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Exploration of Essential Gene Functions via Titratable Promoter Alleles
Open accessAbstract
Nearly 20% of yeast genes are required for viability, hindering genetic analysis with knockouts. We created promoter-shutoff strains for over two-thirds of all essential yeast genes and subjected them to morphological analysis, size profiling, drug sensitivity screening, and microarray expression profiling. We then used this compendium of data to ask which phenotypic features characterized different functional classes and used these to infer potential functions for uncharacterized genes. We identified genes involved in ribosome biogenesis (HAS1, URB1, and URB2), protein secretion (SEC39), mitochondrial import (MIM1), and tRNA charging (GSN1). In addition, apparent negative feedback transcriptional regulation of both ribosome biogenesis and the proteasome was observed. We furthermore show that these strains are compatible with automated genetic analysis. This study underscores the importance of analyzing mutant phenotypes and provides a resource to complement the yeast knockout collection.
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“In general, essential genes participated in ~5-fold more negative and positive interactions than nonessential genes, confirming previous estimates (Fig. 5A)(24).”
From A global genetic interaction network maps a wiring diagram of cellular function (2016) · cites this paper as [24]
In the citing paper
“First, consistent with the results of our previous smaller scale surveys (1, 24), essential genes are major hubs and form the basic scaffold of the global genetic interaction network.”
From A global genetic interaction network maps a wiring diagram of cellular function (2016) · cites this paper as [24]
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“This method for simulating mutants mimics experimental Tet-OFF mutants, in which the transcription of a given gene is controlled by a tetracycline- responsive promoter and can be turned off by adding tetracycline to the growth medium [70].”
MethodNovel Method for Genomic Promoter Shuffling by Using Recyclable Cassettes
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Multipurpose Transposon Insertion Libraries for Large-Scale Analysis of Gene Function in Yeast
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“…of a complete collection of S. cerevisiae gene deletion mutants (Giaever et al., 2002; Winzeler et al., 1999), along with libraries of conditional alleles of essential genes (Kanemaki et al., 2003; Mnaimneh et al., 2004), have allowed for systematic genetic analyses to determine gene function.”
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Restricted glycolysis is a primary cause of the reduced growth rate of zinc-deficient yeast cells
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“To investigate this possibility, we used a strain in which the CDC19 promoter was replaced with the doxycycline-repressible TetO 7 promoter ( cdc19 TetO 7 ) , which enabled the repression of WT Pyk1 expression by addition of doxycycline (40).”
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“we crossed strains from the Tet-Promoters Hughes library (Tet-Off) [47] for doxycycline-controlled repression of the NRD1 and NAB3 genes with the Ura8-DsRed Rnr3-GFP reporter strain.”
MethodBenzoic Acid-Inducible Gene Expression in Mycobacteria
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“For instance, over-expression or conditional regulation of genes enables us to map gene function, determine gene essentiality and validate drug targets [3–5].”
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Schaeffer, D., Meaux, S., Clark, A., & van Hoof, A. (2008) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(08)02612-8 · Cited by 7
“These were made as part of a genome-wide effort to put each of the essential yeast genes under control of the TET promoter (Mnaimneh et al., 2004) and are commercially available through Open Biosystems (http://www.openbiosystems.com/ GeneExpression/Yeast/Tet%2DPromoters/).”
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Self-citationChuartzman, S. G., & Schuldiner, M. (2018) · Yeast · doi:10.1002/yea.3312 · Cited by 7
“, 2011); TET‐off promoters for repression of transcription (Mnaimneh et al., 2004); destabilization of mRNA for reduced expression (Breslow et al.”
BackgroundYeast-Based Screens to Target Alpha-Synuclein Toxicity
Brás, I. C., Popova, B., Braus, G. H., & Outeiro, T. F. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9124-2_12 · Cited by 7
Yeast Phenomics—Large-scale Mapping of the Genetic Basis for Organismal Traits
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Yeast as a Model System to Study DNA Damage and DNA Repair
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From functional genomics to systems biology
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“With this approach, Boone’s laboratory conducted 30 SGA screens of 575 essential genes and built the corresponding genetic network [30].”
