genetic interaction landscape reveals critical ... · a. sánchez et al. 3 si figure s2 figure s2...

Genetic Interaction Landscape Reveals Critical Requirements

for Schizosaccharomyces pombe Brc1 in DNA Damage

Response Mutants

Arancha Sánchez*, Assen Roguev§, Nevan J. Krogan§ and Paul Russell*

*Department of Cell and Molecular Biology, The Scripps Research Institute, La

Jolla, California, USA

§Department of Cellular and Molecular Pharmacology, University of California,

San Francisco, California, USA

Corresponding author: Paul Russell

10550 North Torrey Pines Rd, The Scripps Research Institute, MB3, La Jolla, CA,

92037

Phone: 858-784-8273

Email: [email protected]

DOI: 10.1534/g3.115.017251

2 SI A. Sánchez et al.

Figure S1

Figure S1 Genetic interactions between Brc1 and Rad26 (A), Rad17 (B), Srs2 (C),

Pnk1 (D) or Swi3 (E). 10-fold serial dilutions of the strains were exposed to the

indicated DNA damaging agents. Plates were incubated at 30ºC for 3-4 days.

A. Sánchez et al. 3 SI

Figure S2

Figure S2 Genetic interactions between Brc1 and Sde2 (A), Raf1 (B), Set1 (C) or

Snt1 (D). 10-fold serial dilutions of the strains were exposed to the indicated DNA

damaging agents. Plates were incubated at 30ºC for 3-4 days.


Figure S3

Figure S3 Genetic interactions between Brc1 and Csi1 (A), Cbp1 (B) or Msh2 (C). 10-

fold serial dilutions of the strains were exposed to the indicated DNA damaging agents.

Plates were incubated at 30ºC for 3-4 days.


