1932

Abstract

The complex manner in which organisms respond to changes in their gene dosage has long fascinated geneticists. Oddly, although the existence of dominance implies that dosage reductions often have mild phenotypes, extra copies of whole chromosomes (aneuploidy) are generally strongly deleterious. Even more paradoxically, an extra copy of the genome is better tolerated than is aneuploidy. We review the resolution of this paradox, highlighting the roles of biochemistry, protein aggregation, and disruption of cellular microstructure in that explanation. Returning to life's curious combination of robustness and sensitivity to dosage changes, we argue that understanding how biological robustness evolved makes these observations less inexplicable. We propose that noise in gene expression and evolutionary strategies for its suppression play a role in generating dosage phenotypes. Finally, we outline an unappreciated mechanism for the preservation of duplicate genes, namely preservation to limit expression noise, arguing that it is particularly relevant in polyploid organisms.

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2016-11-23
2024-06-19
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Literature Cited

  1. Alon U. 1.  2007. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 8:450–61 [Google Scholar]
  2. Aury JM, Jaillon O, Duret L, Noel B, Jubin C. 2.  et al. 2006. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–78 [Google Scholar]
  3. Bar-Even A, Paulsson J, Maheshri N, Carmi M, O'Shea E. 3.  et al. 2006. Noise in protein expression scales with natural protein abundance. Nat. Genet. 38:636–43 [Google Scholar]
  4. Barkai N, Leibler S. 4.  2000. Biological rhythms: circadian clocks limited by noise. Nature 403:267–68 [Google Scholar]
  5. Batada NN, Hurst LD. 5.  2007. Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat. Genet. 39:945–49 [Google Scholar]
  6. Becskei A, Kaufmann BB, van Oudenaarden A. 6.  2005. Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat. Genet. 37:937–44 [Google Scholar]
  7. Becskei A, Serrano L. 7.  2000. Engineering stability in gene networks by autoregulation. Nature 405:590–93 [Google Scholar]
  8. Bekaert M, Edger PP, Pires JC, Conant GC. 8.  2011. Two-phase resolution of polyploidy in the Arabidopsis metabolic network gives rise to relative followed by absolute dosage constraints. Plant Cell 23:1719–28 [Google Scholar]
  9. Berg OG. 9.  1978. A model for the statistical fluctuations of protein numbers in a microbial population. J. Theor. Biol. 71:587–603 [Google Scholar]
  10. Birchler JA. 10.  2010. Reflections on studies of gene expression in aneuploids. Biochem. J. 426:119–23 [Google Scholar]
  11. Birchler JA. 11.  2013. Aneuploidy in plants and flies: the origin of studies of genomic imbalance. Semin. Cell Dev. Biol. 24:315–19 [Google Scholar]
  12. Birchler JA. 12.  2014. Facts and artifacts in studies of gene expression in aneuploids and sex chromosomes. Chromosoma 123:459–69 [Google Scholar]
  13. Birchler JA, Riddle NC, Auger DL, Veitia RA. 13.  2005. Dosage balance in gene regulation: biological implications. Trends Genet. 21:219–26 [Google Scholar]
  14. Birchler JA, Veitia RA. 14.  2012. Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. PNAS 109:14746–53 [Google Scholar]
  15. Blakeslee AF, Belling J, Farnham M. 15.  1920. Chromosomal duplication and Mendelian phenomena in Datura mutants. Science 52:388–90 [Google Scholar]
  16. Blanc G, Wolfe KH. 16.  2004. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–91 [Google Scholar]
  17. Blank LM, Lehmbeck F, Sauer U. 17.  2005. Metabolic-flux and network analysis of fourteen hemiascomycetous yeasts. FEMS Yeast Res. 5:545–58 [Google Scholar]
  18. Brandina I, Graham J, Lemaitre-Guillier C, Entelis N, Krasheninnikov I. 18.  et al. 2006. Enolase takes part in a macromolecular complex associated to mitochondria in yeast. Biochim. Biophys. Acta 1757:1217–28 [Google Scholar]
  19. Bridges CB. 19.  1925. Sex in relation to chromosomes and genes. Am. Nat. 59:127–37 [Google Scholar]
