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

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 read...

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Main Authors: J Javier Díaz‐Mejía, Albi Celaj, Joseph C Mellor, Atina Coté, Attila Balint, Brandon Ho, Pritpal Bansal, Fatemeh Shaeri, Marinella Gebbia, Jochen Weile, Marta Verby, Anna Karkhanina, YiFan Zhang, Cassandra Wong, Justin Rich, D'Arcy Prendergast, Gaurav Gupta, Sedide Öztürk, Daniel Durocher, Grant W Brown, Frederick P Roth
Format: Article
Language:English
Published: Springer Nature 2018-05-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.15252/msb.20177985
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author J Javier Díaz‐Mejía
Albi Celaj
Joseph C Mellor
Atina Coté
Attila Balint
Brandon Ho
Pritpal Bansal
Fatemeh Shaeri
Marinella Gebbia
Jochen Weile
Marta Verby
Anna Karkhanina
YiFan Zhang
Cassandra Wong
Justin Rich
D'Arcy Prendergast
Gaurav Gupta
Sedide Öztürk
Daniel Durocher
Grant W Brown
Frederick P Roth
author_facet J Javier Díaz‐Mejía
Albi Celaj
Joseph C Mellor
Atina Coté
Attila Balint
Brandon Ho
Pritpal Bansal
Fatemeh Shaeri
Marinella Gebbia
Jochen Weile
Marta Verby
Anna Karkhanina
YiFan Zhang
Cassandra Wong
Justin Rich
D'Arcy Prendergast
Gaurav Gupta
Sedide Öztürk
Daniel Durocher
Grant W Brown
Frederick P Roth
author_sort J Javier Díaz‐Mejía
collection DOAJ
description 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.
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spelling doaj-art-2cc42bd94f72421daa7d032148d66de42025-08-20T03:46:32ZengSpringer NatureMolecular Systems Biology1744-42922018-05-0114511710.15252/msb.20177985Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion geneticsJ Javier Díaz‐Mejía0Albi Celaj1Joseph C Mellor2Atina Coté3Attila Balint4Brandon Ho5Pritpal Bansal6Fatemeh Shaeri7Marinella Gebbia8Jochen Weile9Marta Verby10Anna Karkhanina11YiFan Zhang12Cassandra Wong13Justin Rich14D'Arcy Prendergast15Gaurav Gupta16Sedide Öztürk17Daniel Durocher18Grant W Brown19Frederick P Roth20Donnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoLunenfeld‐Tanenbaum Research Institute, Mt. Sinai HospitalDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoDepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical SchoolDepartment of Molecular Genetics, University of TorontoDonnelly Centre, University of TorontoDonnelly Centre, University of TorontoAbstract 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.https://doi.org/10.15252/msb.20177985condition‐dependentDNA barcodeen massegenetic interactionsequencing
spellingShingle J Javier Díaz‐Mejía
Albi Celaj
Joseph C Mellor
Atina Coté
Attila Balint
Brandon Ho
Pritpal Bansal
Fatemeh Shaeri
Marinella Gebbia
Jochen Weile
Marta Verby
Anna Karkhanina
YiFan Zhang
Cassandra Wong
Justin Rich
D'Arcy Prendergast
Gaurav Gupta
Sedide Öztürk
Daniel Durocher
Grant W Brown
Frederick P Roth
Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion genetics
Molecular Systems Biology
condition‐dependent
DNA barcode
en masse
genetic interaction
sequencing
title Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion genetics
title_full Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion genetics
title_fullStr Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion genetics
title_full_unstemmed Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion genetics
title_short Mapping DNA damage‐dependent genetic interactions in yeast via party mating and barcode fusion genetics
title_sort mapping dna damage dependent genetic interactions in yeast via party mating and barcode fusion genetics
topic condition‐dependent
DNA barcode
en masse
genetic interaction
sequencing
url https://doi.org/10.15252/msb.20177985
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