The origins of mutational robustness

Trends in Genetics

Volumn 31, Issue 7, 2015, Pages 373-381

  Fares, Mario A ^a,b  

^a Universitat Politècnica de València   (Spain)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Evolutionary capacitors; Evolvability; Experimental evolution; Gene duplication; Mutational robustness; Regulatory plasticity

Indexed keywords

CAENORHABDITIS ELEGANS; CODING; DUPLICATE GENE; GENE DUPLICATION; GENE MUTATION; GENE SEQUENCE; GENETIC LINKAGE; GENETIC REGULATION; GENETIC TRAIT; MOLECULAR EVOLUTION; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; REDUNDANCY ANALYSIS; REVIEW; SACCHAROMYCES CEREVISIAE; ANIMAL; GENETIC VARIATION; GENOMIC INSTABILITY; GENOTYPE; HUMAN; MUTATION;

ANIMALS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENETIC VARIATION; GENOMIC INSTABILITY; GENOTYPE; HUMANS; MUTATION;

EID: 84937517714     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2015.04.008     Document Type: Review

References (100)

1. Wagner A. Circuit topology and the evolution of robustness in two-gene circadian oscillators. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:11775-11780.
2. Wagner A. The role of robustness in phenotypic adaptation and innovation. Proc. Biol. Sci. 2012, 279:1249-1258.
3. Waddington C.H. Canalization of development and genetic assimilation of acquired characters. Nature 1959, 183:1654-1655.
4. Waddington C.H. Genetic assimilation of an acquired character. Evolution 1953, 7:9.
5. Waddington C.H. Genetic assimilation of the bithorax phenotype. Evolution 1956, 10:13.
6. Rennell D., et al. Systematic mutation of bacteriophage T4 lysozyme. J. Mol. Biol. 1991, 222:67-88.
7. Sinha N., Nussinov R. Point mutations and sequence variability in proteins: redistributions of preexisting populations. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:3139-3144.
8. Edwards J.S., Palsson B.O. Robustness analysis of the Escherichia coli metabolic network. Biotechnol. Prog. 2000, 16:927-939.
9. Raj A., et al. Stochastic mRNA synthesis in mammalian cells. PLoS Biol. 2006, 4:e309.
10. Raser J.M., O'Shea E.K. Noise in gene expression: origins, consequences, and control. Science 2005, 309:2010-2013.
11. Batada N.N., Hurst L.D. Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat. Genet. 2007, 39:945-949.
12. Giaever G., et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature 2002, 418:387-391.
13. White J.K., et al. Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 2013, 154:452-464.
14. Vachias C., et al. Tight coordination of growth and differentiation between germline and soma provides robustness for drosophila egg development. Cell Rep. 2014, 9:531-541.
15. Hartman J.L., 4th, et al. Principles for the buffering of genetic variation. Science 2001, 291:1001-1004.
16. Masel J., Siegal M.L. Robustness: mechanisms and consequences. Trends Genet. 2009, 25:395-403.
17. Wagner A., Wright J. Alternative routes and mutational robustness in complex regulatory networks. Biosystems 2007, 88:163-172.
18. Wagner A. Genotype networks shed light on evolutionary constraints. Trends Ecol. Evol. 2011, 26:577-584.
19. Draghi J.A., et al. Mutational robustness can facilitate adaptation. Nature 2010, 463:353-355.
20. Ferrada E., Wagner A. Evolutionary innovations and the organization of protein functions in genotype space. PLoS ONE 2010, 5:e14172.
21. Hermisson J., Wagner G.P. The population genetic theory of hidden variation and genetic robustness. Genetics 2004, 168:2271-2284.
22. Ancel L.W., Fontana W. Plasticity, evolvability, and modularity in RNA. J. Exp. Zool. 2000, 288:242-283.
23. Goldsmith M., Tawfik D.S. Potential role of phenotypic mutations in the evolution of protein expression and stability. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:6197-6202.
24. Nowak M.A., et al. Evolution of genetic redundancy. Nature 1997, 388:167-171.
25. Montville R., et al. Evolution of mutational robustness in an RNA virus. PLoS Biol. 2005, 3:e381.
26. Fraser H.B., Schadt E.E. The quantitative genetics of phenotypic robustness. PLoS ONE 2010, 5:e8635.
27. Cooper T.F., et al. Effect of random and hub gene disruptions on environmental and mutational robustness in Escherichia coli. BMC Genomics 2006, 7:237.
28. Richardson J.B., et al. Histone variant HTZ1 shows extensive epistasis with, but does not increase robustness to, new mutations. PLoS Genet. 2013, 9:e1003733.
29. Freddolino P.L., et al. Newly identified genetic variations in common Escherichia coli MG1655 stock cultures. J. Bacteriol. 2012, 194:303-306.
