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Transgenerational Epigenetic Inheritance: Prevalence, Mechanisms, and Implications for the Study of Heredity and Evolution

Eva Jablonka and Gal Raz
The Quarterly Review of Biology
Vol. 84, No. 2 (June 2009), pp. 131-176
DOI: 10.1086/598822
Stable URL: http://www.jstor.org/stable/10.1086/598822
Page Count: 46
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Transgenerational Epigenetic Inheritance: Prevalence, Mechanisms, and Implications for the Study of Heredity and Evolution
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Abstract

ABSTRACT This review describes new developments in the study of transgenerational epigenetic inheritance, a component of epigenetics. We start by examining the basic concepts of the field and the mechanisms that underlie epigenetic inheritance. We present a comprehensive review of transgenerational cellular epigenetic inheritance among different taxa in the form of a table, and discuss the data contained therein. The analysis of these data shows that epigenetic inheritance is ubiquitous and suggests lines of research that go beyond present approaches to the subject. We conclude by exploring some of the consequences of epigenetic inheritance for the study of evolution, while also pointing to the importance of recognizing and understanding epigenetic inheritance for practical and theoretical issues in biology.

Notes and References

This item contains 236 references.

References
  • ['Adam M., Murali B., Glenn N. O., Potter S. S. 2008. Epigenetic inheritance based evolution of antibiotic resistance in bacteria. BMC Evolutionary Biology 8:52.']
  • ['Agrawal A. A., Laforsch C., Tollrian R. 1999. Transgenerational induction of defences in animals and plants. Nature 401(6748):60–63.']
  • ['Alleman M., Doctor J. 2000. Genomic imprinting in plants: observations and evolutionary implications. Plant Molecular Biology 43(2–3):147–161.']
  • ['Allen J. A., editor. 2004. Issue on plant polyploidy. Biological Journal of the Linnean Society82(4):409–700.']
  • ['Allen N. D., Norris M. L., Surani M. A. 1990. Epigenetic control of transgene expression and imprinting by genotype‐specific modifiers. Cell 61(5):853–861.']
  • ['Allis C. D., Jenuwein T., Reinberg D., Caparros M.‐L., editors. 2007. Epigenetics. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Allshire R. C., Selker E. U. 2007. Fungal models for epigenetic research: Schizosaccharomyces pombe and Neurospora crassa. Pages 101–125 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Anway M. D., Cupp A. S., Uzumcu M., Skinner M. K. 2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308(5727):1466–1469.']
  • ['Anway M. D., Leathers C., Skinner M. K. 2006a. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult‐onset disease. Endocrinology 147(12):5515–5523.']
  • ['Anway M. D., Memon M. A., Uzumcu M., Skinner M. K. 2006b. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. Journal of Andrology 27(6):868–879.']
  • ['Avital E., Jablonka E. 2000. Animal Traditions: Behavioural Inheritance in Evolution. Cambridge (UK): Cambridge University Press.']
  • ['Badyaev A. V. 2005. Stress‐induced variation in evolution: from behavioural plasticity to genetic assimilation. Proceedings of the Royal Society of London, Series B: Biological Sciences 272(1566):877–886.']
  • ['Balaban N. Q., Merrin Q. J., Chait R., Kowalik L., Leibler S. 2004. Bacterial persistence as a phenotypic switch. Science 305(5690):1622–1625.']
  • ['Bantignies F., Cavalli G. 2006. Cellular memory and dynamic regulation of polycomb group proteins. Current Opinion in Cell Biology 18(3):275–283.']
  • ['Barlow D. P., Bartolomei M. S. 2007. Genomic imprinting in mammals. Pages 357–373 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Bateman R. M., DiMichele W. A. 2002. Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited. Pages 109–159 in Developmental Genetics and Plant Evolution, edited by Q. C. B. Cronk et al. London (UK): Taylor & Francis.']
  • ["Bateson P., Barker D., Clutton‐Brock T., Deb D., D'Udine B., Foley R. A., Gluckman P., et al. 2004. Developmental plasticity and human health. Nature 430(6998):419–421."]
  • ['Baulcombe D. C. 2007. Amplified silencing. Science 315(5809):199–200.']
  • ['Baxa U., Cassese T., Kajava A. V., Steven A. C. 2006. Structure, function, and amyloididogenesis of fungal prions: filament polymorphisms and prions variants. Advances in Protein Chemistry 73:125–180']
  • ['Baylin S. B., Jones P. A. 2007. Epigenetic determinants of cancer. Pages 457–476 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Bean C. J., Schaner C. E., Kelly W. G. 2004. Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nature Genetics 36(1):100–105.']
  • ['Beisson J., Sonneborn T. M. 1965. Cytoplasmic inheritance of the organization of the cell cortex in Paramecium aurelia. Proceedings of the National Academy of Sciences USA 53(2):275–282.']
  • ['Belyaev D. K., Borodin P. M. 1982. The influence of stress on variation and its role in evolution. Biologisches Zentralblatt 100:705–714.']
  • ['Belyaev D. K., Ruvinsky A. O., Borodin P. M. 1981a. Inheritance of alternative states of the fused gene in mice. Journal of Heredity 72:107–112.']
  • ['Belyaev D. K., Ruvinsky A. O., Trut L. N. 1981b. Inherited activation‐inactivation of the star gene in foxes: its bearing on the problem of domestication. Journal of Heredity 72(4):267–274.']