Table S1 S. pombe strains used in this study

Strain Genotype Source

AS5121 h- leu1-32 Lab stock

PR110 h+ leu1-32 ura4-D18 Lab stock

AS127 h- leu1-32 ade6M210/216 Lab stock

AS1225 h+ leu1-32 his3-D1 Lab stock

TMN3288 h+ leu1-32 ura4-D18 his3-D1 Lab stock

AS5122 h- leu1-32 brc1::hphMX6 Lab stock

JW4724 h+ leu1-32 ura4-D18 brc1::HphMX Lab stock

JW4701 h+ leu1-32 brc1::HphMX Lab stock

AS1224 h+ leu1-32 his3-D1 brc1::KanMX6 This study

JW4718 h- leu1-32 ura4-D18 brc1::HphMX Lab stock

AS411 h- leu1-32 csn1::KanMX6 This study

AS1072 h+ leu1-32 ura4-D18 his3-D1 csn1::KanMX6 This study

AS503 h+ leu1-32 ura4-D18 csn1::KanMX6 This study

AS1149 h+ leu1-32 ura4-D18 csn5::KanMX6 This study

AS5131 h- leu1-32 ddb1::KanMX6 Lab stock

AS360 h- leu1-32 spd1::NatMX6 This study

AS478 h+ leu1-32 brc1::HphMX6 csn1::KanMX6 This study

AS1160 h+ leu1-32 brc1::HphMX6 csn5::NatMX6 This study

AS466 h+ leu1-32 ddb1::KanMX6 brc1::HphMX6 This study

AS473 h- leu1-32 brc1::HphMX6 spd1::NatMX6 This study

AS475 h- leu1-32 ddb1::KanMX6 spd1::NatMX6 This study

AS511 h+ leu1-32 csn1::KanMX6 spd1::NatMX6 This study

AS474 h+ leu1-32 brc1::HphMX6 ddb1::KanMX6 spd1::NatMX6 This study

AS509 h- leu1-32 brc1::HphMX6 csn1::KanMX6 spd1::NatMX6 This study

OL5102 h- leu1-32 ura4-D18 rad11-GFP::HphMX6 Lab stock

AS712 h- leu1-32 ura4-D18 brc1::HphMX6 Rad11-GFP::HphMX6 This study


AS1506 h- leu1-32 csn1::KanMX6 Rad11-GFP::HphMX6 This study

AS1505 h+ leu1-32 ura4-D18 csn1::KanMX6 brc1::HphMX6 Rad11-GFP::HphMX6

This study

AS1409 h+ leu1-32 ura4-D18 Rad22-YFP:kanMX6 This study

AS1431 h+ leu1-32 ura4-D18 brc1::HphMX6 Rad22-YFP:kanMX6 This study

AS1510 h+ leu1-32 ura4-D18 csn1::KanMX6 rad22-YFP:KanMX This study

AS1531 h+ leu1-32 ura4-D18 csn1::KanMX6 brc1::HphMX6 Rad22-YFP:KanMX6

This study

TMN3290 h+ leu1-32 ura4-D18 his3-D1 hta-S129A::ura4+ hta2-S128A::his3+ Lab stock

AS1106 h+ leu1-32 ura4-D18 his3-D1 hta-S129A::ura4+ hta2-S128A::his3+ csn1::KanMX6

This study

LLD3259 h- leu1-32 ura4-D18 crb2::ura4 Lab stock

AS1363 h+ leu1-32 ura4-D18 csn1::KanMX6 crb2::ura4 This study

SS3134 h- leu1-32 ura4-D18 rad26::ura4 Lab stock

AS142 h+ leu1-32 ura4-D18 brc1::HphMX rad26::ura4 This study

YYY4260 h+ leu1-32 ura4-D18 rad17::ura4 Lab stock

AS201 h+ leu1-32 ura4-D18 brc1::HphMX rad17::ura4 This study

AS366 h- leu1-32 pnk1::KanMX6 This study

AS420 h+ leu1-32 brc1::HphMX6 pnk1::KanMX6 This study

AS647 h- leu1-32 swi3::KanMX6 Lab stock

AS650 h+ leu1-32 brc1::HphMX6 swi3::KanMX6 This study

AS315 h+ leu1-32 sde2::KanMX6 This study

AS312 h+ leu1-32 sde2::KanMX6 brc1::HphMX This study

AS1057 h+ leu1-32 raf1::KanMX6 This study

AS1076 h? leu1-32 brc1::HphMX6 raf1::KanMX6 This study

AS167 h+ leu1-32 set1::KanMX Lab stock

AS173 h+ leu1-32 brc1::HphMX set1::KanMX This study

AS327 h+ leu1-32 snt1::KanMX6 This study

AS322 h- leu1-32 snt1::KanMX6 brc1::HphMX This study


V2-12-C06 h+ ade6M210/216 ura4-D18 leu1-32 cbp1::kanMX4 Bioneer

AS1536 h- ade6M210/216 ura4-D18 leu1-32 brc1::HphMX6 cbp1::kanMX4 This study

PS2704 h- his3-D1 msh2::his3 O. Fleck

AS1519 h+ leu1-32 his3-D1 brc1::KanMX6 msh2::his3+ This study

V2-12-F08 h+ ade6M210/216 ura4-D18 leu1-32 csi1::kanMX4 Bioneer

AS1543 h? leu1-32 ura4-D18 brc1::HphMX6 csi1::KanMX4 This study


Table S2 S. pombe brc1 E-MAP summary

Gene Name Systematic ID Interaction

Score Function

csn1 SPBC215.03C -15.0564 COP9/Signalosome complex subunit. Activation RNR

apn2 SPBC3D6.10 -14.5842 AP-endonuclease, BER hrq1 SPAC23A1.19C -14.0666 RecQ type DNA helicase

ddb1 SPAC17H9.10C -13.6206

Damage DNA binding protein. Part of the ubiquitin ligase complex. Transcription couple repair of stalled RNA III

rad26 SPAC9E9.08 -12.4663 Cell cycle arrest

ssb3 SPCC23B6.05C -10.9769 DNA replication factor A subunit

pmt3 SPBC365.06 -10.2373 SUMO

cbf11 SPCC736.08 -8.9934 CBF1/Su(H)/LAG-1 family transcription factor

rad1 SPAC1952.07 -8.733 Checkpoint clamp protein rad9 SPAC664.07C -8.6945 Checkpoint clamp protein

rad17 SPAC14C4.13 -8.4424 RFC-related checkpoint protein

dcd1 SPBC2G2.13C -7.8334 Deoxycytidylate deaminase

nrl1 SPBC20F10.05 -7.3312 NRDE-2 family protein (predicted)

