Essential gene disruptions reveal complex relationships between phenotypic robustness, pleiotropy, and fitness

Molecular Systems Biology

Volumn 11, Issue 1, 2015, Pages

  Bauer, Christopher R ^a   Li, Shuang ^a   Siegal, Mark L ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

heterogeneity; pleiotropy; robustness; variation

Indexed keywords

ARTICLE; ESSENTIAL GENE; GENE DELETION; GENE DISRUPTION; GENETIC STABILITY; MOLECULAR BIOLOGY; NONHUMAN; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; ALLELE; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; MOLECULAR EVOLUTION; REPRODUCTIVE FITNESS; SACCHAROMYCES CEREVISIAE;

MESSENGER RNA;

ALLELES; DATABASES, GENETIC; EVOLUTION, MOLECULAR; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENES, ESSENTIAL; GENETIC FITNESS; GENETIC PLEIOTROPY; GENOTYPE; IMAGE PROCESSING, COMPUTER-ASSISTED; PHENOTYPE; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE;

EID: 84922875419     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20145264     Document Type: Article

References (49)

1. Aldridge BB, Fernandez-Suarez M, Heller D, Ambravaneswaran V, Irimia D, Toner M, Fortune SM, (2012) Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science 335: 100-104
2. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S, (2004) Bacterial persistence as a phenotypic switch. Science 305: 1622-1625
3. Bergman A, Siegal ML, (2003) Evolutionary capacitance as a general feature of complex gene networks. Nature 424: 549-552
4. Boeger H, Griesenbeck J, Kornberg RD, (2008) Nucleosome retention and the stochastic nature of promoter chromatin remodeling for transcription. Cell 133: 716-726
5. Breslow DK, Cameron DM, Collins SR, Schuldiner M, Stewart-Ornstein J, Newman HW, Braun S, Madhani HD, Krogan NJ, Weissman JS, (2008) A comprehensive strategy enabling high-resolution functional analysis of the yeast genome. Nat Methods 5: 711-718
6. Cai L, Dalal CK, Elowitz MB, (2008) Frequency-modulated nuclear localization bursts coordinate gene regulation. Nature 455: 485-490
7. Cai L, Friedman N, Xie XS, (2006) Stochastic protein expression in individual cells at the single molecule level. Nature 440: 358-362
8. Choi JK, Kim YJ, (2009) Intrinsic variability of gene expression in nucleosome positioning sequences. Nat Genet 41: 498-503
9. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, Prinz J, St Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M, et al, (2010) The genetic landscape of a cell. Science 327: 425-431.
10. Eldar A, Chary VK, Xenopoulos P, Fontes ME, Losõn OC, Dworkin J, Piggot PJ, Elowitz MB, (2009) Partial penetrance facilitates developmental evolution in bacteria. Nature 460: 510-514
11. Eldar A, Elowitz MB, (2010) Functional roles for noise in genetic circuits. Nature 467: 167-173
12. Frank SA, Rosner MR, (2012) Nonheritable cellular variability accelerates the evolutionary processes of cancer. PLoS Biol 10: e1001296
13. Geiler-Samerotte KA, Bauer CR, Li S, Ziv N, Gresham D, Siegal ML, (2013) The details in the distributions: why and how to study phenotypic variability. Curr Opin Biotechnol 4: 752-759
14. Graham JH, Robb DT, Poe AR, (2012) Random phenotypic variation of yeast (Saccharomyces cerevisiae) single-gene knockouts fits a double pareto-lognormal distribution. PLoS ONE 7: e48964
15. Jacobs GH, (2009) Evolution of colour vision in mammals. Philos Trans R Soc Lond B Biol Sci 364: 2957-2967
16. Johnston Jr RJ, Desplan C, (2010) Preview. A penetrating look at stochasticity in development. Cell 140: 610-612
17. Kussell E, Leibler S, (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075-2078
18. Lehner B, (2010) Genes confer similar robustness to environmental, stochastic, and genetic perturbations in yeast. PLoS ONE 5: e9035
19. Levin D, Harari D, Schreiber G, (2011) Stochastic receptor expression determines cell fate upon interferon treatment. Mol Cell Biol 31: 3252-3266
20. Levy SF, Siegal ML, (2008) Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol 6: e264
21. Levy SF, Siegal ML, (2012) The robustness continuum. Adv Exp Med Biol 751: 431-452
22. Levy SF, Ziv N, Siegal ML, (2012) Bet hedging in yeast by heterogeneous, age-correlated expression of a stress protectant. PLoS Biol 10: e1001325
23. Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R, (2006) Interchromosomal interactions and olfactory receptor choice. Cell 126: 403-413
24. Masel J, Siegal ML, (2009) Robustness: mechanisms and consequences. Trends Genet 25: 395-403
25. McCullagh E, Seshan A, El-Samad H, Madhani HD, (2010) Coordinate control of gene expression noise and interchromosomal interactions in a MAP kinase pathway. Nat Cell Biol 12: 954-962
26. Meiklejohn CD, Hartl DL, (2002) A single mode of canalization. Trends Ecol Evol 17: 468-473
27. Miller-Jensen K, Dey SS, Schaffer DV, Arkin AP, (2011) Varying virulence: epigenetic control of expression noise and disease process. Trends Biotechnol 29: 517-525
28. Mnaimneh S, Davierwala AP, Haynes J, Moffat J, Peng WT, Zhang W, Yang X, Pootoolal J, Chua G, Lopez A, Trochesset M, Morse D, Krogan NJ, Hiley SL, Li Z, Morris Q, Grigull J, Mitsakakis N, Roberts CJ, Greenblatt JF, et al, (2004) Exploration of essential gene functions via titratable promoter alleles. Cell 118: 31-44
29. Ohya Y, Sese J, Yukawa M, Sano F, Nakatani Y, Saito TL, Saka A, Fukuda T, Ishihara S, Oka S, Suzuki G, Watanabe M, Hirata A, Ohtani M, Sawai H, Fraysse N, Latgé JP, François JM, Aebi M, Tanaka S, et al, (2005) High-dimensional and large-scale phenotyping of yeast mutants. Proc Natl Acad Sci USA 102: 19015-19020
30. Paaby A, Rockman M, (2013) The many faces of pleiotropy. Trend Genet 29: 66-73
31. Raj A, Rifkin SA, Andersen E, van Oudenaarden A, (2010) Variability in gene expression underlies incomplete penetrance. Nature 463: 913-918
32. Raser JM, O'Shea EK, (2004) Control of stochasticity in eukaryotic gene expression. Science 304: 1811-1814
33. Ribeiro AS, Häkkinen A, Healy S, Yli-Harja O, (2010) Dynamical effects of transcriptional pause-prone sites. Comput Biol Chem 34: 143-148
34. Richardson JB, Uppendahl LD, Traficante MK, Levy SF, Siegal ML, (2013) Histone variant HTZ1 shows extensive epistasis with, but does not increase robustness to, new mutations. PLoS Genet 9: e1003733
35. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, Basu D, Gimotty P, Vogt T, Herlyn M, (2010) A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141: 583-594
36. Rutherford SL, Lindquist S, (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342
37. Sangster TA, Lindquist S, Queitsch C, (2004) Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance. BioEssays 26: 348-362
38. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, Wong KK, Brandstetter K, Wittner B, Ramaswamy S, Classon M, Settleman J, (2010) A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141: 69-80
39. Siegal ML, Bergman A, (2002) Waddington's canalization revisited: developmental stability and evolution. Proc Natl Acad Sci USA 99: 10528-10532
40. Simko GI, Csermely P, (2013) Nodes having a major influence to break cooperation define a novel centrality measure: game centrality. PLoS ONE 8: e67159
41. Soll DR, (1997) Gene regulation during high-frequency switching in Candida albicans. Microbiology 143: 279-288
42. Thattai M, van Oudenaarden A, (2004) Stochastic gene expression in fluctuating environments. Genetics 167: 523-530
43. Tolstoy L, (1877) Anna Karenina. Moscow: The Russian Messenger
44. Trott J, Hayashi K, Surani A, Babu MM, Martinez-Arias A, (2012) Dissecting ensemble networks in ES cell populations reveals micro-heterogeneity underlying pluripotency. Mol BioSyst 8: 744-752
45. Vardi N, Levy S, Assaf M, Carmi M, Barkai N, (2013) Budding yeast escape commitment to the phosphate starvation program using gene expression noise. Curr Biol 23: 2051-2057
46. Venancio TM, Balaji S, Geetha S, Aravind L, (2010) Robustness and evolvability in natural chemical resistance: identification of novel systems properties, biochemical mechanisms and regulatory interactions. Mol BioSyst 6: 1475-1491
47. Wang GZ, Liu J, Wang W, Zhang HY, Lercher MJ, (2011) A gene's ability to buffer variation is predicted by its fitness contribution and genetic interactions. PLoS ONE 6: e17650
48. Yvert G, Ohnuki S, Nogami S, Imanaga Y, Fehrmann S, Schacherer J, Ohya Y, (2013) Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast. BMC Syst Biol 7: 54
49. Ziv N, Siegal ML, Gresham D, (2013) Genetic and nongenetic determinants of cell growth variation assessed by high-throughput microscopy. Mol Biol Evol 30: 2568-2578