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Azizoğlu, A., Brent, R., & Rudolf, F. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2019.12.12.874461 · Cited by 7
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“The e ff ect of Mim1 on the functionality of the TOM complex led to its initial identi fi cation as a factor that generally in fl uences the import of mitochondrial proteins (Ishikawa et al. 2004; Mnaimneh et al. 2004).”
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Evaluation of the lower protein limit in the budding yeast Saccharomyces cerevisiae using TIPI-gTOW
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“cerevisiae are as follows: (1) decreasing the expression rate of the transcript using a repressible promoter [15], (2) decreasing the transcription rate or increasing the degradation rate using RNA interference (RNAi) [16], (3) increasing the degradation of mRNA by the decreased abundance by mRNA perturbation (DAmP) m…”
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Adaptation of Organisms by Resonance of RNA Transcription with the Cellular Redox Cycle
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Self-citationStudy Essential Gene Functions by Plasmid Shuffling
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“In this strain, CDC48 is placed under the control of a tetracycline-repressible promoter (PTET-07-CDC48); adding the tetracycline derivative doxycycline (Dox) to the growing yeast culture therefore leads to Cdc48 depletion [51].”
BackgroundSystems Level Modeling of the Cell Cycle Using Budding Yeast
Ingalls, B., Duncker, B. P., Kim, D. R., & McConkey, B. J. (2007) · Cancer Informatics · doi:10.1177/117693510700300020 · Cited by 6
“These include strain collections for systematic gene deletion (Winzeler et al. 1999, available from EUROSCARF, http://web.uni-frankfurt.de/ fb15/mikro/euroscarf/), TAP (tandem affinity puri fi cation)-fusions (Ghaemmaghami et al. 2003, available from Open Biosystems; Gavin et al. 2006, available from EUROSCARF), GFP fu…”
BackgroundTang, M., Bai, Y., Fan, T.-P., Zheng, X., & Cai, Y. (2021) · Systems Microbiology and Biomanufacturing · doi:10.1007/s43393-021-00053-9 · Cited by 5
Noise and non-linearities in high-throughput data
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“ied the Bayesian spectral method on two different data sets. The first one is the measurements of the transcription levels under different experimental conditions of 215 mutants of essential yeast genes [18]. The dataset was extracted by the authors from microarray measurements of about 5000 genes of the budding yeast S.…”
MethodPredicting gene ontology annotations of orphan GWAS genes using protein-protein interactions
Kuppuswamy, U., Ananthasubramanian, S., Wang, Y., Balakrishnan, N., & Ganapathiraju, M. K. (2014) · Algorithms for Molecular Biology · doi:10.1186/1748-7188-9-10 · Cited by 5
“The Mnaimneh gene expression data set [33] was used to generate a detailed list of ranked predictions by the label similarity-incorporated kNN classifiers.”
MethodIn-Frame Deletion of Escherichia Coli Essential Genes in Complex Regulon
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Family-Specific Gains and Losses of Protein Domains in the Legume and Grass Plant Families
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“Cultures from the essential doxycycline-repressible (“Tet-off”) promoter collection (Mnaimneh et al. 2004) were screened similarly, except that an additional series of plates were used for the screen, which included 10 μg/ml doxycycline to effect repression of the essential library gene, as…”
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Self-citationBédard, C., Gagnon‐Arsenault, I., Boisvert, J., Plante, S., Dubé, A. K., Pageau, A., Fijarczyk, A., Sharma, J., Maroc, L., Shapiro, R. S., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.13.571438 · Cited by 5
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“, 2008) or the TetO7-promoter mutant collection (Hughes et al., 2000; Mnaimneh et al., 2004).”
BackgroundMa, Y., Zhou, X., Liu, Z., & Wu, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113518 · Cited by 4
“Previous studies have shown that gene duplications were supposed to be one of the primary driving forces of genetic evolution, and gene duplications can occur through various mechanisms, including tandem duplications, segmental duplications and retroposition [45,46].”
