Biology & Philosophy

, Volume 29, Issue 1, pp 55–69 | Cite as

From DNA- to NA-centrism and the conditions for gene-centrism revisited

  • Alexis De TiègeEmail author
  • Koen Tanghe
  • Johan Braeckman
  • Yves Van de Peer


First the ‘Weismann barrier’ and later on Francis Crick’s ‘central dogma’ of molecular biology nourished the gene-centric paradigm of life, i.e., the conception of the gene/genome as a ‘central source’ from which hereditary specificity unidirectionally flows or radiates into cellular biochemistry and development. Today, due to advances in molecular genetics and epigenetics, such as the discovery of complex post-genomic and epigenetic processes in which genes are causally integrated, many theorists argue that a gene-centric conception of the organism has become problematic. Here, we first explore the causal implications of the following two central dogma-related issues: (1) widespread reverse transcription—arguing for an extension from ‘DNA-genome’ to RNA-encompassing ‘NA-genome’ and, thus, from traditional DNA-centrism to a broader ‘NA-centrism’; and (2) the absence of a mechanism of reverse translation—arguing for the ‘structural primacy’ of NA-sequence over protein in cellular biochemistry. Secondly, we explore whether this latter conclusion can be extended to a ‘functional primacy’ of NA-sequence over protein in cellular biochemistry, which would imply a limited kind of ‘gene/NA-centrism’ confined to the subcellular level of NA/protein-based biochemistry. Finally, we explore the conditions—and their (non)fulfilment—for a more generalised form of gene-centrism extendable to higher levels of biological organisation. We conclude that the higher we go in the biological hierarchy, the more dubious gene-centric claims become.


The Weismann barrier The central dogma Reverse transcription The absence of reverse translation From DNA- to NA-centrism The conditions for gene-centrism Gene-de-centrism 



We are grateful to an anonymous reviewer for extensive comments on an earlier version of the paper, to Kim Sterelny for additional comments and suggestions, and to Linda Van Speybroeck for both constructive criticism and support during previous stages of the paper. Preparation of the manuscript was made possible by the Special Research Fund (BOF), Ghent University (Project Number: B/11196/02) and by the Fund for Scientific Research Flanders (FWO), Belgium (Project Number: G001013N).