SPCC1442.02 SPCC1442.02 -6.6826 Central kinetochore associated protein (predicted)

SPBC1711.09C SPBC1711.09C -6.0633 SNARE associated Golgi protein (predicted)

srs2 SPAC4H3.05 -5.6676 ATP-dependent DNA helicase

vps60 SPCC162.06C -5.444 Vacuolar sorting protein pku80 SPBC543.03C -5.3538 Ku domain protein

ppk3 SPAC15A10.13 -5.3353 Serine/Threonine protein kinase

pnk1 SPAC23C11.04C -5.214 DNA kinase/phosphatase SPBC1711.15C SPBC1711.15C -5.0006 Sequence orphan SPBC1289.14 SPBC1289.14 -4.7565 Adducin (predicted)

nse6 SPAC11E3.08C -4.6124 Smc5-6 complex non-SMC subunit

swi3 SPBC30D10.04 -4.5891 Replication fork protection complex subunit

csn71 SPAC1952.12C -4.3123 COP9/Signalosome subunit 7a

sde2 SPAC31G5.18C -4.2931 Silencing defective protein SPBC27.05 SPBC27.05 -4.2388 Dubious

mpp6 SPACUNK4.11C -4.1176 Nuclear exosome-associated RNA binding protein

SPAC1635.01 SPAC1635.01 -4.0234 Voltage-dependent anion-selective channel

pmp3 SPCC1183.09C -3.9671 Plasma membrane proteolipid

hus1 SPAC20G4.04C -3.9493 Checkpoint clamp complex protein


SPAC1071.09C SPAC1071.09C -3.8619 DNAJ domain protein, DNAJC9 family

csn5 SPAC1687.13C -3.8167 COP9/Signalosome complex subunit 5

SPBP16F5.05C SPBP16F5.05C -3.6932 Ribosome biogenesis protein Nop8

raf1 SPCC613.12C -3.6911 Rik1-associated factor

set1 SPCC306.04C -3.6712 Histone lysine methyltransferase

snt1 SPAC22E12.19 -3.4215 Histone deacetylase complex subunit (predicted)

clr1 SPBC2D10.17 -3.3288 Cryptic loci regulator

arp42 SPAC23D3.09 -3.2565 SWI/SNF and RSC complex subunit

naa30 SPBC15D4.06 -3.0513 NatC N-acetyltransferase complex catalytic subunit (predicted)

rad2 SPAC3G6.06C -2.987 FEN-1 endonuclease hat1 SPAC139.06 -2.9669 Histone acetyltransferase

hmt1 SPCC737.09C -2.836 ATP-binding cassette-type vacuolar membrane transporter

ire1 SPAC167.01 -2.8239 Serine/threonine protein kinase, sensor for unfolded proteins in the ER

ubp8 SPAC13A11.04C -2.7714 SAGA complex ubiquitin C-terminal hydrolase

nup60 SPCC285.13C -2.7603 Nucleoporin

SPBP16F5.08C SPBP16F5.08C -2.7352 Flavin dependent monooxygenase (predicted)

rga8 SPAC13A11.01C -2.7328 Rho-type GTPase activating protein

SPBC651.02 SPBC651.02 -2.716 Bis(5'-adenosyl)-triphosphatase (predicted)

dbl1 SPCC2H8.05C -2.6494 Sequence orphan, localizing to double strand breaks Dbl1

urm1 SPCC548.04 -2.6257 Ubiquitin family protein (predicted)

spt3 SPCC61.02 -2.5745 SAGA complex subunit ngg1 SPBC28F2.10C -2.5184 SAGA complex subunit

atg22 SPAC2G11.13 -2.4811 Vacuolar amino acid efflux transporter

mms22 SPAC6B12.02C -2.4499 DNA repair protein

fep1 SPAC23E2.01 -2.4156 Iron-sensing transcription factor

did2 SPBC13G1.12 2.0066 ESCRT III complex subunit

ppk29 SPBC557.04 2.0439

Ark1/Prk1 family protein kinase

rqc1 SPAC1142.01 2.1391 Ribosome quality control complex (RQC) complex subunit

csi1 SPBC2G2.14 2.1446 Chromosome segregation impaired protein 1


elp6 SPBC3H7.10 2.1562 Elongator complex subunit Elp6 (predicted)

