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Searching for Possible Ancestors of RNA: The Self-Assembly Hypothesis for the Origin of Proto-RNA

  • Brian J. Cafferty
  • David M. Fialho
  • Nicholas V. Hud
Chapter
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 35)

Abstract

There are currently two main schools of thought regarding the origins of RNA. In one school, RNA is considered to be a product of nonenzymatic, prebiotic reactions. In the other, RNA is considered to be a product of chemical and/or biological evolution. The numerous challenges to demonstrating a plausible prebiotic synthesis of RNA support the hypothesis that life started with an ancestral RNA-like polymer, or proto-RNA. If RNA is an “invention” of early life, then it is logical to assume that identifying the chemical structure of proto-RNA, and intermediate pre-RNAs, would require exploration of a seemingly insurmountable number of possible proto-RNA building blocks and prebiotic reactions. Here we report progress toward finding a proto-RNA that is the product of molecular self-assembly. Results obtained thus far demonstrate that seemingly minor changes to the structure of the extant building blocks of RNA (e.g., the substitution of uracil by barbituric acid) alleviate several long-standing problems associated with finding a prebiotic synthesis for RNA.

Notes

Acknowledgments

We thank Profs. Frank A. L. Anet, Ram Krishnamurthy, Gary B. Schuster, and Loren Dean Williams, who have been valuable collaborators and consultants on much of the work described in this chapter from our laboratory. This work was supported by the NSF and the NASA Astrobiology Program, under the NSF Center for Chemical Evolution (CHE-1504217) and the NASA Exobiology Program NNX13AI02G.