  • ['Belyaev D. K., Ruvinsky A. O., Agulnik A. I., Agulnik S. I. 1983. Effect of hydrocortisone on the frequency and inheritance of the fused gene in mice. Genetika 64(4):275–281.']
  • ['Benkemoun L., Saupe S. J. 2006. Prion proteins as genetic material in fungi. Fungal Genetics and Biology 43(12):789–803.']
  • ['Bennett S. T., Wilson A. J., Esposito L., Bouzekri N., Undlien D. E., Cucca F., Nisticò L., et al. 1997. Insulin VNTR allele‐specific effect in type 1 diabetes depends on identity of untransmitted paternal allele. Nature Genetics 17(3):350–352.']
  • ['Berger S. L. 2007. The complex language of chromatin regulation during transcription. Nature 447(7143):407–412.']
  • ['Bestor T. H. 1990. DNA methylation: evolution of a bacterial immune function into a regulator of gene expression and genome structure in higher eukaryotes. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 326(1235):179–187.']
  • ['Bird A. P. 1995. Gene number, noise reduction and biological complexity. Trends in Genetics 11(3):94–100.']
  • ['Blasco M. A. 2007. The epigenetic regulation of mammalian telomeres. Nature Reviews Genetics 8(4):299–309.']
  • ['Blewitt M. E., Vickaryous N. K., Paldi A., Koseki H., Whitelaw E. 2006. Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genetics 2(4):399–405.']
  • ['Bossdorf O., Richards C. L., Pigliucci M. 2008. Epigenetics for ecologists. Ecology Letters 11(2):106–115.']
  • ['Brink R. A. 1973. Paramutation. Annual Review of Genetics 7:129–152.']
  • ['Buiting K., Groβ S., Lich C., Gillessen‐Kaesbach G., El‐Maarri O., Horsthemke B. 2003. Epimutations in Prader‐Willi and Angelman syndromes: a molecular study of 136 patients with an imprinting defect. American Journal of Human Genetics 72(3):571–577.']
  • ['Burdge G. C., Slater‐Jefferies J., Torrens C., Phillips E. S., Hanson M. A., Lillycrop K. A. 2007. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. British Journal of Nutrition 97(3):435–439.']
  • ['Buss L. W. 1987. The Evolution of Individuality. Princeton (NJ): Princeton University Press.']
  • ['Campbell P., editor. 2007. Follow the curve: the forces that shape cell membranes. Nature 447(7143 Insight):353–500.']
  • ['Casadesús J., Low D. 2006. Epigenetic gene regulation in the bacterial world. Microbiology and Molecular Biology Reviews 70(3):830–856.']
  • ['Cavalier‐Smith T. 2004. The membranome and membrane heredity in development and evolution. Pages 335–351 in Organelles, Genomes and Eukaryote Phylogeny, edited by R. P. Hirt and D. S. Horner. Boca Raton (FL): CRC Press.']
  • ['Cerutti H., Casas‐Mollano J. A. 2006. On the origin and functions of RNA‐mediated silencing: from protists to man. Current Genetics 50(2):81–99.']
  • ['Chandler V. L. 2007. Paramutation: from maize to mice. Cell 128(4):641–645.']
  • ['Chandler V. L., Eggleston W. B., Dorweiler J. E. 2000. Paramutation in maize. Plant Molecular Biology 43(2–3):121–145.']
  • ['Chang H.‐S., Anway M. D., Rekow S. S., Skinner M. K. 2006. Transgenerational epigenetic imprinting of the male germline by endocrine disruptor exposure during gonadal sex determination. Endocrinology 147(12):5524–5541.']
  • ['Chien P., Weissman J. S., DePace A. H. 2004. Emerging principles of conformation‐based prion inheritance. Annual Review of Biochemistry 73:617–656.']
  • ['Chong S., Vickaryous N., Ashe A., Zamudio N., Youngson N., Hemley S., Stopka T., et al. 2007. Modifiers of epigenetic reprogramming show paternal effects in the mouse. Nature Genetics 39(5):614–622.']
  • ["Čikoš Š., Veselá J., Il'ková G., Rehák P., Czikková S., Koppel J. 2005. Expression of beta adrenergic receptors in mouse oocytes and preimplantation embryos. Molecular Reproduction and Development 71(2):145–153."]
  • ['Colot V., Rossignol J. L. 1999. Eukaryotic DNA methylation as an evolutionary device. BioEssays 21(5):402–411.']
  • ['Cormier S., Vandormael‐Pournin S., Babinet C., Cohen‐Tannoudji M. 2004. Developmental expression of the Notch signaling pathway genes during mouse preimplantation development. Gene Expression Patterns 4(6):713–717.']
  • ['Costa Y., Speed R. M., Gautier P., Semple C. A., Maratou K., Turner J. M. A., Cooke H. J. 2006. Mouse MAELSTROM: the link between meiotic silencing of unsynapsed chromatin and microRNA pathway? Human Molecular Genetics 15(15):2324–2334.']
  • ['Crews D., Gore A. C., Hsu T. S., Dangleben N. L., Spinetta M., Schallert T., Anway M. D., Skinner M. K. 2007. Transgenerational epigenetic imprints on mate preference. Proceedings of the National Academy of Sciences USA 104(14):5942–5946.']
  • ['Cropley J. E., Suter C. M., Beckman K. B., Martin D. I. K. 2006. Germ‐line epigenetic modification of the murine Avy allele by nutritional supplementation. Proceedings of the National Academy of Sciences USA 103(46):17308–17312.']