SPBC25H2.03 SPBC25H2.03 2.1751 Vacuolar protein involved in phosphoinositide metabolism (predicted)

bob1 SPBC215.02 2.1891 prefoldin subunit 5 (predicted)

SPAC8C9.12C SPAC8C9.12C 2.2607 Mitochondrial iron ion transporter (predicted)

SPCC1494.08C SPCC1494.08C 2.2622 Conserve fangal protein ptl3 SPAC1A6.05C 2.2921 Triacylglycerol lipase erg5 SPAC19A8.04 2.2957 C-22 sterol desaturase msh2 SPBC19G7.01C 2.3301 MutS protein homolog 2 cbp1 SPBC1105.04C 2.3398 CENP-B homolog

meu29 SPAC25H1.05 2.387 Sequence orphan

ski3 SPCC1919.05 2.4761 Ski complex TPR repeat subunit (predicted)

zfs1 SPBC1718.07C 2.5101

CCCH tandem zinc finger protein, human Tristetraprolin homolog Zfs1, involved in mRNA catabolism

erf4 SPAC3F10.07C 2.5688

Palmitoyltransferase complex subunit

SPAC4H3.06 SPAC4H3.06 2.7796 Sequence orphan

SPCC553.12C SPCC553.12C 2.9294

Transmembrane transporter (predicted)

dot2 SPBC651.05C 3.0537 ESCRT II complex subunit SPAC17A2.11 SPAC17A2.11 3.2024 Sequence orphan

git5 SPBC32H8.07 4.0991

Heterotrimeric G protein beta subunit

SPBC725.10 SPBC725.10 4.709

TspO homolog, involved in the cytoplasmic to mitochondrial transport of haem (predicted)


Table S3 S. cerevisiae RTT107 E-MAP significant genetic interactions (Collins et al, 2007)