  20. Brown CJ, Todd KM, Rosenzweig RF. 20.  1998. Multiple duplications of yeast hexose-transport genes in response to selection in a glucose-limited environment. Mol. Biol. Evol. 15:931–42 [Google Scholar]
  21. Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L. 21.  et al. 2002. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416:507–11 [Google Scholar]
  22. Campanella ME, Chu H, Low PS. 22.  2005. Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane. PNAS 102:2402–7 [Google Scholar]
  23. Charlesworth B. 23.  1979. Evidence against Fisher's theory of dominance. Nature 278:848–49 [Google Scholar]
  24. Clausen R, Goodspeed T. 24.  1925. Interspecific hybridization in Nicotiana. II. A tetraploid glutinosa-tabacum hybrid, an experimental verification of Winge's hypothesis. Genetics 10:278 [Google Scholar]
  25. Coate JE, Doyle JJ. 25.  2015. Variation in transcriptome size: Are we getting the message?. Chromosoma 124:27–43 [Google Scholar]
  26. Codoner FM, Fares MA. 26.  2008. Why should we care about molecular coevolution?. Evol. Bioinform. 4:29–38 [Google Scholar]
  27. Comai L. 27.  2005. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6:836–46 [Google Scholar]
  28. Conant GC. 28.  2014. Comparative genomics as a time machine: how relative gene dosage and metabolic requirements shaped the time-dependent resolution of yeast polyploidy. Mol. Biol. Evol. 31:3184–93 [Google Scholar]
  29. Conant GC, Birchler JA, Pires JC. 29.  2014. Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time. Curr. Opin. Plant Biol. 19:91–98 [Google Scholar]
  30. Conant GC, Wagner A. 30.  2004. Duplicate genes and robustness to transient gene knockouts in Caenorhabditis elegans. Proc. R. Soc. Biol. Sci. 271:89–96 [Google Scholar]
  31. Conant GC, Wolfe KH. 31.  2007. Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Mol. Syst. Biol. 3:129 [Google Scholar]
  32. Cooke J, Nowak MA, Boerlijst M, Maynard-Smith J. 32.  1997. Evolutionary origins and maintenance of redundant gene expression during metazoan development. Trends Genet. 13:360–64 [Google Scholar]
  33. Dekel E, Alon U. 33.  2005. Optimality and evolutionary tuning of the expression level of a protein. Nat. Genet. 436:588–92 [Google Scholar]
  34. Deng X, Hiatt JB, Nguyen DK, Ercan S, Sturgill D. 34.  et al. 2011. Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat. Genet. 43:1179–85 [Google Scholar]
  35. Dephoure N, Hwang S, O'Sullivan C, Dodgson SE, Gygi SP. 35.  et al. 2014. Quantitative proteomic analysis reveals posttranslational responses to aneuploidy in yeast. eLife 3:e03023 [Google Scholar]
  36. Deutschbauer AM, Jaramillo DF, Proctor M, Kumm J, Hillenmeyer ME. 36.  et al. 2005. Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169:1915–25 [Google Scholar]
  37. Dhroso A, Korkin D, Conant GC. 37.  2014. The yeast protein interaction network has a capacity for self-organization. FEBS J. 281:3420–32 [Google Scholar]
  38. Di Talia S, Skotheim JM, Bean JM, Siggia ED, Cross FR. 38.  2007. The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature 448:947–51 [Google Scholar]
  39. Disteche CM. 39.  2012. Dosage compensation of the sex chromosomes. Annu. Rev. Genet. 46:537–60 [Google Scholar]
  40. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH. 40.  2005. Why highly expressed proteins evolve slowly. PNAS 102:14338–43 [Google Scholar]
  41. Durek P, Walther D. 41.  2008. The integrated analysis of metabolic and protein interaction networks reveals novel molecular organizing principles. BMC Syst. Biol. 2:100 [Google Scholar]
  42. Duret L, Chureau C, Samain S, Weissenbach J, Avner P. 42.  2006. The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312:1653–55 [Google Scholar]
  43. Ellis RJ. 43.  2001. Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 26:597–604 [Google Scholar]
  44. Evangelisti AM, Conant GC. 44.  2010. Nonrandom survival of gene conversions among yeast ribosomal proteins duplicated through genome doubling. Genome Biol. Evol. 2:826–34 [Google Scholar]
