Rad53. Synopsis A new method, Barcode Fusion Genetics to Map Genetic Interactions (BFG‐GI) allows generating double mutants and measuring condition‐dependent genetic interactions en masse. Application of BFG‐GI to DNA repair genes reveals a new function for the Shu complex. BFG‐GI involves generating double‐mutant‐specific fused barcodes, enabling to measure the abundance of double mutants en masse by next generation sequencing. Once a double mutant BFG‐GI pool has been generated genetic interactions can be tested in new growth conditions. BFG‐GI is applied to 26 genes related to DNA damage repair in nine different conditions, including seven DNA‐damaging agents. A novel relationship is reported between the Shu complex and the checkpoint protein kinase Rad53. A new method, Barcode Fusion Genetics to Map Genetic Interactions (BFG‐GI) allows generating double mutants and measuring condition‐dependent genetic interactions en masse. Application of BFG‐GI to DNA repair genes reveals a new function for the Shu complex.
Condition-dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions. State-of-the-art yeast genetic interaction mapping, which relies on robotic manipulation of arrays of double-mutant strains, does not scale readily to multi-condition studies. Here, we describe barcode fusion genetics to map genetic interactions (BFG-GI), by which double-mutant strains generated via "party" mating can also be monitored for growth to detect genetic interactions. By using site-specific recombination to fuse two DNA barcodes, each representing a specific gene deletion, BFG-GI enables multiplexed quantitative tracking of double mutants via next-generation sequencing. We applied BFG-GI to a matrix of DNA repair genes under nine different conditions, including methyl methanesulfonate (MMS), 4-nitroquinoline 1-oxide (4NQO), bleomycin, zeocin, and three other DNA-damaging environments. BFG-GI recapitulated known genetic interactions and yielded new condition-dependent genetic interactions. We validated and further explored a subnetwork of condition-dependent genetic interactions involving , and genes encoding the Shu complex, and inferred that loss of the Shu complex leads to an increase in the activation of the checkpoint protein kinase Rad53.
Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions. State‐of‐the‐art yeast genetic interaction mapping, which relies on robotic manipulation of arrays of double‐mutant strains, does not scale readily to multi‐condition studies. Here, we describe barcode fusion genetics to map genetic interactions (BFG‐GI), by which double‐mutant strains generated via en masse “party” mating can also be monitored en masse for growth to detect genetic interactions. By using site‐specific recombination to fuse two DNA barcodes, each representing a specific gene deletion, BFG‐GI enables multiplexed quantitative tracking of double mutants via next‐generation sequencing. We applied BFG‐GI to a matrix of DNA repair genes under nine different conditions, including methyl methanesulfonate (MMS), 4‐nitroquinoline 1‐oxide (4NQO), bleomycin, zeocin, and three other DNA‐damaging environments. BFG‐GI recapitulated known genetic interactions and yielded new condition‐dependent genetic interactions. We validated and further explored a subnetwork of condition‐dependent genetic interactions involving MAG1 , SLX4, and genes encoding the Shu complex, and inferred that loss of the Shu complex leads to an increase in the activation of the checkpoint protein kinase Rad53. Synopsis A new method, Barcode Fusion Genetics to Map Genetic Interactions (BFG‐GI) allows generating double mutants and measuring condition‐dependent genetic interactions en masse . Application of BFG‐GI to DNA repair genes reveals a new function for the Shu complex. BFG‐GI involves generating double‐mutant‐specific fused barcodes, enabling to measure the abundance of double mutants en masse by next generation sequencing. Once a double mutant BFG‐GI pool has been generated genetic interactions can be tested in new growth conditions. BFG‐GI is applied to 26 genes related to DNA damage repair in nine different conditions, including seven DNA‐damaging agents. A novel relationship is reported between the Shu complex and the checkpoint protein kinase Rad53. Graphical Abstract A new method, Barcode Fusion Genetics to Map Genetic Interactions (BFG‐GI) allows generating double mutants and measuring condition‐dependent genetic interactions en masse . Application of BFG‐GI to DNA repair genes reveals a new function for the Shu complex.