30. Freddolino P.L., et al. Fitness landscape transformation through a single amino acid change in the rho terminator. PLoS Genet. 2012, 8:e1002744.
31. Freddolino P.L., Tavazoie S. Beyond homeostasis: a predictive-dynamic framework for understanding cellular behavior. Annu. Rev. Cell Dev. Biol. 2012, 28:363-384.
32. True H.L., Lindquist S.L. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 2000, 407:477-483.
33. Jarosz D.F., Lindquist S. Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 2010, 330:1820-1824.
34. Halfmann R., et al. Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 2012, 482:363-368.
35. Duveau F., Felix M.A. Role of pleiotropy in the evolution of a cryptic developmental variation in Caenorhabditis elegans. PLoS Biol. 2012, 10:e1001230.
36. Milloz J., et al. Intraspecific evolution of the intercellular signaling network underlying a robust developmental system. Genes Dev. 2008, 22:3064-3075.
37. Queitsch C., et al. Hsp90 as a capacitor of phenotypic variation. Nature 2002, 417:618-624.
38. Rutherford S.L., Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 1998, 396:336-342.
39. Sangster T.A., et al. Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance. Bioessays 2004, 26:348-362.
40. Rohner N., et al. Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 2013, 342:1372-1375.
41. Lachowiec J., et al. Hsp90 promotes kinase evolution. Mol. Biol. Evol. 2015, 32:91-99.
42. Fares M.A., et al. Endosymbiotic bacteria: groEL buffers against deleterious mutations. Nature 2002, 417:398.
43. Bogumil D., Dagan T. Chaperonin-dependent accelerated substitution rates in prokaryotes. Genome Biol. Evol. 2010, 2:602-608.
44. Williams T.A., Fares M.A. The effect of chaperonin buffering on protein evolution. Genome Biol. Evol. 2010, 2:609-619.
45. Tokuriki N., Tawfik D.S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 2009, 459:668-673.
46. Ohno S. Evolution by Gene Duplication 1970, Springer Verlag.
47. Ibarra R.U., et al. Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth. Nature 2002, 420:186-189.
48. Barve A., Wagner A. A latent capacity for evolutionary innovation through exaptation in metabolic systems. Nature 2013, 500:203-206.
49. Ohno S. Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin. Cell Dev. Biol. 1999, 10:517-522.
50. Wolfe K.H., Shields D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997, 387:708-713.
51. Castillo-Davis C.I., et al. Selection for short introns in highly expressed genes. Nat. Genet. 2002, 31:415-418.
52. Pal C., et al. Highly expressed genes in yeast evolve slowly. Genetics 2001, 158:927-931.
53. Blanc G., Wolfe K.H. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 2004, 16:1667-1678.
54. Cui L., et al. Widespread genome duplications throughout the history of flowering plants. Genome Res. 2006, 16:738-749.
55. Blanc G., Wolfe K.H. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 2004, 16:1679-1691.
56. Scannell D.R., Wolfe K.H. A burst of protein sequence evolution and a prolonged period of asymmetric evolution follow gene duplication in yeast. Genome Res. 2008, 18:137-147.
57. Conant G.C., Wolfe K.H. Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 2008, 9:938-950.
58. Fares M.A., et al. Rate asymmetry after genome duplication causes substantial long-branch attraction artifacts in the phylogeny of Saccharomyces species. Mol. Biol. Evol. 2006, 23:245-253.
59. Gu Z., et al. Role of duplicate genes in genetic robustness against null mutations. Nature 2003, 421:63-66.
60. VanderSluis B., et al. Genetic interactions reveal the evolutionary trajectories of duplicate genes. Mol. Syst. Biol. 2010, 6:429.
61. Hsiao T.L., Vitkup D. Role of duplicate genes in robustness against deleterious human mutations. PLoS Genet. 2008, 4:e1000014.
62. Conant G.C., Wagner A. Duplicate genes and robustness to transient gene knock-downs in Caenorhabditis elegans. Proc. Biol. Sci. 2004, 271:89-96.
63. Freeling M., Thomas B.C. Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 2006, 16:805-814.
64. Makino T., McLysaght A. Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:9270-9274.
65. Lynch M., Conery J.S. The evolutionary fate and consequences of duplicate genes. Science 2000, 290:1151-1155.
66. Force A., et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
67. Barkman T., Zhang J. Evidence for escape from adaptive conflict?. Nature 2009, 462:E1. discussion E2-3.
68. Des Marais D.L., Rausher M.D. Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 2008, 454:762-765.