  45. Ferrell JE, Machleder EM. 45.  1998. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science 280:895–98 [Google Scholar]
  46. Fisher RA. 46.  1928. The possible modification of the response of the wild type to recurrent mutations. Am. Nat. 62:115–26 [Google Scholar]
  47. Fisher RA. 47.  1928. Two further notes on the origin of dominance. Am. Nat. 62:571–74 [Google Scholar]
  48. Fisher RA. 48.  1935. The sheltering of lethals. Am. Nat. 69:446–55 [Google Scholar]
  49. Fraser HB, Hirsh AE, Giaever G, Kumm J, Eisen MB. 49.  2004. Noise minimization in eukaryotic gene expression. PLOS Biol. 2:834–38 [Google Scholar]
  50. Freeling M. 50.  2009. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 60:433–53 [Google Scholar]
  51. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR. 51.  1999. Ploidy regulation of gene expression. Science 285:251–54 [Google Scholar]
  52. Gelbart ME, Kuroda MI. 52.  2009. Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136:1399–410 [Google Scholar]
  53. Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A. 53.  et al. 2003. Global analysis of protein expression in yeast. Nature 425:737–41 [Google Scholar]
  54. Gilchrist MA, Nijhout HF. 54.  2001. Nonlinear developmental processes as sources of dominance. Genetics 159:423–32 [Google Scholar]
  55. Graham JW, Williams TC, Morgan M, Fernie AR, Ratcliffe RG, Sweetlove LJ. 55.  2007. Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 19:3723–38 [Google Scholar]
  56. Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li W-H. 56.  2003. Role of duplicate genes in genetic robustness against null mutations. Nature 421:63–66 [Google Scholar]
  57. Gutiérrez J, Maere S. 57.  2014. Modeling the evolution of molecular systems from a mechanistic perspective. Trends Plant Sci. 19:292–303 [Google Scholar]
  58. Hahn MW. 58.  2009. Distinguishing among evolutionary models for the maintenance of gene duplicates. J. Hered. 100:605–17 [Google Scholar]
  59. Hakes L, Pinney JW, Lovell SC, Oliver SG, Robertson DL. 59.  2007. All duplicates are not equal: the difference between small-scale and genome duplication. Genome Biol. 8:R209 [Google Scholar]
  60. Haldane J. 60.  1930. A note on Fisher's theory of the origin of dominance, and on a correlation between dominance and linkage. Am. Nat. 64:87–90 [Google Scholar]
  61. Haldane JBS. 61.  1933. The part played by recurrent mutation in evolution. Am. Nat. 67:5–9 [Google Scholar]
  62. Hoops S, Sahle S, Gauges R, Lee C, Pahle J. 62.  et al. 2006. COPASI–a COmplex PAthway SImulator. Bioinformatics 22:3067–74 [Google Scholar]
  63. Hughes TR, Roberts CJ, Dai H, Jones AR, Meyer MR. 63.  et al. 2000. Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25:333–37 [Google Scholar]
  64. Huminiecki L, Heldin CH. 64.  2010. 2R and remodeling of vertebrate signal transduction engine. BMC Biol. 8:146 [Google Scholar]
  65. Huthmacher C, Gille C, Holzhutter HG. 65.  2007. Computational analysis of protein-protein interactions in metabolic networks of Escherichia coli and yeast. Genome Inf. 18:162–72 [Google Scholar]
  66. Hyde CC, Ahmed SA, Padlan EA, Miles EW, Davies DR. 66.  1988. Three-dimensional structure of the tryptophan synthase α2β2 multienzyme complex from Salmonella typhimurium. J. Biol. Chem. 263:17857–71 [Google Scholar]
  67. Kacser H, Burns JA. 67.  1981. The molecular basis of dominance. Genetics 97:639–66 [Google Scholar]
  68. Klemm K, Bornholdt S. 68.  2005. Topology of biological networks and reliability of information processing. PNAS 102:18414–19 [Google Scholar]
  69. Ko MS. 69.  1991. A stochastic model for gene induction. J. Theor. Biol. 153:181–94 [Google Scholar]
  70. Korbel JO, Tirosh-Wagner T, Urban AE, Chen XN, Kasowski M. 70.  et al. 2009. The genetic architecture of Down syndrome phenotypes revealed by high-resolution analysis of human segmental trisomies. PNAS 106:12031–36 [Google Scholar]
  71. Kuwada Y. 71.  1911. Maiosis in the pollen mother cells of Zea mays L. (with Plate V.). Bot. Mag. 25:163–81 [Google Scholar]