References

  1. Abo-Riziq A, Grace L, Nir E, Kabelac M, Hobza P, de Vries MS (2005) Photochemical selectivity in guanine-cytosine base-pair structures. Proc Natl Acad Sci U S A 102:20–23PubMedCrossRefGoogle Scholar
  2. Arnott S, Bond PJ (1973) Triple-stranded polynucleotide helix containing only purine bases. Science 181:68PubMedCrossRefGoogle Scholar
  3. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Ångstrom resolution. Science 289:905–920PubMedCrossRefGoogle Scholar
  4. Barks HL, Buckley R, Grieves GA, Di Mauro E, Hud NV, Orlando TM (2010) Guanine, adenine, and hypoxanthine production in UV-irradiated formamide solutions: relaxation of the requirements for prebiotic purine nucleobase formation. Chembiochem 11:1240–1243PubMedCrossRefGoogle Scholar
  5. Battersby TR, Albalos M, Friesenhahn MJ (2007) An unusual mode of DNA duplex association: Watson-Crick interaction of all-purine deoxyribonucleic acids. Chem Biol 14:525–531PubMedCrossRefPubMedCentralGoogle Scholar
  6. Benner SA (2004) Understanding nucleic acids using synthetic chemistry. Acc Chem Res 37:784–797PubMedCrossRefPubMedCentralGoogle Scholar
  7. Benner SA, Ricardo A, Carrigan MA (2004) Is there a common chemical model for life in the universe? Curr Opin Chem Biol 8:672–689PubMedCrossRefPubMedCentralGoogle Scholar
  8. Benner SA, Kim H-J, Carrigan MA (2012) Asphalt, water, and the prebiotic synthesis of ribose, ribonucleosides, and RNA. Acc Chem Res 45:2025–2034PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bernhardt HS (2012) The RNA world hypothesis: the worst theory of the early evolution of life (except for all the others)(a). Biol Direct 7:23–23PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bogert MT (1910) The instability of alloxan. J Am Chem Soc 32:809–810CrossRefGoogle Scholar
  11. Bohanon TM, Denzinger S, Fink R, Paulus W, Ringsdorf H, Weck M (1995) Barbituric-acid 2,4,6-triaminopyrimidine aggregates in water and their competitive interaction with a monolayer of barbituric-acid lipids at the gas-water interface. Angew Chem Int Ed Engl 34:58–60CrossRefGoogle Scholar
  12. Bolli M, Micura R, Eschenmoser A (1997) Pyranosyl-RNA: chiroselective self-assembly of base sequences by ligative oligomerization of tetra nucleotide-2′,3′-cyclophosphates (with a commentary concerning the origin of biomolecular homochirality). Chem Biol 4:309–320PubMedCrossRefPubMedCentralGoogle Scholar
  13. Borquez E, Cleaves HJ, Lazcano A, Miller SL (2005) An investigation of prebiotic purine synthesis from the hydrolysis of HCN polymers. Orig Life Evol Biosph 35:79–90PubMedCrossRefPubMedCentralGoogle Scholar
  14. Botta O, Bada JL (2002) Extraterrestrial organic compounds in meteorites. Surv Geophys 23:411–467CrossRefGoogle Scholar
  15. Bowman J, Hud N, Williams L (2015) The ribosome challenge to the RNA world. J Mol Evol 80:143–161PubMedCrossRefPubMedCentralGoogle Scholar
  16. Brister MM, Pollum M, Crespo-Hernandez CE (2016) Photochemical etiology of promising ancestors of the RNA nucleobases. Phys Chem Chem Phys 18:20097–20103PubMedCrossRefPubMedCentralGoogle Scholar
  17. Buckley R, Enekwa CD, Williams LD, Hud NV (2011) Molecular recognition of Watson-Crick-like purine-purine base pairs. Chembiochem 12:2155–2158PubMedCrossRefPubMedCentralGoogle Scholar
  18. Cafferty BJ, Hud NV (2014) Abiotic synthesis of RNA in water: a common goal of prebiotic chemistry and bottom-up synthetic biology. Curr Opin Chem Biol 22:146–157PubMedCrossRefPubMedCentralGoogle Scholar
  19. Cafferty BJ, Hud NV (2015) Was a pyrimidine-pyrimidine base pair the ancestor of Watson-Crick base pairs? Insights from a systematic approach to the origin of RNA. Isr J Chem 55:891–905CrossRefGoogle Scholar
  20. Cafferty BJ, Gallego I, Chen MC, Farley KI, Eritja R, Hud NV (2013) Efficient self-assembly in water of long noncovalent polymers by nucleobase analogues. J Am Chem Soc 135:2447–2450PubMedCrossRefPubMedCentralGoogle Scholar
