Abstract
The French school of theoretical biology has been mainly initiated in Poitiers during the sixties by scientists like J. Besson, G. Bouligand, P. Gavaudan, M. P. Schützenberger and R. Thom, launching many new research domains on the fractal dimension, the combinatorial properties of the genetic code and related amino-acids as well as on the genetic regulation of the biological processes. Presently, the biological science knows that RNA molecules are often involved in the regulation of complex genetic networks as effectors, e.g., activators (small RNAs as transcription factors), inhibitors (micro-RNAs) or hybrids (circular RNAs). Examples of such networks will be given showing that (1) there exist RNA “relics” that have played an important role during evolution and have survived in many genomes, whose probability distribution of their sub-sequences is quantified by the Shannon entropy, and (2) the robustness of the dynamics of the networks they regulate can be characterized by the Kolmogorov–Sinaï dynamic entropy and attractor entropy.
Similar content being viewed by others
References
Almeida L, Demongeot J (2012) Predictive power of “a minima” models in biology. Acta Biotheor 60:3–19
Besson J (1977) Topology of circular DNA. Annales de Génétique 20:145–152
Besson J (1994) Passion des formes: dynamique qualitative sémiophysique et intelligibilité. A René Thom. Porte M (ed). ENS Editions, Fontenay-Saint Cloud, p 803
Besson J (2001) La quête de M.P. Schützenberger en biologie et médecine, pp 1–6. http://igm.univ-mlv.fr/~berstel/Mps/Souvenirs/Contributions/JacquesBesson/MPSParBesson.pdf
Besson J, Gavaudan P (1967a) On the logarithmic organization of the genetic code. C R Acad Sci D 264:1311–1314
Besson J, Gavaudan P (1967b) Antinomias in the axiomatization of genetic coding by triplets. C R Acad Sci D 264:2405–2408
Besson J, Gavaudan P, Schützenberger MP (1969) Sur l’existence d’une certaine corrélation entre le poids moléculaire des acides aminés et le nombre de triplets intervenant dans leurs codages. C R Acad Sci Paris 268:1342–1344
Binder S, Schuster W, Grienenberger JM, Weil JH, Brennicke A (1990) Genes for Gly-, His-, Lys-, Phe-, Ser- and Tyr-tRNA are encoded in Oenothera mitochondrial DNA. Curr Genet 17:353–358
Brent MR, Guigó R (2004) Recent advances in gene structure prediction. Curr Opin Struct Biol 14:264–272
Brooks DJ, Fresco JR, Arthur M, Lesk AM, Singh M (2002) Evolution of amino acid frequencies in proteins over deep time: inferred order of introduction of amino acids into the genetic code. Mol Biol Evol 19:1645–1655
Choi H, Gabriel K, Schneider J, Otten S, McClain WH (2003) Recognition of acceptor-stem structure of tRNAAsp by Escherichia coli aspartyl-tRNA synthetase. RNA 9:386–393
Chomsky N, Schützenberger MP (1963) The algebraic theory of context-free languages. In: Braffort P, Hirschberg D (eds) Computer programming and formal systems. North Holland, Amsterdam, pp 118–161
Crick FHC, Barnett L, Brenner S, Watts-Tobin RJ (1961) General nature of the genetic code for proteins. Nature 192:1227–1232
Crick FHC, Brenner S, Klug A, Pieczenik G (1976) A speculation on the origin of protein synthesis. Orig Life 7:389–397
Cuénot L (1938) Présentation d’un arbre généalogique du Règne animal. Bull Soc Sci Nancy 3:110–115
Cullmann G, Labouygues JM (1983) Noise immunity of the genetic code. Biosystems 16:9–29
Demetrius L (1983) Statistical mechanics and population biology. J Stat Phys 30:709–753
Demetrius L (1997) Directionality principles in thermodynamics and evolution. Proc Natl Acad Sci USA 94:3491–3498
Demetrius L, Ziehe M (2007) Darwinian fitness. Theor Popul Biol 72:323–345
Demetrius L, Gundlach M, Ochs G (2004) Complexity and demographic stability in population models. Theor Popul Biol 65:211–225
Demongeot J (1975) Au sujet de quelques modèles stochastiques appliqués à la biologie. Doctoral dissertation, Université J. Fourier, Grenoble. http://tel.archives-ouvertes.fr/tel-00286222
Demongeot J (1978) Sur la possibilité de considérer le code génétique comme un code à enchaînement. Revue de Biomathématiques 62:61–66
Demongeot J, Besson J (1983) Code génétique et codes à enchaînement I. C R Acad Sci Ser III 296:807–810
Demongeot J, Besson J (1996) Genetic code and cyclic codes II. C R Acad Sci Ser III 319:520–528
Demongeot J, Demetrius L (2015) Complexity and stability in biological systems. Int J Bifurc Chaos 25:1540013