  72. Lane N, Martin W. 72.  2010. The energetics of genome complexity. Nature 467:929–34 [Google Scholar]
  73. Lee TI, Rinaldi NJ, Robert F, Odom DT, Joseph Z. 73.  et al. 2002. Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298:799–804 [Google Scholar]
  74. Lemos B, Meiklejohn CD, Hartl DL. 74.  2004. Regulatory evolution across the protein interaction network. Nat. Genet. 36:1059–60 [Google Scholar]
  75. Lindsley DL, Sandler L, Baker BS, Carpenter AT, Denell R. 75.  et al. 1972. Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 71:157–84 [Google Scholar]
  76. Luscombe NM, Babu MM, Yu H, Snyder M, Teichmann SA, Gerstein M. 76.  2004. Genomic analysis of regulatory network dynamics reveals large topological changes. Nature 431:308–12 [Google Scholar]
  77. Lynch M, Conery JS. 77.  2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151–55 [Google Scholar]
  78. Lynch M, Conery JS. 78.  2003. The origins of genome complexity. Science 302:1401–4 [Google Scholar]
  79. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M. 79.  et al. 2005. Modeling gene and genome duplications in eukaryotes. PNAS 102:5454–59 [Google Scholar]
  80. Makino T, Hokamp K, McLysaght A. 80.  2009. The complex relationship of gene duplication and essentiality. Trends Genet. 25:152–55 [Google Scholar]
  81. Makino T, McLysaght A. 81.  2010. Ohnologs in the human genome are dosage balanced and frequently associated with disease. PNAS 107:9270–74 [Google Scholar]
  82. Mangan S, Alon U. 82.  2003. Structure and function of the feed-forward loop network motif. PNAS 100:11980–85 [Google Scholar]
  83. Mark RJ, Pang Z, Geddes JW, Uchida K, Mattson MP. 83.  1997. Amyloid β-peptide impairs glucose transport in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J. Neurosci. 17:1046–54 [Google Scholar]
  84. Marygold SJ, Roote J, Reuter G, Lambertsson A, Ashburner M. 84.  et al. 2007. The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol. 8:R216 [Google Scholar]
  85. McAdams HH, Arkin A. 85.  1997. Stochastic mechanisms in gene expression. PNAS 94:814–19 [Google Scholar]
  86. McGrath CL, Gout J-F, Doak TG, Yanagi A, Lynch M. 86.  2014. Insights into three whole-genome duplications gleaned from the Paramecium caudatum genome sequence. Genetics 197:1417–28 [Google Scholar]
  87. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U. 87.  2002. Network motifs: simple building blocks of complex networks. Science 298:824–27 [Google Scholar]
  88. Mitelman F. 88.  2000. Recurrent chromosome aberrations in cancer. Mutat. Res. 462:247–53 [Google Scholar]
  89. Muller H. 89.  1925. Why polyploidy is rarer in animals than in plants. Am. Nat. 59:346–53 [Google Scholar]
  90. Muller HJ. 90.  1932. Further studies on the nature and causes of gene mutations. Proc. Int. Congr. Genet, 6th Ithaca, NY 1213–55 New York: Macmillan [Google Scholar]
  91. Muller HJ. 91.  1935. The origination of chromatin deficiencies as minute deletions subject to insertion elsewhere. Genetica 17:237–52 [Google Scholar]
  92. Newman JR, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M. 92.  et al. 2006. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441:840–46 [Google Scholar]
  93. Nowak MA, Boerlijst MC, Cooke J, Maynard-Smith J. 93.  1997. Evolution of genetic redundancy. Nature 388:167–71 [Google Scholar]
  94. Ohno S. 94.  1970. Evolution by Gene Duplication New York: Springer160 [Google Scholar]
  95. Orr HA. 95.  1991. A test of Fisher's theory of dominance. PNAS 88:11413–15 [Google Scholar]
  96. Ovádi J, Orosz F, Hollán S. 96.  2004. Functional aspects of cellular microcompartmentation in the development of neurodegeneration: mutation induced aberrant protein-protein associations. Mol. Cell. Biochem. 256–257:83–93 [Google Scholar]
  97. Papp B, Pal C, Hurst LD. 97.  2003. Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–97 [Google Scholar]
  98. Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A. 98.  et al. 2010. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468:321–25 [Google Scholar]