  21. Cafferty BJ, Avirah RR, Schuster GB, Hud NV (2014) Ultra-sensitive pH control of supramolecular polymers and hydrogels: pK(a) matching of biomimetic monomers. Chem Sci 5:4681–4686CrossRefGoogle Scholar
  22. Cafferty BJ, Fialho DM, Khanam J, Krishnamurthy R, Hud NV (2016) Spontaneous formation and base pairing of plausible prebiotic nucleotides in water. Nat Commun 7:11328PubMedPubMedCentralCrossRefGoogle Scholar
  23. Callahan MP, Smith KE, Cleaves HJ, Ruzicka J, Stern JC, Glavin DP, House CH, Dworkin JP (2011) Carbonaceous meteorites contain a wide range of extraterrestrial nucleobases. Proc Natl Acad Sci U S A 108:13995–13998PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cassidy LM, Burcar BT, Stevens W, Moriarty EM, McGown LB (2014) Guanine-centric self-assembly of nucleotides in water: an important consideration in prebiotic chemistry. Astrobiology 14:876–886PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chen MC, Cafferty BJ, Mamajanov I, Gállego I, Khanam J, Krishnamurthy R, Hud NV (2014) Spontaneous prebiotic formation of a β-ribofuranoside that self-assembles with a complementary heterocycle. J Am Chem Soc 136:5640–5646PubMedCrossRefPubMedCentralGoogle Scholar
  26. Cleaves HJ, Nelson KE, Miller SL (2006) The prebiotic synthesis of pyrimidines in frozen solution. Naturwissenschaften 93:228–231PubMedCrossRefPubMedCentralGoogle Scholar
  27. Cnossen I, Sanz-Forcada J, Favata F, Witasse O, Zegers T, Arnold NF (2007) Habitat of early life: solar X-ray and UV radiation at Earth’s surface 4-3.5 billion years ago. J Geophys Res Planets 112:10CrossRefGoogle Scholar
  28. Crespo-Hernandez CE, Cohen B, Hare PM, Kohler B (2004) Ultrafast excited-state dynamics in nucleic acids. Chem Rev 104:1977–2019PubMedCrossRefPubMedCentralGoogle Scholar
  29. Crick FHC (1968) The origin of the genetic code. J Mol Biol 38:367–379PubMedCrossRefPubMedCentralGoogle Scholar
  30. Davis JT (2004) G-quartets 40 years later: from 5'-GMP to molecular biology and supramolecular chemistry. Angew Chem Int Ed Engl 43:668–698PubMedCrossRefGoogle Scholar
  31. Davis JT, Spada GP (2007) Supramolecular architectures generated by self-assembly of guanosine derivatives. Chem Soc Rev 36:296–313PubMedCrossRefGoogle Scholar
  32. Decker P, Schweer P, Pohlmann R (1982) Identification of formose sugars, presumable prebiotic metabolites, using capillary gas chromatography/gas chromatography-mass spectroscopy of n-butoxime trifluoroacetates on OV-225. J Chromatogr 244:281–291CrossRefGoogle Scholar
  33. Dorr M, Loffler PMG, Monnard PA (2012) Non-enzymatic polymerization of nucleic acids from monomers: monomer self-condensation and template-directed reactions. Curr Org Synth 9:735–763CrossRefGoogle Scholar
  34. Egli M, Pallan PS, Pattanayek R, Wilds CJ, Lubini P, Minasov G, Dobler M, Leumann CJ, Eschenmoser A (2006) Crystal structure of homo-DNA and Nature’s choice of pentose over hexose in the genetic system. J Am Chem Soc 128:10847–10856PubMedCrossRefGoogle Scholar
  35. Engelhart AE, Hud NV (2010) Primitive genetic polymers. Cold Spring Harb Perspect Biol 2:a002196.  https://doi.org/10.1101/cshperspect.a002196CrossRefPubMedPubMedCentralGoogle Scholar
  36. Eschenmoser A (1999) Chemical etiology of nucleic acid structure. Science 284:2118–2124PubMedCrossRefGoogle Scholar
  37. Eschenmoser A (2004) The TNA-family of nucleic acid systems: properties and prospects. Orig Life Evol Biosph 34:277–306PubMedCrossRefGoogle Scholar
  38. Eschenmoser A (2007) The search for the chemistry of life’s origin. Tetrahedron 63:12821–12844CrossRefGoogle Scholar
  39. Eschenmoser A (2011) Etiology of potentially primordial biomolecular structures: from vitamin B12 to the nucleic acids and an inquiry into the chemistry of life’s origin: A retrospective. Angew Chem Int Ed Engl 50:12412–12472PubMedCrossRefGoogle Scholar