Demongeot J, Moreira A (2007) A circular RNA at the origin of life. J Theor Biol 249:314–324
Demongeot J, Weil G (2008) Complexification de la mémoire génétique. In: Bourgine P, Chavalarias D, Cohen-Boulakia C (eds) Déterminismes et complexités: du physique à l’éthique. Editions de la Découverte, Paris, pp 81–112
Demongeot J, Aracena J, Thuderoz F, Baum TP, Cohen O (2003) Genetic regulation networks: circuits, regulons and attractors. C R Biol 326:171–188
Demongeot J, Drouet E, Moreira A, Rechoum Y, Sené S (2009a) MicroRNAs: viral genome and robustness of the genes expression in host. Philos Trans R Soc A 367:4941–4965
Demongeot J, Glade N, Moreira A, Vial L (2009b) RNA relics and origin of life. Int J Mol Sci 10:3420–3441
Demongeot J, Cohen O, Henrion-Caude A (2013) MicroRNAs and robustness in biological regulatory networks. A generic approach with applications at different levels: physiologic, metabolic, and genetic. Springer Ser Biophys 16:63–114
Demongeot J, Ben Amor H, Hazgui H, Waku J (2014) Robustness in neural and genetic regulatory networks: mathematical approach and biological applications. Acta Biotheor 62:243–284
Demongeot J, Hazgui H, Henrion Caude A (2015) Genetic regulatory networks: focus on attractors of their dynamics. In: Tran QN, Arabnia HR (eds) Computational biology, bioinformatics & systems biology. Elsevier, New York, pp 135–165
Di Giulio M (2009) A comparison among the models proposed to explain the origin of the tRNA molecule: a synthesis. J Mol Evol 69:1–9
Franch T, Petersen M, Gerhart E, Wagner H, Jacobsen JP, Gerdes K (1999) Antisense RNA regulation in prokaryotes: rapid RNA/RNA interaction facilitated by a general U-turn loop structure. J Mol Biol 294:1115–1125
Gamow G, Ycas M (1955) Statistical correlation of protein and ribonucleic acid composition. Proc Natl Acad Sci USA 41:1011–1019
Gamow G, Rich A, Ycas M (1956) The problem of information transfer from the nucleic acids to proteins. Adv Biol Med Phys 4:23–68
Gavaudan P (1971) Internal logic of genetic coding. C R Acad Sci D 272:1672–1675
Gavaudan P (1984) Atomes et molécules biogéniques dans l’univers des nombres. Edition Pierre Gavaudan, Sorgues
Gavaudan P, Besson J (1967) Remarks on the methods of translation of the genetic code in polypeptide chains. C R Acad Sci D 264:1919–1922
Gavaudan P, Besson J (1969a) Statistical and segmental analysis of the composition of polypeptide chains. C R Acad Sci D 268:173–175
Gavaudan P, Besson J (1969b) On the causes of the mode of distribution of redundancies in the genetic code. C R Acad Sci D 268:2130–2132
Gavaudan P, Gavaudan N (1938) Mécanisme d’action de la colchicine sur la caryocinèse des végétaux. C R Soc Biol 128:714
Gavaudan P, Schützenberger MP, Poussel H (1947) L’excitation des chimiorécepteurs de la langue par des substances du groupe des narcotiques indifférentes et la règle thermodynamique de la narcose. C R Acad Sci 224:1525–1527
Gavaudan P, Poussel H, Schützenberger MP (1948) Le mécanisme physico-chimique de l’excitation sapide et la notion d’excitant indifférent. C R Acad Sci Paris 226:751–752
Griffiths-Jones S, Marshall M, Khanna A, Eddy SR, Bateman A (2005) Rfam: annotating non-coding RNAs in complete genomes. Nucl Acids Res 33:121–124
Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388
Hobish MK, Wickramasinghe NSMD, Ponnamperuma C (1995) Direct interaction between amino-acids and nucleotides as a possible physico-chemical basis for the origin of the genetic code. Adv Space Res 15:365–375
Holley RW, Everett GA, Madison JT, Zamir A (1965a) Nucleotide sequences in the yeast alanine transfer ribonucleic acid. J Biol Chem 240:2122–2128
Holley RW, Apgar J, Everett GA, Madison JT, Marquisee M, Merrill SH, Penswick JR, Zamir A (1965b) Structure of a ribonucleic acid. Science 147:1462–1465
Huck J (2011) Emergence in complex systems based on synthetic replicators. Doctoral dissertation, University of St Andrews
Katchalsky A (1973) Prebiotic synthesis of biopolymers on inorganic templates. Naturwissenschaften 60:215–220
Klingler T, Brutlag DL (1993) Detection of correlations in tRNA with structural implications. Intell Syst Mol Biol 1:225–233
Lejeune J, Gautier M, Turpin R (1959) Etude des chromosomes somatiques de neuf enfants mongoliens. C R Acad Sci 248:1721–1722
Lewin B (1960) Alternatives for splicing: recognizing the ends of lntrons. Cell 22:324–326
Lewin B (2008) Genes IX. Jones & Bartlett, Boston