  99. Payne JL, Wagner A. 99.  2014. The robustness and evolvability of transcription factor binding sites. Science 343:875–77 [Google Scholar]
  100. Pérez-Bercoff Å, McLysaght A, Conant GC. 100.  2011. Patterns of indirect protein interactions suggest a spatial organization to metabolism. Mol. BioSyst. 7:3056–64 [Google Scholar]
  101. Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H. 101.  et al. 2007. Diet and the evolution of human amylase gene copy number variation. Nat. Genet. 39:1256–60 [Google Scholar]
  102. Phadnis N, Fry JD. 102.  2005. Widespread correlations between dominance and homozygous effects of mutations: implications for theories of dominance. Genetics 171:385–92 [Google Scholar]
  103. Piacentini L, Fanti L, Specchia V, Bozzetti MP, Berloco M. 103.  et al. 2014. Transposons, environmental changes, and heritable induced phenotypic variability. Chromosoma 123:345–54 [Google Scholar]
  104. Plunkett C. 104.  1933. A contribution to the theory of dominance. Am. Nat. 67:84–85 [Google Scholar]
  105. Price RN, Uhlemann AC, Brockman A, McGready R, Ashley E. 105.  et al. 2004. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet 364:438–47 [Google Scholar]
  106. Prill RJ, Iglesias PA, Levchenko A. 106.  2005. Dynamic properties of network motifs contribute to biological network organization. PLOS Biol. 3:e343 [Google Scholar]
  107. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S. 107.  2006. Stochastic mRNA synthesis in mammalian cells. PLOS Biol. 4:e309 [Google Scholar]
  108. Rao CV, Wolf DM, Arkin AP. 108.  2002. Control, exploitation and tolerance of intracellular noise. Nature 420:231–37 [Google Scholar]
  109. Raser JM, O'Shea EK. 109.  2004. Control of stochasticity in eukaryotic gene expression. Science 304:1811–14 [Google Scholar]
  110. Raser JM, O'Shea EK. 110.  2005. Noise in gene expression: origins, consequences, and control. Science 309:2010–13 [Google Scholar]
  111. Rovelet-Lecrux A, Hannequin D, Raux G, Le Meur N, Laquerriere A. 111.  et al. 2006. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat. Genet. 38:24–26 [Google Scholar]
  112. Savageau MA. 112.  1974. Comparison of classical and autogenous systems of regulation in inducible operons. Nature 252:546–49 [Google Scholar]
  113. Schrödinger E. 113.  1944. What is Life? Cambridge: Cambridge Univ. Press [Google Scholar]
  114. Schuster-Böckler B, Conrad D, Bateman A. 114.  2010. Dosage sensitivity shapes the evolution of copy-number varied regions. PLOS ONE 5:e9474 [Google Scholar]
  115. Scienski K, Fay JC, Conant GC. 115.  2015. Patterns of gene conversion in duplicated yeast histones suggests strong selection on a co-adapted macromolecular complex. Genome Biol. Evol. doi: 10.1093/gbe/evv216 [Google Scholar]
  116. Selmecki A, Forche A, Berman J. 116.  2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313:367–70 [Google Scholar]
  117. Seoighe C, Wolfe KH. 117.  1999. Yeast genome evolution in the post-genome era. Curr. Opin. Microbiol. 2:548–54 [Google Scholar]
  118. Seppet EK, Kaambre T, Sikk P, Tiivel T, Vija H. 118.  et al. 2001. Functional complexes of mitochondria with Ca,MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells. Biochim. Biophys. Acta 1504:379–95 [Google Scholar]
  119. Shen-Orr SS, Milo R, Mangan S, Alon U. 119.  2002. Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 31:64–68 [Google Scholar]
  120. Shi Q, Martin R. 120.  2000. Aneuploidy in human sperm: a review of the frequency and distribution of aneuploidy, effects of donor age and lifestyle factors. Cytogenet. Genome Res. 90:219–26 [Google Scholar]
  121. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S. 121.  et al. 2003. α-Synuclein locus triplication causes Parkinson's disease. Science 302:841 [Google Scholar]
  122. Sopko R, Huang D, Preston N, Chua G, Papp B. 122.  et al. 2006. Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 21:319–30 [Google Scholar]