BackgroundCharacterization of promoters in Escherichia coli and application for xylitol synthesis
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“…data were obtained from the transcription factor deletion analyses of Iyer and colleagues (Hu et al., 2007) and from a variety of experiments collected by McCord et al., and provided to us (Chua et al., 2006; Hughes et al., 2000; Ihmels et al., 2004; McCord et al., 2007; Mnaimneh et al., 2004).”
Saccharomyces cerevisiaeEssential Genes with an Opi− Phenotype
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“Addition of 10 μg/mL Dox, on the other hand, switches off the promoter activity.(28,34)”
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Liu, W., Li, D., Liu, Q., Zhu, Y., & He, F. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-s11-s15 · Cited by 4
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Self-citationAppendix A1: Yeast Nomenclature Systematic Open Reading Frame (ORF) and Other Genetic Designations
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“This finding suggests that genes with more essential cellular functions are more likely central hubs in the coevolution network ( 1 , 2 , 5 , 32 , 60 ).”
Örn, O. E., Hagman, A., Ismail, M., Eriksson, N. L., & Hatti‐Kaul, R. (2024) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-024-13256-6 · Cited by 3
“…to make use of inducible promoters, which allows fine tuning of gene expression levels, but these systems have limitations when scaling up in terms of inducer costs, hypersensitivity to inducer concentration, and transcriptional heterogeneity between cells (Mnaimneh et al. 2004; Siegele & Hu 1997).”
Experimental evolution of gene essentiality in bacteria
Bao, L., Zhu, Z., Ismail, A., Zhu, B., Anandan, V., Whiteley, M., Kitten, T. O., & Xu, P. (2025) · mBio · doi:10.1128/mbio.03005-25 · Cited by 6
“Traditional approaches, such as conditional promoter-shutoff (56, 57), antisense RNA knockdowns (58) and CRISPR interference (59, 60), while valuable, may exhibit limitations, including incomplete target gene silencing and suboptimal design efficacy (60), thereby potentially compromising the…”
Silencing of Nicotiana benthamiana Neuroblastoma-Amplified Genecauses ER stress and cell death
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“Sec39p was first identified as an essential protein involved in ER-Golgi transport in a large-scale promoter shutoff analysis of essential yeast genes [32].”
BackgroundThe Modest Beginnings of One Genome Project
Kaback, D. B. (2013) · Genetics · doi:10.1534/genetics.113.151258 · Cited by 3
“I wanted to produce gene knockout mutants for the differentially expressed sequences, experiments that could lead to a better understanding of meiosis.”
BackgroundMethodTOM and SAM Machineries in Mitochondrial Protein Import and Outer Membrane Biogenesis
(2007) · The Enzymes · doi:10.1016/s1874-6047(07)25012-7 · Cited by 3
The centromeric histone CenH3 is recruited into the tombusvirus replication organelles
González, P. A., & Nagy, P. D. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010653 · Cited by 3
Petrík, T., Brzáčová, Z., Sepšiová, R., Veljačiková, K., & Tomáška, Ľ. (2024) · Yeast · doi:10.1002/yea.3971 · Cited by 2
“Other approaches to reduce the level of the POI are to employ (1) hypomorphic alleles of the corresponding genes (Breslow et al., 2008; Mnaimneh et al., 2004), (2) a system to sequester nuclear proteins in the cytoplasm (anchor ‐ away) (Haruki et al., 2008), and (3) methods based on the regulated…”
Sanz, A. B., Díez-Muñiz, S., Moya, J., Petryk, Y., Nombela, C., Rodríguez-Peña, J. M., & Arroyo, J. (2022) · Journal of Fungi · doi:10.3390/jof8070718 · Cited by 4
“As an alternative, the yeast Tet-promoters Hughes collection (yTHC) [29] is available.”
MethodImproved functional overview of protein complexes using inferred epistatic relationships
Ryan, C. J., Greene, D., Guénolé, A., van Attikum, H., Krogan, N. J., Cunningham, P., & Cagney, G. (2011) · BMC Systems Biology · doi:10.1186/1752-0509-5-80 · Cited by 3
“[4-8].”