  • ['Csaba G., Karabélyos C., Inczefi‐Gonda A., Pallinger E. 2005. Three‐generation investigation on serotonin content in rat immune cells long after β‐endorphin exposure in late pregnancy. Hormone and Metabolic Research 37:172–177.']
  • ['Cullen B. R. 2004. Transcription and processing of human microRNA precursors. Molecular Cell 16(6):861–865.']
  • ['Cullis C. A. 2005. Mechanisms and control of rapid genomic changes in flax. Annals of Botany 95(1):201–206.']
  • ['Delage Y., Goldsmith M. 1912. The Theories of Evolution. Trans. André Tridon. New York: B. W. Huebsch.']
  • ['Dobzhansky T. 1937. Genetics and the Origin of Species. New York: Columbia University Press.']
  • ['Dubnau D., Losick R. 2006. Bistability in bacteria. Molecular Microbiology 61(3):564–572.']
  • ['Dubrova Y. E. 2003. Radiation‐induced transgenerational instability. Oncogene 22(45):7087–7093.']
  • ['Ekwall K. 2007. ‘Arc’ escorts siRNAs in heterochromatin assembly. Nature Structural and Molecular Biology 14(3):178–179.']
  • ['Felsenfeld G., Groudine M. 2003. Controlling the double helix. Nature 421(6921):448–453.']
  • ['Flanagan J. M., Popendikyte V., Pozdniakovaite N., Sobolev M., Assadzadeh A., Schumacher A., Zangeneh M., et al. 2006. Intra‐ and interindividual epigenetic variation in human germ cells. American Journal of Human Genetics 79(1):67–84.']
  • ['Flintoft L., editor. 2007. Focus on: epigenetics. Nature Reviews Genetics 8(4):245–314.']
  • ['Fontdevila A. 2005. Hybrid genome evolution by transposition. Cytogenetic and Genome Research110(1):49–55.']
  • ['Fothergill P. G. 1952. Historical Aspects of Organic Evolution. London (UK): Hollis and Carter.']
  • ['Frankel J. 1989. Pattern Formation Ciliate Studies and Models. New York: Oxford University Press.']
  • ['Genereux D. P., Miner B. E., Bergstrom C. T., Laird C. D. 2005. A population‐epigenetic model to infer site‐specific methylation rates from double‐stranded DNA methylation patterns. Proceedings of the National Academy of Sciences USA 102(16):5802–5807.']
  • ['Ginsburg S., Jablonka E. 2008. Epigenetic learning in non‐neural organisms. Journal of Biosciences 33(4).']
  • ['Gluckman P., Hanson M. 2005. The Fetal Matrix: Evolution, Development and Disease. Cambridge (UK): Cambridge University Press.']
  • ['Gluckman P. D., Hanson M. A., Beedle A. S. 2007. Non‐genomic transgenerational inheritance of disease risk. BioEssays 29(2):145–154.']
  • ['Goldschmidt R. B. 1940. The Material Basis of Evolution. New Haven (CT): Yale University Press.']
  • ['Gottlieb G. 2002. Developmental‐behavioral initiation of evolutionary change. Psychological Review 109(2):211–218.']
  • ['Grandjean V., Hauck Y., Beloin C., Le Hégarat F., Hirschbein L. 1998. Chromosomal inactivation of Bacillus subtilisexfusants: a prokaryotic model of epigenetic regulation. Biological Chemistry 379(4–5):553–557.']
  • ['Grant‐Downton R. T., Dickinson H. G. 2005. Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Annals of Botany 96(7):1143–1164.']
  • ['Grant‐Downton R. T., Dickinson H. G. 2006. Epigenetics and its implications for plant biology. 2. The ‘epigenetic epiphany’: epigenetics, evolution and beyond. Annals of Botany 97(1):11–27.']
  • ['Grewal S. I. S., Jia S. T. 2007. Heterochromatin revisited. Nature Reviews Genetics 8(1):35–46.']
  • ['Grimes G., Aufderheide K. 1991. Cellular aspects of pattern formation: the problem of assembly. Monographs in Developmental Biology 22:1–94.']
  • ['Groth A., Rocha W., Verreault A., Almouzni G. 2007. Chromatin challenges during DNA replication and repair. Cell 128(4):721–733.']
  • ['Gu Z., Rifkin S. A., White K. P., and Li W.‐H. 2004. Duplicate genes increase gene expression diversity within and between species. Nature Genetics 36(6):577–579.']
  • ['Hadchouel M., Farza H., Simon D., Tiollais P., Pourcel C. 1987. Maternal inhibition of hepatitis B surface antigen gene expression in transgenic mice correlates with de novo methylation. Nature 329(6138):454–456.']
  • ['Haig D. 2002. Genomic Imprinting and Kinship. New Brunswick (NJ): Rutgers University Press.']
  • ['Haig D. 2004. The (dual) origin of epigenetics. Cold Spring Harbor Symposia on Quantitative Biology 69:67–70.']
  • ['Hajkova P., Erhardt S., Lane N., Haaf T., El‐Maarri O., Reik W., Walter J., Surani M. A. 2002. Epigenetic reprogramming in mouse primordial germ cells. Mechanisms of Development 117(1–2):15–23.']
  • ['Henderson I. R., Jacobsen S. E. 2007. Epigenetic inheritance in plants. Nature 447(7143):418–424.']