Saccharomyces cerevisiae Schizosaccharomyces pombe ortholog

Gene Name

Systematic ID

Interaction Score

Gene NameSystematic

ID Interaction

Score RRM3 YHR031C -10.865 pfh1 SPBC887.14c -

RMI1 YPL024W -7.273 rmi1 SPAC26A3.03c -

MND2 YIR025W -7.008 apc15 SPBC83.04 0.6006

SGS1 YMR190C -5.911 rqh1 SPAC2G11.12 0.8835

RPN6 YDL097C -5.894 rpn6 SPAC23G3.11 -

RPA190 YOR341W -5.662 nuc1 SPBC4C3.05c -

POL30-DAMP YBR088C -5.522 pcn1 SPBC16D10.09 -

YNR048W YNR048W -4.281 ivn1 SPBC11B10.07c -1.7049

GET2 YER083C -4.154 sif1 SPCC1235.06 -

TEL1 YBL088C -4.051 tel1 SPCC23B6.03c -0.3103

POL30-819 YBR088C -3.945 pcn1 SPBC16D10.09 -

SPT4 YGR063C -3.926 spt4 SPBC21C3.16c -

TSA1 YML028W -3.917 tpx1 SPCC576.03c -

AIM4 YBR194W -3.498 saf1 SPCC663.11 -

RTT101 YJL047C -3.477 - - -

TOP3 YLR234W -3.416 top3 SPBC16G5.12c -

REB1 YBR049C -3.317 reb1 SPBC1198.11c -

NUT1 YGL151W -3.316 - - -

SRS2 YJL092W -3.300 srs2 SPAC4H3.05 -5,6676

NUP84 YDL116W -3.219 nup107 SPBC428.01c -

BEM2 YER155C -3.216 - - -

YOR338W YOR338W -3.207 laf1 laf2

SPAC14C4.12c SPCC1682.13

- -

RPN10 YHR200W -3.124 rpn10 SPAC14C4.12c -0.2667

TAH1 YCR060W -3.100 - - -

CLB2 YPR119W -3.040 - - -

SWI6 YLR182W -3.019 cdc10 SPBC336.12c -

SRP40 YKR092C -2.970 srp40 SPBC1711.05 1.4792

SLX5 YDL013W -2.777 rfp1 rfp2

SPAC19A8.10 SPAC343.18

- -0.0238

MSH1 YHR120W -2.593 msh1 SPAC13F5.01c -

DST1 YGL043W -2.550 tsf1 SPAC2044.03c -

CDC10 YCR002C -2.539 spn2 SPAC821.06 -0.5399

XRS2 YDR369C -2.405 nbs1 SPBC6B1.09c -

MRE11 YMR224C -2.343 mre11 SPAC13C5.07 -

NEJ1 YLR265C -2.210 xlf1 SPCC24B10.14c -

ELP2 YGR200C 2.088 epl2 SPCC895.06 -

UME6 YDR207C 2.177 - - -

MMS22 YLR320W 2.195 mms22 SPAC6B12.02c -2,4499

ARD1 YHR013C 2.412 naa10 SPAC15E1.08 -

YTA7 YGR270W 2.495 abo1 abo2

SPAC31G5.19 SPBP22H7.05c

- -0.7466

YML119W YML119W 2.771 - - -

CTR9 YOL145C 2.825 tpr1 SPAC27D7.14c -

RGP1 YDR137W 2.865 sat1 SPBC23E6.08 1.3302


TAF14 YPL129W 3.497 tfg3 SPAC22H12.02 -

VPH2 YKL119C 3.621 vph2 SPCC757.10 0.5963

REI1 YBR267W 4.096 SPCC550.15c SPCC550.15c 0.5156


Table S4 S. pombe brc1 E-MAP significant genetic interactions and its S. cerevisiae orthologs

Schizosaccharomyces pombe Saccharomyces cerevisiae ortholog

Gene Systematic ID Gene Systematic ID Null Interaction with Rtt107

csn1 SPBC215.03C - - apn2 SPBC3D6.10 APN2 YBL019W Viable No hrq1 SPAC23A1.19C HRQ1 YDR291W Viable No ddb1 SPAC17H9.10C - - rad26 SPAC9E9.08 LCD1 YDR499W Essential No ssb3 SPCC23B6.05C RFA3 YJL173C Essential No

pmt3 SPBC365.06 SMT3 YDR510W Essential Physical interaction (Cremona et al. 2012) Synthetic growth defect (Srikumar et al. 2013)

cbf11 SPCC736.08 - - rad1 SPAC1952.07 RAD17 YOR368W Viable No rad9 SPAC664.07C DDC1 YPL194W Viable No rad17 SPAC14C4.13 RAD24 YER173W Viable Phenotypic Suppression (Curcio et al. 2007; Hanway et al. 2002) dcd1 SPBC2G2.13C DCD1 YHR144C Viable No nrl1 SPBC20F10.05 - -

SPCC1442.02 SPCC1442.02 YBP1 YPB2

YBR216C YGL060W

Viable Viable

No No

SPBC1711.09C SPBC1711.09C TVP38 YKR088C Viable No

srs2 SPAC4H3.05 SRS2 YJL092W Viable Negative interaction (Collins et al. 2007; Costanzo et al. 2010; St Onge et al. 2007) Synthetic growth defect (Pan et al. 2006; Tong et al. 2004)

vps60 SPCC162.06C VPS60 YDR486C Viable No pku80 SPBC543.03C YKU80 YMR106C Viable No ppk3 SPAC15A10.13 CEX1 YOR112W Viable No pnk1 SPAC23C11.04C TPP1 YMR156C Viable No

SPBC1711.15C SPBC1711.15C - - SPBC1289.14 SPBC1289.14 - - -

nse6 SPAC11E3.08C KRE29 YER038C Essential Physical interaction (Leung et al. 2011; Ohouo et al. 2010) swi3 SPBC30D10.04 CSM3 YMR048W Viable Positive genetic (St Onge et al. 2007)

csn71 SPAC1952.12C - - sde2 SPAC31G5.18C - -

SPBC27.05 SPBC27.05 - -


mpp6 SPACUNK4.11C MPP6 YNR024W Viable No

SPAC1635.01 SPAC1635.01 POR1 POR2

YNL055C YIL114C

Viable Viable

No No

pmp3 SPCC1183.09C SNA3 PMP3 SNA4

YJL151C YDR276C YDL123W

Viable Viable Viable

No No No

hus1 SPAC20G4.04C MEC3 YLR288C Viable Negative genetic (Costanzo et al. 2010) SPAC1071.09C SPAC1071.09C - -