Self-citationQuantitative cell array screening to identify regulators of gene expression
Kainth, P., & Andrews, B. (2009) · Briefings in Functional Genomics · doi:10.1093/bfgp/elp047 · Cited by 3
“Analysis of essential gene function on reporter genes can also be examined more directly by screening other available yeast arrays of essential genes including: (1) arrays of tetracycline-repressible alleles [54, 55], (2) temperature sensitive strains and (3) alleles which contain a disruption in the 30 untranslated r…”
BackgroundSelf-citationHost Factors in Viral Life Cycles
Pérez‐Vilaró, G., Jungfleisch, J., Saludes, V., Scheller, N., Giménez‐Barcons, M., & Díez, J. (2012) · Mathematical Modelling of Natural Phenomena · doi:10.1051/mmnp/20127509 · Cited by 3
“These comprise (i) a gene deletion mutant collection covering around 85% of all yeast genes in which each strain contains a deletion of one non-essential gene [83], (ii) a downregulable essential-gene library that allows the study of essential genes [52], and (iii) gene libraries with fluorescent or affinity tags that…”
BackgroundSystematic Phenotyping of Plant Development in Arabidopsis thaliana
(2014) · CRC Press eBooks · doi:10.1201/b16437-9 · Cited by 4
Yeast Genetics as a Powerful Tool to Study Human Diseases
Dabas, P., Kumar, D., & Sharma, N. (2017) · Springer eBooks · doi:10.1007/978-981-10-2621-8_8 · Cited by 3
Integrating yeast chemical genomics and mammalian cell pathway analysis
Zhou, F.-L., Li, S. C., Zhu, Y., Guo, W.-J., Shao, L.-J., Nelson, J., Simpkins, S. W., Yang, D., Liu, Q., Yashiroda, Y., et al. (2019) · Acta Pharmacologica Sinica · doi:10.1038/s41401-019-0231-y · Cited by 3
Self-citationBreitenbach, M., Dickinson, J. R., & Laun, P. (2007) · Methods in microbiology · doi:10.1016/s0580-9517(06)36015-1 · Cited by 3
Evolutionary Genomics of Yeasts
Dujon, B. (2010) · Wiley eBooks · doi:10.1002/9780470570418.ch6 · Cited by 2
Coorey, N. (2017) · doi:10.26686/wgtn.17067545.v1 · Cited by 2
“Several other comprehensive mutant libraries are also available to investigate essential genes including the essential heterozygous diploid gene deletion libray, the decreased abundance by mRNA perturbation (DAmP) library (Schuldiner et al., 2005) and the TET-off library (Mnaimneh et al., 2004).”
BackgroundJann, J., Gagnon‐Arsenault, I., Pageau, A., Dubé, A. K., Fijarczyk, A., Durand, R., & Landry, C. R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.29.656836 · Cited by 3
“Yeast strain construction (Supplementary Figure 2A) The ScPDR1 -DOX strain was generated based on the Yeast Tet-Promoters Hughes Collection (yTHC) 36 .”
Discovery and development of new antibacterial drugs
Elassal, E. S., Fahmy, A., Saad, A. N. M., Ali, A. H., Elshenety, A. H., Badr, O. A., Amer, A. N., Fouda, W. M., & Elshaier, Y. A. M. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-18866-4.00012-2 · Cited by 2
Yeast: a microbe with macro-implications to antimicrobial drug discovery
Balibar, C. J., & Roemer, T. (2015) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv038 · Cited by 2
1 Introduction to Functional Analysis in Yeast
Oliver, S. G. (2007) · Methods in microbiology · doi:10.1016/s0580-9517(06)36001-1 · Cited by 2
Identification of Inhibitors of Chromatin Modifying Enzymes Using the Yeast Phenotypic Screens
Newcomb, B., & Bedalov, A. (2009) · Methods in molecular biology · doi:10.1007/978-1-59745-540-4_8 · Cited by 2
Parallel Real-Time PCR on a Chip for Genetic Tug-of-War (gTOW) Method
Naito, T., Yatsuhashi, A., Kaji, N., Ando, T., Sato, K. Z., Moriya, H., Kitano, H., Yasui, T., Tokeshi, M., & Baba, Y. (2013) · Analytical Sciences · doi:10.2116/analsci.29.367 · Cited by 2
Chapter 3 Synthetic Genetic Interactions
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A dual system to manipulate protein levels for DNA replication- and cell cycle-related studies
García‐Rodríguez, N., & Ulrich, H. D. (2019) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2018.12.038 · Cited by 2
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Regulation of telomere silencing by the core histones–autophagy–Sir2 axis
Mei, Q., Yu, Q., Li, X., Chen, J., & Yu, X. (2022) · Life Science Alliance · doi:10.26508/lsa.202201614 · Cited by 2
“Meanwhile, knockdown of CRM1 in TetO7-CRM1 mutant, where the CRM1 promoter was replaced with TetO7 and CRM1 transcription, was shut off by doxycycline treatment (Fig S2E) (Mnaimneh et al, 2004; Yu et al, 2017), impeded rapamycin-induced degradation of Sir2 (Fig S2F).”