  • ['Henikoff S., Ahmad K., Malik H. S. 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293(5532):1098–1102.']
  • ['Henikoff S., Smith M. M. 2007. Histone variants and epigenetics. Pages 249–264 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Himber C., Dunoyer P., Moissiard G., Ritzenthaler C., Voinnet O. 2003. Transitivity‐dependent and ‐independent cell‐to‐cell movement of RNA silencing. EMBO Journal 22(17):4523–4533.']
  • ['Hitchins M. P., Wong J. J. L., Suthers G., Suter C. M., Martin D. I. K., Hawkins N. J., Ward R. L. 2007. Brief report: inheritance of a cancer‐associated MLH1germ‐line epimutation. New England Journal of Medicine 356(7):697–705.']
  • ['Holliday R. 1984. The significance of DNA methylation in cellular aging. Pages 269–283 in Molecular Biology of Aging, edited by A. D. Woodhead et al. New York: Plenum Press.']
  • ['Holliday R. 1994. Epigenetics—an overview. Developmental Genetics 15:453–457.']
  • ['Holliday R. 2002. Epigenetics come of age in the twenty‐first century. Journal of Genetics 81(1):1–4.']
  • ['Holliday R. 2006. Epigenetics: a historical overview. Epigenetics 1(2):76–80.']
  • ['Huettel B., Kanno T., Daxinger L., Bucher E., van der Winden J., Matzke A. J., Matzke M. 2007. RNA‐directed DNA methylation mediated by DRD1 and Pol IVb: a versatile pathway for transcriptional gene silencing in plants. Biochimica et Biophysica Acta‐Gene Structure and Expression 1769(5–6):358–374.']
  • ['Issa J. P. 2000. CpG‐island methylation in aging and cancer. Current Topics in Microbiology and Immunology249:101–118.']
  • ['Jablonka E. 2004a. The evolution of the peculiarities of mammalian sex chromosomes: an epigenetic view. BioEssays 26(12):1327–1332.']
  • ['Jablonka E. 2004b. Epigenetic epidemiology. International Journal of Epidemiology 33(5):929–935.']
  • ['Jablonka E., Lachmann M., Lamb M. J. 1992. Evidence, mechanisms and models for the inheritance of acquired characters. Journal of Theoretical Biology 158(2):245–268.']
  • ['Jablonka E., Lamb M. J. 1989. The inheritance of acquired epigenetic variations. Journal of Theoretical Biology 139(1):69–83.']
  • ['Jablonka E., Lamb M. J. 1995. Epigenetic Inheritance and Evolution: The Lamarckian Dimension. Oxford (UK): Oxford University Press.']
  • ['Jablonka E., Lamb M. J. 2002. The changing concept of epigenetics. Annals of the New York Academy of Sciences 981:82–96.']
  • ['Jablonka E., Lamb M. J. 2005. Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. Cambridge (MA): MIT Press.']
  • ['Jablonka E., Lamb M. J. 2006a. Evolutionary epigenetics. Pages 252–264 in Evolutionary Genetics: Concepts and Case Studies, edited by C. W. Fox and J. B. Wolf. New York: Oxford University Press.']
  • ['Jablonka E., Lamb M. J. 2006b. The evolution of information in the major transitions. Journal of Theoretical Biology 239(2):236–246.']
  • ['Jablonka E., Lamb M. J. 2007a. Précis of Evolution in Four Dimensions. Behavioral and Brain Sciences30:353–365.']
  • ['Jablonka E., Lamb M. J. 2007b. Bridging the gap: the developmental aspects of evolution. Behavioral and Brain Sciences 30:378–392.']
  • ['Jablonka E., Lamb M. J. 2007c. The expanded evolutionary synthesis—a response to Godfrey‐Smith, Haig, and West‐Eberhard. Biology and Philosophy 22(3):453–472.']
  • ['Jablonka E., Lamb M. J. 2008. The epigenome in evolution: beyond the modern synthesis. VOGis Herald 12:242–254.']
  • ['Jablonka E., Oborny B., Molnar I., Kisdi E., Hofbauer J., Czaran T. 1995. The adaptive advantage of phenotypic memory in changing environments. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 350(1332):133–141.']
  • ['Jaenisch R., Gurdon J. 2007. Nuclear transplantation and the reprogramming of the genome. Pages 415–434 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Jirtle R. L., Skinner M. K. 2007. Environmental epigenomics and disease susceptibility. Nature Reviews Genetics 8(4):253–262.']
  • ['Jollos V. Experimentelle Protistenstudien 1. 1921. Untersuchungen über Variabilität und Vererbung bei Infusorien. Archiv für Protistenkunde 43:1–222.']
  • ["Jorgensen R. A. 2004. Restructuring the genome in response to adaptive challenge: McClintock's bold conjecture revisited. Cold Spring Harbor Symposia on Quantitative Biology 69:349–354."]
  • ['Karpen G. H., Hawley R. S. 2007. Epigenetic regulation of chromosome inheritance. Pages 265–289 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Kidwell M. G., Lisch D. 1997. Transposable elements as sources of variation in animals and plants. Proceedings of the National Academy of Sciences USA 94(15):7704–7711.']
  • ['Kim V. N. 2006. Small RNAs just got bigger: Piwi‐interacting RNAs (piRNAs) in mammalian testes. Genes and Development 20(15):1993–1997.']