  1. Baranov PV, Gurvich OL, Hammer AW, Gesteland RF, Atkins JF (2003) RECODE 2003. Nucleic Acids Res 31:87–89CrossRefGoogle Scholar
  2. Brennicke A, Marchfelder A, Binder S (1999) RNA editing. FEMS Microbiol Rev 23:297–316CrossRefGoogle Scholar
  3. Brosius J (1999) RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene 238:115–134CrossRefGoogle Scholar
  4. Brosius J (2003) The contribution of RNAs and retroposition to evolutionary novelties. Genetica 118:99–116CrossRefGoogle Scholar
  5. Cairns-Smith AG (1985) Seven clues to the origin of life. Cambridge University Press, CantoGoogle Scholar
  6. Callebaut W, Rasskin-Gutman D (eds) (2005) Modularity: understanding the development and evolution of natural complex systems. MIT Press, CambridgeGoogle Scholar
  7. Callebaut W, Müller GB, Newman SA (2007) The organismic systems approach: EvoDevo and the streamlining of the naturalistic agenda. In: Sansom R, Brandon R (eds) Integrating evolution and development: from theory to practice. MIT Press, Cambridge, pp 25–92Google Scholar
  8. Crick F (1958) On protein synthesis. Sympos Soc Exp Biol 12:138–163Google Scholar
  9. Crick F (1970) Central dogma of molecular biology. Nature 227:561–563CrossRefGoogle Scholar
  10. Dawkins R (1982) The extended phenotype. Oxford University Press, OxfordGoogle Scholar
  11. Dawkins R (2004) Extended phenotype: but not too extended. A reply to Laland, Turner and Jablonka. Biol Philos 19:377–396CrossRefGoogle Scholar
  12. De Backer P, De Waele D, Van Speybroeck L (2010) Ins and outs of systems biology vis-à-vis molecular biology: continuation or clear cut? Acta Biotheor 58:15–49CrossRefGoogle Scholar
  13. Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Dev Biol 173:357–372CrossRefGoogle Scholar
  14. Godfrey-Smith P (2007) Is it a revolution? Biol Philos 22:429–437CrossRefGoogle Scholar
  15. Goodman MF (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Ann Rev Biochem 71:17–50CrossRefGoogle Scholar
  16. Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Cambridge, MAGoogle Scholar
  17. Griesemer J (2000) The units of evolutionary transition. Selection 1:67–80CrossRefGoogle Scholar
  18. Griesemer J (2002) What is “epi” about epigenetics? Ann NY Acad Sci 981:97–110CrossRefGoogle Scholar
  19. Griesemer J (2005) The informational gene and the substantial body: On the generalization of evolutionary theory by abstraction. In: Jones MR, Cartwright N (eds) Idealization XII: correcting the model. Idealization and abstraction in the sciences (Poznan studies in the philosophy of sciences and the humanities, vol 86. Rodopi, Amsterdam, pp 59–115Google Scholar
  20. Haig D (2004) The (dual) origin of epigenetics. Cold Spring Harbor Symp Quant Biol 69:67–70CrossRefGoogle Scholar
  21. Haig D (2007) Weismann rules! OK? Epigenetics and the Lamarckian temptation. Biol Philos 22:415–428CrossRefGoogle Scholar
  22. Halfmann R, Jarosz DF, Jones SK, Chang A, Lancaster AK, Lindquist S (2012) Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482:363–368CrossRefGoogle Scholar
  23. Hall BK (2003) Unlocking the black box between genotype and phenotype: cell condensations as morphogenetic (modular) units. Biol Philos 18:219–247CrossRefGoogle Scholar
  24. Holliday R (1990) Mechanisms for the control of gene activity during development. Biol Rev 65:431–471CrossRefGoogle Scholar
  25. International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921CrossRefGoogle Scholar
  26. Jablonka E, Lamb M (1995) Epigenetic inheritance and evolution: the Lamarckian dimension. Oxford University Press, OxfordGoogle Scholar
  27. Jablonka E, Lamb M (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, Cambridge, MAGoogle Scholar
  28. Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84:131–176CrossRefGoogle Scholar
  29. Keller EF (2000) The century of the gene. Harvard University Press, Cambridge, MAGoogle Scholar
  30. Knoop V (2011) When you can’t trust the DNA: RNA editing changes transcript sequences. Cell Mol Life Sci 68:567–586CrossRefGoogle Scholar
  31. Koonin EV (2012) Does the central dogma still stand? Biol Direct 7:27CrossRefGoogle Scholar
  32. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220CrossRefGoogle Scholar
  33. Maas S, Rich A (2000) Changing genetic information through RNA editing. BioEssays 22:790–802CrossRefGoogle Scholar
  34. Maydanovych O, Beal PA (2006) Breaking the central dogma by RNA editing. Chem Rev 106(8):3397–3411CrossRefGoogle Scholar
  35. Maynard Smith J (1993) The theory of evolution. Cambridge University Press, CantoGoogle Scholar
  36. Maynard Smith J (2000) The concept of information in biology. Philos Sci 67:177–194CrossRefGoogle Scholar