  123. Springer M, Weissman JS, Kirschner MW. 123.  2010. A general lack of compensation for gene dosage in yeast. Mol. Syst. Biol. 6:368 [Google Scholar]
  124. Spudich JL, Koshland D Jr. 124.  1976. Non-genetic individuality: chance in the single cell. Nature 262:467–71 [Google Scholar]
  125. Srere PA. 125.  2000. Macromolecular interactions: tracing the roots. Trends Biochem. Sci. 25:150–53 [Google Scholar]
  126. Stadler LJ. 126.  1929. Chromosome number and the mutation rate in Avena and Triticum. PNAS 15:876 [Google Scholar]
  127. Stoebel DM, Dean AM, Dykhuizen DE. 127.  2008. The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178:1653–60 [Google Scholar]
  128. Sun L, Johnson AF, Li J, Lambdin AS, Cheng J, Birchler JA. 128.  2013. Differential effect of aneuploidy on the X chromosome and genes with sex-biased expression in Drosophila. PNAS 110:16514–19 [Google Scholar]
  129. Swain PS, Elowitz MB, Siggia ED. 129.  2002. Intrinsic and extrinsic contributions to stochasticity in gene expression. PNAS 99:12795–800 [Google Scholar]
  130. Taylor JP, Hardy J, Fischbeck KH. 130.  2002. Toxic proteins in neurodegenerative disease. Science 296:1991–95 [Google Scholar]
  131. Taylor JS, Raes J. 131.  2004. Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38:615–43 [Google Scholar]
  132. Thomas BC, Pedersen B, Freeling M. 132.  2006. Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res. 16:934–46 [Google Scholar]
  133. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M. 133.  et al. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317:916–24 [Google Scholar]
  134. van Hoek MJ, Hogeweg P. 134.  2009. Metabolic adaptation after whole genome duplication. Mol. Biol. Evol. 26:2441–53 [Google Scholar]
  135. Vavouri T, Semple JI, Garcia-Verdugo R, Lehner B. 135.  2009. Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 138:198–208 [Google Scholar]
  136. Veitia RA. 136.  2010. A generalized model of gene dosage and dominant negative effects in macromolecular complexes. FASEB J. 24:994–1002 [Google Scholar]
  137. Veitia RA, Birchler JA. 137.  2015. Models of buffering of dosage imbalances in protein complexes. Biol. Dir. 10:1–11 [Google Scholar]
  138. Veitia RA, Bottani S, Birchler JA. 138.  2013. Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation. Trends Genet. 29:385–93 [Google Scholar]
  139. Veitia RA, Potier MC. 139.  2015. Gene dosage imbalances: action, reaction, and models. Trends Biochem. Sci. 40:309–17 [Google Scholar]
  140. von Dassow G, Meir E, Munro EM, Odell GM. 140.  2000. The segment polarity network is a robust developmental module. Nature 406:188–92 [Google Scholar]
  141. Waddington CH. 141.  1942. Canalization of development and the inheritance of acquired characters. Nature 150:563–65 [Google Scholar]
  142. Wagner A. 142.  2005. Distributed robustness versus redundancy as causes of mutational robustness. BioEssays 27:176–88 [Google Scholar]
  143. Wagner A. 143.  2005. Energy constraints on the evolution of gene expression. Mol. Biol. Evol. 22:1365–74 [Google Scholar]
  144. Wagner A. 144.  2005. Robustness and Evolvability in Living Systems Princeton, NJ: Princeton Univ. Press [Google Scholar]
  145. Wang Z, Zhang J. 145.  2011. Impact of gene expression noise on organismal fitness and the efficacy of natural selection. PNAS 108:E67–76 [Google Scholar]
  146. Wolfe KH, Shields DC. 146.  1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–13 [Google Scholar]
  147. Wright S. 147.  1929. Fisher's theory of dominance. Am. Nat. 63:274–79 [Google Scholar]
  148. Wright S. 148.  1934. Physiological and evolutionary theories of dominance. Am. Nat. 68:24–53 [Google Scholar]
  149. Yanofsky C, Rachmeler M. 149.  1958. The exclusion of free indole as an intermediate in the biosynthesis of tryptophan in Neurospora crassa. Biochim. Biophys. Acta 28:640–41 [Google Scholar]
  150. Zhu J, Pavelka N, Bradford WD, Rancati G, Li R. 150.  2012. Karyotypic determinants of chromosome instability in aneuploid budding yeast. PLOS Genet. 8:e1002719 [Google Scholar]
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