  • ['Kölle S., Stojkovic M., Prelle K., Waters M., Wolf E., Sinowatz F. 2001. Growth hormone (GH)/GH receptor expression and GH‐mediated effects during early bovine embryogenesis. Biology of Reproduction 64:1826–1834.']
  • ['Kussell E., Leibler S. 2005. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309(5743):2075–2078.']
  • ['Lachmann M., Jablonka E. 1996. The inheritance of phenotypes: an adaptation to fluctuating environments. Journal of Theoretical Biology 181:1–9.']
  • ['Lamb M. J. 1994. Epigenetic inheritance and aging. Reviews in Clinical Gerontology 4(2):97–105.']
  • ['Lamm E., Jablonka E. 2008. The nurture of nature: hereditary plasticity in evolution. Philosophical Psychology 21(3):305–319.']
  • ['Laurent M., Charvin G., Guespin‐Michel J. 2005. Bistability and hysteresis in epigenetic regulation of the lactose operon. Since Delbruck, a long series of ignored models. Cellular and Molecular Biology 51(7):583–594.']
  • ['Levites E. V. 2000. Epigenetic variability as a source of biodiversity and a factor of evolution. Pages 73–75 in Biodiversity and Dynamics of Ecosystems in North Eurasia, Volume 1, Part 3. Novosibirsk (Russia): Institute of Cytology and Genetics SB RAS.']
  • ['Levy A. A., Feldman M. 2004. Genetic and epigenetic reprogramming of the wheat genome upon allopolyploidization. Biological Journal of the Linnean Society 82(4):607–613.']
  • ['Li E., Bird A. 2007. DNA methylation in mammals. Pages 341–356 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Lindegren C. C. 1949. The Yeast Cell, its Genetics and Cytology. Saint Louis (MO): Educational Publishers.']
  • ['Lindqvist C., Janczak A. M., Nätt D., Baranowska I., Lindqvist N., Wichman A., Lundeberg J., Lindberg J., Torjesen P. A., Jensen P. 2007. Transmission of stress‐induced learning impairment and associated brain gene expression from parents to offspring in chickens. PLoS ONE 2(4):e364.']
  • ['Little J. B. 2003. Genomic instability and bystander effects: a historical perspective. Oncogene 22(45):6978–6987.']
  • ['Logan C. A. 2007. Overheated rats, race, and the double gland: Paul Kammerer, endocrinology and the problem of somatic induction. Journal of the History of Biology 40(4):683–725.']
  • ['Long L., Lin X., Zhai J., Kou H., Yang W., Liu B. 2006. Heritable alteration in DNA methylation pattern occurred specifically at mobile elements in rice plants following hydrostatic pressurization. Biochemical and Biophysical Research Communications 340(2):369–376.']
  • ['Lyon M. F. 1998. X‐chromosome inactivation: a repeat hypothesis. Cytogenetics and Cell Genetics80:133–137.']
  • ['Malagnac F., Silar P. 2003. Non‐Mendelian determinants of morphology in fungi. Current Opinion in Microbiology 6(6):641–645.']
  • ['Malagnac F., Silar P. 2006. Regulation, cell differentiation and protein‐based inheritance. Cell Cycle 5(22):2584–2587.']
  • ['Mandrioli M. 2004. Epigenetic tinkering and evolution: is there any continuity in the role of cytosine methylation from invertebrates to vertebrates? Cellular and Molecular Life Sciences 61(19–20):2425–2427.']
  • ['Marcus E., editor. 2007. Issue on epigenetics. Cell 128(4):627–802.']
  • ['Martin C., Zhang Y. 2007. Mechanisms of epigenetic inheritance. Current Opinion in Cell Biology 19(3):266–272.']
  • ['Masel J., Bergman A. 2003. The evolution of the evolvability properties of the yeast prion [PSI+]. Evolution 57(7):1498–1512.']
  • ['Matzke M. A., Birchler J. A. 2005. RNAi‐mediated pathways in the nucleus. Nature Reviews Genetics 6(1):24–35.']
  • ['Matzke M. A., Scheid O. M. 2007. Epigenetic regulation in plants. Pages 167–189 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Maynard Smith J. 1990. Models of a dual inheritance system. Journal of Theoretical Biology143(1):41–53.']
  • ['Maynard Smith J., Szathmáry E. 1995. The Major Transitions in Evolution. Oxford (UK) and New York: W. H. Freeman Spektrum.']
  • ['Mayr E. 1982. The Growth of Biological Thought: Diversity, Evolution, and Inheritance. Cambridge (MA): Belknap Press.']
  • ['McClintock B. 1984. The significance of responses of the genome to challenge. Science 226(4676):792–801.']
  • ['Meister G., Tuschl T. 2004. Mechanisms of gene silencing by double‐stranded RNA. Nature 431(7006):343–349.']
  • ['Meyer E., Chalker D. L. 2007. Epigenetics of ciliates. Pages 127–150 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Misteli T. 2007. Beyond the sequence: cellular organization of genome function. Cell 128:787–800.']
  • ['Molinier J., Ries G., Zipfel C., Hohn B. 2006. Transgeneration memory of stress in plants. Nature 442:1046–1049.']
  • ['Morris C. A., Moazed D. 2007. Centromere assembly and propagation. Cell 128(4):647–650.']
  • ['Mortusewicz O., Schermelleh L., Walter J., Cardoso M. C., Leonhardt H. 2005. Recruitment of DNA methyltransferase I to DNA repair sites. Proceedings of the National Academy of Sciences USA 102(25):8905–8909.']