  37. Medina M (2005) Genomes, phylogeny, and evolutionary systems biology. PNAS 102:6630–6635CrossRefGoogle Scholar
  38. Moss L (2003) What genes can’t do. MIT Press, Cambridge, MAGoogle Scholar
  39. Neumann-Held EM, Rehmann-Sutter C (eds) (2006) Genes in development: re-reading the molecular paradigm. Duke University Press, DurhamGoogle Scholar
  40. Noble D (2008) Genes and causation. Philos Trans A Math Phys Eng Sci 366:3001–3015CrossRefGoogle Scholar
  41. Noble D (2011) Neo-Darwinism, the modern synthesis, and selfish genes: are they of use in physiology? J Physiol 589:1007–1015CrossRefGoogle Scholar
  42. Odling-Smee J, Laland KN (2011) Ecological inheritance and cultural inheritance: what are they and how do they differ? Biol Theory 6:220–230CrossRefGoogle Scholar
  43. Oyama S (1985) The ontogeny of information: developmental systems and evolution. Cambridge University Press, CambridgeGoogle Scholar
  44. Oyama S, Griffiths PE, Gray RD (eds) (2001) Cycles of contingency: developmental systems and evolution. MIT Press, Cambridge, MAGoogle Scholar
  45. Rando OJ, Verstrepen KJ (2007) Timescales of genetic and epigenetic inheritance. Cell 128:655–668CrossRefGoogle Scholar
  46. Richards EJ (2006) Inherited epigenetic variation: revisiting soft inheritance. Nat Rev Genet 7:395–401CrossRefGoogle Scholar
  47. Richards CL, Bossdorf O, Pigliucci M (2010) What role does heritable epigenetic variation play in phenotypic evolution? Bioscience 60:232–237CrossRefGoogle Scholar
  48. Sarkar S (2000) Information in genetics and developmental biology: comments on Maynard Smith. Philos Sci 67:208–213CrossRefGoogle Scholar
  49. Sarkar S (2005) Molecular models of life: philosophical papers on molecular biology. MIT Press, Cambridge, MAGoogle Scholar
  50. Shapiro JA (2009) Revisiting the central dogma in the 21st century. Natural genetic engineering and natural genome editing. Ann N Y Acad Sci 1178:6–28CrossRefGoogle Scholar
  51. Shapiro JA (2011) Evolution: a view from the 21st century. FT Press Science, Upper Saddle River, NJGoogle Scholar
  52. Sharp PA (1994) Split genes and RNA splicing. Cell 77:805–815CrossRefGoogle Scholar
  53. Stotz K (2006a) Molecular epigenesis: distributed specificity as a break in the central dogma. Hist Philos Life Sci 28:527–544Google Scholar
  54. Stotz K (2006b) With ‘genes’ like that, who needs an environment? Postgenomics’ argument for the ‘ontogeny of information’. Philos Sci 73:905–917CrossRefGoogle Scholar
  55. Temin HM (1985) Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol Biol Evol 2:455–468Google Scholar
  56. Temin HM, Mizutani S (1970) RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226:1211–1213CrossRefGoogle Scholar
  57. Thieffry D, Sarkar S (1998) Forty years under the central dogma. TiBS 23:312–316Google Scholar
  58. True HL, Berlin I, Lindquist S (2004) Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431:184–187CrossRefGoogle Scholar
  59. Weismann A (1889) Essays upon heredity and kindred biological problems, vol 1. Clarendon Press, OxfordGoogle Scholar
  60. Weismann A (1893a) The germ-plasm: a theory of heredity (trans: Parker WN, Rönnfeldt H). Charles Scribner’s Sons, New YorkGoogle Scholar
  61. Weismann A (1893b) The all-sufficiency of natural selection: a reply to Herbert Spencer. Contemp Rev 64:309–338Google Scholar
  62. Weismann A (1904) The evolution theory (trans: Thomson JA, Thomson M). Edward Arnold, LondonGoogle Scholar
  63. Wilkins A (2011) Epigenetic inheritance: where does the field stand today? What do we still need to know? In: Gissis SB, Jablonka E (eds) Transformations of Lamarckism: from subtle fluids to molecular biology. MIT Press, Cambridge, MA, pp 389–393CrossRefGoogle Scholar
  64. Winther RG (2001) August Weismann on germ-plasm variation. J Hist Biol 34:517–555CrossRefGoogle Scholar
  65. Woodward J (2010) Causation in biology: stability, specificity, and the choice of levels of explanation. Biol Philos 25:287–318CrossRefGoogle Scholar
  66. Wu T, Wang J, Changning L et al (2006) NPInter: the noncoding RNAs and protein related biomacromolecules interaction database. Nucleic Acids Res 34:D150–D152CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Alexis De Tiège
    • 1
    Email author
  • Koen Tanghe
    • 1
  • Johan Braeckman
    • 1
  • Yves Van de Peer
    • 2
    • 3
  1. 1.Department of Philosophy and Moral ScienceGhent UniversityGhentBelgium
  2. 2.Department of Plant Systems BiologyVIBGhentBelgium
  3. 3.Department of Plant Biotechnology and BioinformaticsGhent UniversityGhentBelgium

Personalised recommendations