Author Gebbia, Marinella
Karkhanina, Anna
Durocher, Daniel
Shaeri, Fatemeh
Celaj, Albi
Verby, Marta
Brown, Grant W
Weile, Jochen
Coté, Atina
Ho, Brandon
Roth, Frederick P
Wong, Cassandra
Balint, Attila
Bansal, Pritpal
Rich, Justin
Öztürk, Sedide
Gupta, Gaurav
Díaz‐Mejía, J Javier
Zhang, YiFan
Mellor, Joseph C
Prendergast, D'Arcy
AuthorAffiliation 7 Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology Dana‐Farber Cancer Institute Boston MA USA
1 Donnelly Centre University of Toronto Toronto ON Canada
10 Present address: Department of Cellular and Molecular Medicine Center for Chromosome Stability University of Copenhagen Copenhagen Denmark
3 Lunenfeld‐Tanenbaum Research Institute Mt. Sinai Hospital Toronto ON Canada
6 Department of Biochemistry University of Toronto Toronto ON Canada
5 Department of Biological Chemistry and Molecular Pharmacology Harvard Medical School Boston MA USA
8 Canadian Institute for Advanced Research Toronto ON Canada
2 Department of Molecular Genetics University of Toronto Toronto ON Canada
4 Department of Computer Science University of Toronto Toronto ON Canada
9 Present address: SeqWell, Inc. Beverly MA USA
11 Present address: Roche Sequencing Solutions Pleasanton CA USA
AuthorAffiliation_xml – name: 9 Present address: SeqWell, Inc. Beverly MA USA
– name: 1 Donnelly Centre University of Toronto Toronto ON Canada
– name: 5 Department of Biological Chemistry and Molecular Pharmacology Harvard Medical School Boston MA USA
– name: 2 Department of Molecular Genetics University of Toronto Toronto ON Canada
– name: 4 Department of Computer Science University of Toronto Toronto ON Canada
– name: 8 Canadian Institute for Advanced Research Toronto ON Canada
– name: 10 Present address: Department of Cellular and Molecular Medicine Center for Chromosome Stability University of Copenhagen Copenhagen Denmark
– name: 6 Department of Biochemistry University of Toronto Toronto ON Canada
– name: 7 Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology Dana‐Farber Cancer Institute Boston MA USA
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  orcidid: 0000-0002-6481-1772
  surname: Balint
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  organization: Donnelly Centre, University of Toronto, Department of Biochemistry, University of Toronto, Department of Cellular and Molecular Medicine, Center for Chromosome Stability, University of Copenhagen
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  givenname: Brandon
  surname: Ho
  fullname: Ho, Brandon
  organization: Donnelly Centre, University of Toronto, Department of Biochemistry, University of Toronto
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– sequence: 8
  givenname: Fatemeh
  surname: Shaeri
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– sequence: 9
  givenname: Marinella
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  givenname: Jochen
  orcidid: 0000-0003-1628-9390
  surname: Weile
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– sequence: 11
  givenname: Marta
  surname: Verby
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  givenname: Anna
  surname: Karkhanina
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  organization: Donnelly Centre, University of Toronto, Department of Molecular Genetics, University of Toronto, Lunenfeld‐Tanenbaum Research Institute, Mt. Sinai Hospital
– sequence: 13
  givenname: YiFan
  surname: Zhang
  fullname: Zhang, YiFan
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  givenname: Cassandra
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  surname: Gupta
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– sequence: 21
  givenname: Frederick P
  orcidid: 0000-0002-6628-649X
  surname: Roth
  fullname: Roth, Frederick P
  email: fritz.roth@utoronto.ca
  organization: Donnelly Centre, University of Toronto, Department of Molecular Genetics, University of Toronto, Lunenfeld‐Tanenbaum Research Institute, Mt. Sinai Hospital, Department of Computer Science, University of Toronto, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer Institute, Canadian Institute for Advanced Research
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29807908$$D View this record in MEDLINE/PubMed
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Issue 5
Keywords condition‐dependent
DNA barcode
genetic interaction
sequencing
en masse
Language English
License Attribution
2018 The Authors. Published under the terms of the CC BY 4.0 license.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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– ident: e_1_2_8_29_1
  doi: 10.1038/msb.2011.99
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Snippet Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions....
Condition-dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions....
Abstract Condition‐dependent genetic interactions can reveal functional relationships between genes that are not evident under standard culture conditions....
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SourceType Open Website
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StartPage e7985
SubjectTerms Bar codes
Bleomycin
Chromosome Mapping
condition‐dependent
Damage
Deoxyribonucleic acid
DNA
DNA barcode
DNA Barcoding, Taxonomic
DNA Damage
DNA Repair
DNA sequencing
EMBO17
EMBO22
EMBO26
en masse
Epistasis, Genetic
Gene Deletion
Gene mapping
Genes
Genetic engineering
genetic interaction
Genetic Loci
Genetics
Growth conditions
High-Throughput Nucleotide Sequencing
Kinases
Mapping
Mating
Method
Methods
Methyl Methanesulfonate
Models, Theoretical
Mutants
Promoter Regions, Genetic
Protein kinase
Proteins
Recombination
Repair
Reproducibility of Results
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae Proteins - genetics
sequencing
Yeast
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Title Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion genetics
URI https://link.springer.com/article/10.15252/msb.20177985
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fmsb.20177985
https://www.ncbi.nlm.nih.gov/pubmed/29807908
https://www.proquest.com/docview/2046476516
https://pubmed.ncbi.nlm.nih.gov/PMC5974512
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Volume 14
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