  • ['Nanney D. L. 1958. Epigenetic control systems. Proceedings of the National Academy of Sciences USA44(7):712–717.']
  • ['Nanney D. L. 1968. Cortical patterns in cellular morphogenesis: differences in cortical patterns in ciliates may be hereditary, but independent of genic differences. Science 160(3827):496–502.']
  • ['Nanney D. L. 1985. Heredity without genes: ciliate explorations of clonal heredity. Trends in Genetics 1:295–298.']
  • ['Naz R. K., Sellamuthu R. 2006. Receptors in spermatozoa: are they real? Journal of Andrology 27(5):627–636.']
  • ['Newbold R. R., Padilla‐Banks E., Jefferson W. N. 2006. Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 147:S11–S17.']
  • ['Novick A., Weiner M. 1957. Enzyme induction as an all‐or‐none phenomenon. Proceedings of the National Academy of Sciences USA 43(7):553–566.']
  • ['Nowacki M., Vijayan V., Zhou Y., Schotanus K., Doak T. G., Landweber L. F. 2008. RNA‐mediated epigenetic programming of a genome‐rearrangement pathway. Nature 451(7175):153–159.']
  • ['Pak J., Fire A. 2007. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315(5809):241–244.']
  • ['Pál C. 1998. Plasticity, memory and the adaptive landscape of the genotype. Proceedings of the Royal Society of London, Series B: Biological Sciences 265(1403):1319–1323.']
  • ['Palauqui J. C., Elmayan T., Pollien J. M., Vaucheret H. 1997. Systemic acquired silencing: transgene‐specific post‐transcriptional silencing is transmitted by grafting from silenced stocks to non‐silenced scions. EMBO Journal 16(15):4738–4745.']
  • ['Pantaleon M., Whiteside E. J., Harvey M. B., Barnard R. T., Waters M. J., Kaye P. L. 1997. Functional growth hormone (GH) receptors and GH are expressed by preimplantation mouse embryos: a role for GN in early embryogenesis? Proceedings of the National Academy of Sciences USA 94(10):5125–5130.']
  • ['Pavelka J., Koudelová J. 2001. Inheritance of a temperature‐modified phenotype of the short antennae(sa) mutation in a moth, Ephestia kuehniella (Lepidoptera: Pyralidae). Journal of Heredity 92(3):234–242.']
  • ['Pepper J. W., Sprouffske K., Maley C. C. 2007. Animal cell differentiation patterns suppress somatic evolution. PloS Computational Biology 3(12):e250.']
  • ['Petronis A. 2004. The origin of schizophrenia: genetic thesis, epigenetic antithesis, and resolving synthesis. Biological Psychiatry 55(10):965–970.']
  • ['Petronis A. 2006 Epigenetics and twins: three variations on the theme. Trends in Genetics 22(7):347–350.']
  • ['Pigliucci M. 2001. Phenotypic Plasticity: Beyond Nature and Nurture. Baltimore (MD): John Hopkins University Press.']
  • ['Pigliucci M., Murren C. J., Schlichting C. D. 2006. Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology 209(12):2362–2367.']
  • ['Pikaard C. S. 2000. The epigenetics of nucleolar dominance. Trends in Genetics 16(11):495–500.']
  • ['Pikaard C. S. 2003. Nucleolar dominance. Pages 399–402 in Nature Encyclopedia of the Human Genome, Volume 4, edited by D. N. Cooper. London (UK): Nature Publishing Group.']
  • ['Polo S. E., Roche D., Almouzni G. 2006. New histone incorporation marks sites of UV repair in human cells. Cell 127(3):481–493.']
  • ['Popova N. K. 2006. From genes to aggressive behavior: the role of serotonergic system. BioEssays 28(5):495–503.']
  • ['Prusiner S. B. 1998. Prions. Proceedings of the National Academy of Sciences USA 95(23):13363–13383.']
  • ['Rando O. J., Verstrepen K. J. 2007. Timescales of genetic and epigenetic inheritance. Cell 128(4):655–668.']
  • ['Rapp R. A., Wendel J. F. 2005. Epigenetics and plant evolution. New Phytologist 168(1):81–91.']
  • ['Rassoulzadegan M., Grandjean V., Gounon P., Vincent S., Gillot I., Cuzin F. 2006. RNA‐mediated non‐mendelian inheritance of an epigenetic change in the mouse. Nature 441(7092):469–474.']
  • ['Regev A., Lamb M. J., Jablonka E. 1998. The role of DNA methylation in invertebrates: developmental regulation or genome defense? Molecular Biology and Evolution 15(7):880–891.']
  • ['Richards E. J. 2006. Inherited epigenetic variation—revisiting soft inheritance. Nature Reviews Genetics 7(5):395–401.']
  • ['Richerson P. J., Boyd R. 2005. Not by Genes Alone: How Culture Transformed Human Evolution. Chicago (IL): University of Chicago Press.']
  • ['Ringrose L., Paro R. 2004. Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins. Annual Review of Genetics 38:413–443.']
  • ['Ringrose L., Paro R. 2007. Polycomb/trithorax response elements and epigenetic memory of cell identity. Development 134(2):223–232.']
  • ['Roberts B. T., Wickner R. B. 2003. Heritable activity: a prion that propagates by covalent autoactivation. Genes and Development 17(17):2083–2087.']
  • ['Rodin S. N., Parkhomchuk D. V., Riggs A. D. 2005. Epigenetic changes and repositioning determine the evolutionary fate of duplicated genes. Biochemistry (Moscow) 70(5):559–567.']