BackgroundThe Ycx1 protein encoded by the yeast YDL206W gene plays a role in calcium and calcineurin signaling
Lee, G. M., Weng, F., Cranley, J., Rajasekhar, A., Stoeckel, M., Kane, T., Tisi, R., & Wang, Y. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104647 · Cited by 2
“These include the systematic deletion library for nonessential genes (1), the conditional disruption library for essential genes (2), and the epitope-tagged yeast ORF libraries (3, 4).”
BackgroundKnoblach, B., & Rachubinski, R. A. (2023) · Traffic · doi:10.1111/tra.12923 · Cited by 2
“As some PI effector genes are essential for cell viability, we constructed promoter shutoff strains that temporarily repress the expression of a target gene upon addition of doxycycline (DOX) 19,20 and which also express chromosomally integrated sequence encoding the peroxisomal reporter, GFP-PTS1.”
BackgroundKim, I., Lee, H., Lee, K., Han, S. K., Kim, D., & Kim, S. (2019) · Scientific Reports · doi:10.1038/s41598-019-48273-3 · Cited by 2
Clustering labeled data and cross-validation for classification with few positives in yeast
Trochesset, M., & Bonner, A. J. (2004) · Cited by 2
Self-citationMachine learning approaches to biological sequence and phenotype data analysis
Min, R. (2010) · TSpace (University of Toronto) · Cited by 2
Metadata
- Authors
- Mnaimneh, S., Davierwala, A. P., Haynes, J., Moffat, J., Peng, W.-T., Zhang, W., Yang, X., Pootoolal, J., Chua, G., Lopez, A., Trochesset, M., Morse, D., Krogan, N. J., Hiley, S. L., Li, Z., Morris, Q., Grigull, J., Mitsakakis, N., Roberts, C. J., Greenblatt, J. F., Boone, C., Kaiser, C. A., Andrews, B. J., & Hughes, T. R.
- Affiliations
- University of Toronto (CA)
- Massachusetts Institute of Technology (US)
- Merck & Co., Inc., Rahway, NJ, USA (United States) (US)
- Corresponding author
- Hughes, Timothy R
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2004-07
- Volume
- 118
- Issue
- 1
- Pages
- 31-44
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W1974220691
- Cited by
- 604
- References
- 64
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 17 · 2023: 15 · 2022: 22 · 2021: 21 · 2020: 14 · 2019: 17 · 2018: 17 · 2017: 21 · 2016: 23 · 2015: 26 · 2014: 30 · 2013: 28 · 2012: 32
- FWCI
- 14.21
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 3303 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- essential genes, Saccharomyces cerevisiae, gene function prediction, ribosome biogenesis, protein secretion, mitochondrial protein import, aminoacylation, proteasome, mutant phenotypes
- MeSH terms
- Alleles, Pharmaceutical Preparations, Genes, Fungal, Mitochondria, Models, Genetic, Promoter Regions, Genetic, Protein Processing, Post-Translational, Ribosomal Proteins, RNA, Transfer, Saccharomyces cerevisiae, Transcription, Genetic, Gene Expression Regulation, Fungal, Gene Deletion, Genes, Essential, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Feedback, Physiological, Saccharomyces cerevisiae Proteins
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