csn5 SPAC1687.13C - - SPBP16F5.05C SPBP16F5.05C YAR1 YPL239W Viable No

raf1 SPCC613.12C - - set1 SPCC306.04C SET1 YHR119W Viable No snt1 SPAC22E12.19 SNT1 YCR033W Viable No clr1 SPBC2D10.17 - -

arp42 SPAC23D3.09 ARP4 YJL081C Essential naa30 SPBC15D4.06 MAK3 YPR051W Viable

rad2 SPAC3G6.06C RAD27 YKL113C Viable Negative interaction (Costanzo et al. 2010) Synthetic growth defect (Chin et al. 2006; Pan et al. 2006)

hat1 SPAC139.06 HAT1 YPL001W Viable No hmt1 SPCC737.09C - - ire1 SPAC167.01 IRE1 YHR079C Viable No ubp8 SPAC13A11.04C UBP8 YMR223W Viable No nup60 SPCC285.13C NUP60 YAR002W Viable Negative genetic (Costanzo et al. 2010)

SPBP16F5.08C SPBP16F5.08C FMO1 YHR176W Viable No rga8 SPAC13A11.01C RGD2 YFL047W Viable No

SPBC651.02 SPBC651.02 NIT2 YJL126W Viable No dbl1 SPCC2H8.05C - - urm1 SPCC548.04 URM1 YIL008W Viable No spt3 SPCC61.02 SPT3 YDR392W Viable No ngg1 SPBC28F2.10C NGG1 YDR176W Viable No atg22 SPAC2G11.13 ATG22 YCL038C Viable No

mms22 SPAC6B12.02C MMS22 YLR320W Viable Physical interaction (Ho et al. 2002; Mimura et al. 2010; Ohouo et al. 2010) Synthetic growth defect (Baldwin et al. 2005; Chin et al. 2006)

fep1 SPAC23E2.01 - - did2 SPBC13G1.12 DID2 YKR035W-A Viable No


ppk29 SPBC557.04

PRK1 ARK1 ARL1

YIL095W YNL020C YBR059C

Viable Viable Viable

No No No

rqc1 SPAC1142.01 RQC1 YDR333C Viable No csi1 SPBC2G2.14 - - - - elp6 SPBC3H7.10 ELP6 YMR312W Viable No

SPBC25H2.03 SPBC25H2.03 VAC14 YLR386W Viable No bob1 SPBC215.02 GIM5 YML094W Viable No

SPAC8C9.12C SPAC8C9.12C MRS3 MRS4

YJL133W YKR052C

Viable Viable

No No

SPCC1494.08C SPCC1494.08C YBL086C YBL086C Viable No ptl3 SPAC1A6.05C TGL4 YKR089C Viable No erg5 SPAC19A8.04 ERG5 YMR015C Viable No msh2 SPBC19G7.01C MSH2 YOL090W Viable No cbp1 SPBC1105.04C PDC2 YDR081C Viable No

meu29 SPAC25H1.05 - - - - ski3 SPCC1919.05 SKI3 YPR189W Viable No

zfs1 SPBC1718.07C TIS11 CTH1

YLR136C YDR151C

Viable Viable

No No

erf4 SPAC3F10.07C SHR5 YOL110W Viable No SPAC4H3.06 SPAC4H3.06 - - - -

SPCC553.12C SPCC553.12C - - - - dot2 SPBC651.05C SNF8 YPL002C Viable No

SPAC17A2.11 SPAC17A2.11 - - - - git5 SPBC32H8.07 - - - -

SPBC725.10 SPBC725.10 - - - -


Files S1-S3

Available for download as Excel files at http://www.g3journal.org/lookup/suppl/doi:10.1534/g3.115.017251/-/DC1

File S1 Complete Brc1 E-MAP File S2 Brc1 SSL GO analysis File S3 Rtt107 SSL GO analysis


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genetic interaction landscape reveals critical ... · a. sánchez et al. 3 si figure s2 figure s2...

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