  • ['Ruden D. M., Xiao L., Garfinkel M. D., Lu X. 2005. Hsp90 and environmental impacts on epigenetic states: a model for the trans‐generational effects of diethylstibesterol on uterine development and cancer. Human Molecular Genetics 14(Review Issue 1):R149–R155.']
  • ['Ruvinsky A. O., Lobkov Y. I., Belyaev D. K. 1983a. Spontaneous and induced activation of genes affecting the phenotypic expression of glucose 6‐phosphate dehydrogenase in Daphnia pulex. 1. Intraclonal variations in the electrophoretic mobility of G6PD. Molecular & General Genetics 189(3):485–489.']
  • ['Ruvinsky A. O., Lobkov Y. I., Belyaev D. K. 1983b. Spontaneous and induced activation of genes affecting the phenotypic expression of glucose 6‐phosphate dehydrogenase in Daphnia pulex 2. Glucose‐induced changes in the electrophoretic mobility of G6PD. Molecular & General Genetics 189:490–494.']
  • ['Salmon A., Ainouche M. L., Wendel J. F. 2005. Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Molecular Ecology 14(4):1163–1175.']
  • ['Sandman K., Pereira S. L., Reeve J. N. 1998. Diversity of prokaryotic chromosomal proteins and the origin of the nucleosome. Cellular and Molecular Life Sciences 54(12):1350–1364.']
  • ['Sangster T. A., Lindquist S., Queitsch C. 2004. Under cover: causes, effects and implications of Hsp90‐mediated genetic capacitance. BioEssays 26(4):348–362.']
  • ['Sano H., Kamada I., Youssefian S., Katsumi M., Wabiko H. 1990. A single treatment of rice seedlings with 5‐azacytidine induces heritable dwarfism and undermethylation of genomic DNA. Molecular and General Genetics 220(3):441–447.']
  • ['Schacter D. L. 2001. Forgotten Ideas, Neglected Pioneers: Richard Semon and the Story of Memory.Philadelphia (PA): Psychology Press.']
  • ['Schermelleh L., Haemmer A., Spada F., Rösing N., Meilinger D., Rothbauer U., Cardoso M., Leonhardt H. 2007. Dynamics of Dnmt1 interaction with the replication machinery and its role in postreplicative maintenance of DNA methylation. Nucleic Acids Research 35(13):4301–4312.']
  • ['Schlichting C. D., Pigliucci M. 1998 Phenotypic Evolution: A Reaction Norm Perspective. Sunderland (MA): Sinauer.']
  • ['Schmalhausen I. I. 1949. Factors of Evolution: The Theory of Stabilizing Selection. Philadelphia (PA): Blackiston.']
  • ['Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., Cavalli G. 2007. Genome regulation by polycomb and trithorax proteins. Cell 128(4):735–745.']
  • ['Shapiro J. A. 1999. Genome system architecture and natural genetic engineering in evolution. Annals of the New York Academy of Sciences870:23–35.']
  • ['Shiao Y. H., Crawford E. B., Anderson L. M., Patel P., Ko K. 2005. Allele‐specific germ cell epimutation in the spacer promoter of the 45S ribosomal RNA gene after Cr(III) exposure. Toxicology and Applied Pharmacology 205(3):290–296.']
  • ['Shiu P. K. T., Raju N. B., Zickler D., Metzenberg R. L. 2001. Meiotic silencing by unpaired DNA. Cell 107(7):905–916.']
  • ['Shorter J., Lindquist S. 2005. Prions as adaptive conduits of memory and inheritance. Nature Reviews Genetics 6(6):435–450.']
  • ['Siegal M. L., Bergman A. 2006. Canalization. Pages 235–251 in Evolutionary Genetics, edited by C. W. Fox and J. B. Wolf. New York: Oxford University Press.']
  • ['Smits W. K., Kuipers O. P., Veening J. W. 2006. Phenotypic variation in bacteria: the role of feedback regulation. Nature Reviews Microbiology 4(4):259–271.']
  • ['Sokolov V. A. 2006. Imprinting in plants. Russian Journal of Genetics 42(9):1043–1052.']
  • ["Steele E. J., Lindley R. A., Blanden R. V. 1998. Lamarck's Signature: How Retrogenes are Changing Darwin's Natural Selection Paradigm. Reading (MA): Perseus Books."]
  • ['Talbert P. B., Bryson T., Henikoff S. 2004. Adaptive evolution of centromere proteins in plants and animals. Journal of Biology 3:18.']
  • ['True H. L., Lindquist S. L. 2000. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407(6803):477–483.']
  • ['True H. L., Berlin I., Lindquist S. L. 2004. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431(7005):184–187.']
  • ['Trut L. N., Plyusnina I. Z., Oskina I. N. 2004. An experiment on fox domestication and debatable issues of evolution of the dog. Russian Journal of Genetics 40(6):644–655.']
  • ['Tuite M. F., Cox B. S. 2006. The [PSI+] prion of yeast: a problem of inheritance. Methods 39(1):9–22.']
  • ['Turner J. M. A., Mahadevaiah S. K., Fernandez‐Capetillo O., Nussenzweig A., Xu X. L., Deng C.‐X., Burgoyne P. S. 2005. Silencing of unsynapsed meiotic chromosomes in the mouse. Nature Genetics 37(1):41–47.']