69. He X., Zhang J. Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 2005, 169:1157-1164.
70. van Hoof A. Conserved functions of yeast genes support the duplication, degeneration and complementation model for gene duplication. Genetics 2005, 171:1455-1461.
71. Ihmels J., et al. Backup without redundancy: genetic interactions reveal the cost of duplicate gene loss. Mol. Syst. Biol. 2007, 3:86.
72. Plata G., Vitkup D. Genetic robustness and functional evolution of gene duplicates. Nucleic Acids Res. 2014, 42:2405-2414.
73. Guan Y., et al. Functional analysis of gene duplications in Saccharomyces cerevisiae. Genetics 2007, 175:933-943.
74. DeLuna A., et al. Exposing the fitness contribution of duplicated genes. Nat. Genet. 2008, 40:676-681.
75. Musso G., et al. The extensive and condition-dependent nature of epistasis among whole-genome duplicates in yeast. Genome Res. 2008, 18:1092-1099.
76. Liang H., Li W.H. Gene essentiality, gene duplicability and protein connectivity in human and mouse. Trends Genet. 2007, 23:375-378.
77. Liao B.Y., Zhang J. Mouse duplicate genes are as essential as singletons. Trends Genet. 2007, 23:378-381.
78. Makino T., et al. The complex relationship of gene duplication and essentiality. Trends Genet. 2009, 25:152-155.
79. Lynch M., Katju V. The altered evolutionary trajectories of gene duplicates. Trends Genet. 2004, 20:544-549.
80. Keane O.M., et al. Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae. Genome Res. 2014, 24:1830-1841.
81. Conant G.C., Wolfe K.H. Functional partitioning of yeast co-expression networks after genome duplication. PLoS Biol. 2006, 4:e109.
82. Boles E., et al. Characterization of a glucose-repressed pyruvate kinase (Pyk2p) in Saccharomyces cerevisiae that is catalytically insensitive to fructose-1,6-bisphosphate. J. Bacteriol. 1997, 179:2987-2993.
83. Lynch M., et al. The probability of preservation of a newly arisen gene duplicate. Genetics 2001, 159:1789-1804.
84. Fares M.A., et al. The roles of whole-genome and small-scale duplications in the functional specialization of Saccharomyces cerevisiae genes. PLoS Genet. 2013, 9:e1003176.
85. Hakes L., et al. Specificity in protein interactions and its relationship with sequence diversity and coevolution. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:7999-8004.
86. Carretero-Paulet L., Fares M.A. Evolutionary dynamics and functional specialization of plant paralogs formed by whole and small-scale genome duplications. Mol. Biol. Evol. 2012, 29:3541-3551.
87. Kafri R., et al. Transcription control reprogramming in genetic backup circuits. Nat. Genet. 2005, 37:295-299.
88. Koonin E.V. Paralogs and mutational robustness linked through transcriptional reprogramming. Bioessays 2005, 27:865-868.
89. Hurst L.D., Pal C. Dissecting dispensability. Nat. Genet. 2005, 37:214-215.
90. Masel J., Bergman A. The evolution of the evolvability properties of the yeast prion [PSI+]. Evolution 2003, 57:1498-1512.
91. Gould S.J., Vrba E.S. Exaptation - a missing term in the science of form. Paleobiology 1982, 8:12.
92. Price T.D., et al. The role of phenotypic plasticity in driving genetic evolution. Proc. Biol. Sci. 2003, 270:1433-1440.
93. Felix M.A., Wagner A. Robustness and evolution: concepts, insights and challenges from a developmental model system. Heredity 2008, 100:132-140.
94. Giurumescu C.A., et al. Intercellular coupling amplifies fate segregation during Caenorhabditis elegans vulval development. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1331-1336.
95. Shaye D.D., Greenwald I. Endocytosis-mediated downregulation of LIN-12/Notch upon Ras activation in Caenorhabditis elegans. Nature 2002, 420:686-690.
96. Chen N., Greenwald I. The lateral signal for LIN-12/Notch in C. elegans vulval development comprises redundant secreted and transmembrane DSL proteins. Dev. Cell 2004, 6:183-192.
97. Berset T.A., et al. The C. elegans homolog of the mammalian tumor suppressor Dep-1/Scc1 inhibits EGFR signaling to regulate binary cell fate decisions. Genes Dev. 2005, 19:1328-1340.
98. Yoo A.S., et al. Crosstalk between the EGFR and LIN-12/Notch pathways in C. elegans vulval development. Science 2004, 303:663-666.
99. Bennett A.F., Lenski R.E. An experimental test of evolutionary trade-offs during temperature adaptation. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(Suppl 1):8649-8654.
100. Ostrowski E.A., et al. The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli. Proc. Biol. Sci. 2008, 275:277-284.