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495:333–338
Meyer SC, Nelson PA (2011) Can the origin of the genetic code be explained by direct RNA templating? Bio-complexity 2011:1–10
Michaud M, Cognat V, Duchêne AM, Maréchal-Drouard L (2011) A global picture of tRNA genes in plant genomes. Plant J 66:80–93
Miller SL (1953) A production of amino acids under possible primitive Earth conditions. Science 117:528–529
Nirenberg MW, Matthaei HJ (1961) The dependence of cell- free protein synthesis in E. coli upon naturally occurring or synthetic polyribonucleotides. Proc Natl Acad Sci USA 47:1588–1602
Nishimura S, Jones DS, Khorana HG (1965) The in vitro synthesis of a co-polypeptide containing two amino acids in alternating sequence dependent upon a DNA-like polymer containing two nucleotides in alternating sequence. J Mol Biol 13:302–324
Orgel LE, Crick FHC (1993) Anticipating an RNA world. Some past speculations on the origin of life: where are they today? FASEB J 7:238–239
Piccinelli P, Samuelsson T (2007) Evolution of the iron-responsive element. RNA 13:952–966
Prado-Prado F, García-Mera X, Abeijón P, Alonso N, Caamaño O, Yáñez M, Gárate T, Mezo M, González-Warleta M, Muiño L, Ubeira FM, González-Díaz H (2011) Using entropy of drug and protein graphs to predict FDA drug-target network: theoretic-experimental study of MAO inhibitors and hemoglobin peptides from Fasciola hepatica. Eur J Med Chem 44:1074–1094
Riera-Fernández P, Munteanu CR, Escobar M, Prado-Prado F, Martín-Romalde R, Pereira D, Villalba K, Duardo-Sánchez A, González-Díaz H (2012) New Markov–Shannon entropy models to assess connectivity quality in complex networks: from molecular to cellular pathway, parasite-host, neural, industry & legal-social networks. J Theor Biol 293:174–188
Rychlik W, Spencer WJ, Rhoads RE (1990) Optimization of the annealing temperature for DNA amplification in vitro. Nucl Acids Res 18:6409–6412
Sadownik J (2009) Evolving complex systems from simple molecules. Doctoral dissertation, University of St Andrews
Sangokoya C, Doss JF, Chi JT (2013) Iron-responsive miR-485-3p regulates cellular iron homeostasis by targeting ferroportin. PLoS Genet 9:e1003408
Schützenberger MP, Turpin R (1949) L’étude des dermatoglyphes. Semaine des Hôpitaux de Paris 25:2553–2562
Seligmann H, Raoult D (2016) Unifying view of stem–loop hairpin RNA as origin of current and ancient parasitic and non-parasitic RNAs, including in giant viruses. Curr Opin Microbiol 31:1–8
Shigi N, Suzuki T, Tamakoshi M, Oshima T, Watanabe K (2002) Conserved bases in the TψC-loop of tRNA are determinants for thermophile-specific 2-thiouridylation at position 54*. J Biol Chem 277:39128–39135
Sonneborn TM (1965) Degeneracy of the genetic code: extent, nature and genetic implications. In: Bryson V, Vogel H (eds) Evolving genes and proteins. Academic Press, New York, pp 377–397
Sprinzl M, Horn C, Brown M, Ioudovitch A, Steinberg S (1998) Compilation of tRNA sequences and sequences of tRNA genes. Nucl Acids Res 26:148–153
Subirana JA, Messeguer X (2010) The most frequent short sequences in non-coding DNA. Nucl Acids Res 38:1172–1181
Tanaka T, Kikuchi Y (2001) Origin of the cloverleaf shape of transfer RNA—the double-hairpin model: Implication for the role of tRNA intro and the long extra loop. Viva Origino 29:119–142
Thom R (1988) Esquisse d’une sémiophysique. Théorie des catastrophes et physique aristotélicienne. Interéditions, Paris
Turpin R, Lejeune J (1954) Analogie entre le type dermatoglyphe des singes inférieurs et celui des enfants atteints de mongolisme. C R Acad Sci 238:395–397
Waddington CH (1940) Organisers and genes. Cambridge University Press, Cambridge
Waddington CH (1952) The epigenetics of birds. Cambridge University Press, Cambridge
Watson JD, Crick FHC (1953) Genetical implications of the structure of deoxyribonucleic acid. Nature 171:964–967
Yarus M, Widmann JJ, Knight R (2009) RNA-amino acid binding: a stereochemical era for the genetic code. J Mol Evol 69:406–429
Acknowledgments
We thank the ANR Project REGENR for financially aiding our research.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Demongeot, J., Hazgui, H. The Poitiers School of Mathematical and Theoretical Biology: Besson–Gavaudan–Schützenberger’s Conjectures on Genetic Code and RNA Structures. Acta Biotheor 64, 403–426 (2016). https://doi.org/10.1007/s10441-016-9287-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10441-016-9287-y