  • ['Uptain S. M., Lindquist S. 2002. Prions as protein‐based genetic elements. Annual Review of Microbiology 56:703–741.']
  • ['Van der Heijden G. W., Derijck A., Ramos L., Giele M., Van der Vlag J., de Boer P. 2006. Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Developmental Biology 298(2):458–469.']
  • ['Vanyushin B. F. 2006a. DNA methylation and epigenetics. Russian Journal of Genetics 42(9):985–997.']
  • ['Vanyushin B. F. 2006b. DNA methylation in plants. Current Topics in Microbiology and Immunology 301:67–122.']
  • ['Vanyushin B. F., Nemirovsky L. E., Klimenko V. V., Vasiliev V. K., Belozersky A. N. 1973. The 5‐methylcytosine in DNA of rats. Tissue and age specificity and the changes induced by hydrocortisone and other agents. Gerontologia 19(3):138–152.']
  • ['Vastenhouw N. L., Brunschwig K., Okihara K. L., Müller F., Tijsterman M., Plasterk R. H. A. 2006. Long‐term gene silencing by RNAi. Nature 442(7105):882.']
  • ['Veselá J., Rehák P., Mihalik J., Czikková S., Pokorný J., Koppel J. 2003. Expression of serotonin receptors in mouse oocytes and preimplantation embryos. Physiological Research 52(2):223–228.']
  • ["Vrana P. B., Fossella J. A., Matteson P., del Rio T., O'Neill M. J., Tilghman S. M. 2000. Genetic and epigenetic incompatibilities underlie hybrid dysgenesis in Peromyscus. Nature Genetics25(1):120–124."]
  • ['Waddington C. H. 1957. The Strategy of the Genes: A Discussion of Some Aspects of Theoretical Biology. London (UK): Allen & Unwin.']
  • ['Waddington C. H. 1968. The basic ideas of biology. Pages 1–32 in Towards a Theoretical Biology: Prolegomena, edited by C. H. Waddington. Edinburgh (UK): Edinburgh University Press.']
  • ['Waddington C. H. 1975. The Evolution of an Evolutionist. Edinburgh (UK): Edinburgh University Press.']
  • ['Waterland R. A., Travisano M., Tahiliani K. G. 2007. Diet‐induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB Journal 21(12):3380–3385.']
  • ['Waterland R. A., Travisano M., Tahiliani K. G., Rached M. T., Mirza S. 2008. Methyl donor supplementation prevents transgenerational amplification of obesity. International Journal of Obesity 32:1373–1379.']
  • ['Waters E. R., Schaal B. A. 1996. Heat shock induces a loss of rRNA‐encoding DNA repeats in Brassica nigra. Proceedings of the National Academy of Sciences USA 93(4):1449–1452.']
  • ["Weaver I. C. G., Cervoni N., Champagne F. A., D'Alessio A. C., Sharma S., Seckl J. R., Dymov S., Szyf M., Meaney M. J. 2004. Epigenetic programming by maternal behavior. Nature Neuroscience 7(8):847–854."]
  • ['West‐Eberhard M. J. 2003. Developmental Plasticity and Evolution. New York: Oxford University Press.']
  • ['Wickner R. B. 1994. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264(5158):566–569.']
  • ['Wickner R. B., Edskes H. K., Ross E. D., Pierce M. M., Baxa U., Brachmann A., Shewmaker F. 2004. Prion genetics: new rules for a new kind of gene. Annual Review of Genetics 38:681–707.']
  • ['Wolf J. B., Hager R. 2006. A maternal–offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biology 4(12):2238–2243.']
  • ['Wu C.‐T., Morris J. R. 2001. Genes, genetics, and epigenetics: a correspondence. Science 293(5532):1103–1105.']
  • ['Wu T. C. J., Wang L., Wan Y.‐J. Y. 1992. Expression of estrogen receptor gene in mouse oocyte and during embryogenesis. Molecular Reproduction and Development33(4):407–412.']
  • ['Yi H., Riddle N. C., Stokes T. L., Woo H.‐R., Richards E. J. 2004. Induced and natural epigenetic variation. Cold Spring Harbor Symposia on Quantitative Biology 69:155–160.']
  • ['Zacharioudakis I., Gligoris T., Tzamarias D. 2007. A yeast catabolic enzyme controls transcriptional memory. Current Biology 17(23):2041–2046.']
  • ['Zaratiegui M., Irvine D. V., Martienssen R. A. 2007. Non coding RNAs and gene silencing. Cell 128(4):763–776.']
  • ['Zhivotovsky L. A. 2002. A model of the early evolution of soma‐to‐germline feedback. Journal of Theoretical Biology 216(1):51–57.']
  • ['Zoghbi H. Y., Beaudet A. L. 2007. Epigenetics and human disease. Pages 435–456 in Epigenetics, edited by C. D. Allis et al. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.']
  • ['Zordan R. E., Galgoczy D. J., Johnson A. D. 2006. Epigenetic properties of white‐opaque switching in Candida albicans are based on a self‐sustaining transcriptional feedback loop. Proceedings of the National Academy of Sciences USA 103(34):12807–12812.']
  • ['Zuckerkandl E., Cavalli G. 2007. Combinatorial epigenetics, “junk DNA,” and the evolution of complex organisms. Gene 390(1–2):232–242.']
  • ['Zufall R. A., Robinson T., Katz L. A. 2005. Evolution of developmentally regulated genome rearrangements in eukaryotes. Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution 304B(5):448–455.']

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