  40. Fernando C, Von Kiedrowski G, Szathmary E (2007) A stochastic model of nonenzymatic nucleic acid replication: “Elongators” sequester replicators. J Mol Evol 64:572–585PubMedCrossRefPubMedCentralGoogle Scholar
  41. Ferris JP, Hagan WJ (1984) HCN and chemical evolution - the possible role of cyano compounds in prebiotic synthesis. Tetrahedron 40:1093–1120PubMedCrossRefPubMedCentralGoogle Scholar
  42. Ferris JP, Sanchez RA, Orgel LE (1968) Synthesis of pyrimidines from cyanoacetylene and cyanate. J Mol Biol 33:693–704PubMedCrossRefGoogle Scholar
  43. Ferris JP, Hill AR, Liu RH, Orgel LE (1996) Synthesis of long prebiotic oligomers on mineral surfaces. Nature 381:59–61PubMedCrossRefPubMedCentralGoogle Scholar
  44. Fialho DM, Clarke KC, Moore MK, Schuster GB, Krishnamurthy R, Hud NV (2018) Glycosylation of a model proto-RNA nucleobase with non-ribose sugars: implications for the prebiotic synthesis of nucleosides. Org Biomol Chem 16:1263–1271PubMedCrossRefPubMedCentralGoogle Scholar
  45. Forsythe JG, Yu SS, Mamajanov I, Grover MA, Krishnamurthy R, Fernandez FM, Hud NV (2015) Ester-mediated amide bond formation driven by wet-dry cycles: a possible path to polypeptides on the prebiotic Earth. Angew Chem Int Ed Engl 54:9871–9875PubMedPubMedCentralCrossRefGoogle Scholar
  46. Fripiat JJ, Cruzcump M (1974) Clays as catalysts for natural processes. Annu Rev Earth Planet Sci 2:239–256CrossRefGoogle Scholar
  47. Fuller WD, Sanchez RA, Orgel LE (1972a) Studies in prebiotic synthesis. VI. Synthesis of purine nucleosides. J Mol Biol 67:25–33PubMedCrossRefGoogle Scholar
  48. Fuller WD, Sanchez RA, Orgel LE (1972b) Studies in prebiotic synthesis: VII. Solid-state synthesis of purine nucleosides. J Mol Evol 1:249–257PubMedCrossRefGoogle Scholar
  49. Gavette JV, Stoop M, Hud NV, Krishnamurthy R (2016) RNA-DNA chimeras in the context of an RNA world transition to an RNA/DNA world. Angew Chem Int Ed Engl 55:13204–13209PubMedCrossRefGoogle Scholar
  50. Gellert M, Lipsett MN, Davies DR (1962) Helix formation by guanylic acid. Proc Natl Acad Sci U S A 48:2013–2018PubMedPubMedCentralCrossRefGoogle Scholar
  51. Gesteland RF, Cech TR, Atkins JF (2006) The RNA world, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  52. Grew ES, Bada JL, Hazen RM (2011) Borate minerals and origin of the RNA world. Origins Life Evol Biosph 41:307–316CrossRefGoogle Scholar
  53. Groebke K, Hunziker J, Fraser W, Peng L, Diederichsen U, Zimmermann K, Holzner A, Leumann C, Eschenmoser A (1998) Why pentose- and not hexose-nucleic acids? Purine-purine pairing in homo-DNA: guanine, isoguanine, 2,6-diaminopurine, and xanthine. Helv Chim Acta 81:375–474CrossRefGoogle Scholar
  54. Grossmann TN, Strohbach A, Seitz O (2008) Achieving turnover in DNA-templated reactions. Chembiochem 9:2185–2192PubMedCrossRefGoogle Scholar
  55. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849–857PubMedCrossRefGoogle Scholar
  56. Harvey GR, Degens ET, Mopper K (1971) Synthesis of nitrogen heterocycles on kaolinite from CO2 and NH3. Naturwissenschaften 58:624–625CrossRefGoogle Scholar
  57. Hayatsu R, Studier MH, Oda A, Fuse K, Anders E (1968) Origin of organic matter in early solar system 2. Nitrogen compounds. Geochim Cosmochim Acta 32:175–190CrossRefGoogle Scholar
  58. Hayatsu R, Studier MH, Moore LP, Anders E (1975) Purines and triazines in murchison meteorite. Geochim Cosmochim Acta 39:471–488CrossRefGoogle Scholar
  59. He C, Gallego I, Laughlin B, Grover MA, Hud NV (2017) A viscous solvent enables information transfer from gene-length nucleic acids in a model prebiotic replication cycle. Nat Chem 9:318–324PubMedCrossRefPubMedCentralGoogle Scholar
  60. Herdewijn P (2001) TNA as a potential alternative to natural nucleic acids. Angew Chem Int Ed Eng 40:2249–2251CrossRefGoogle Scholar
  61. Heuberger BD, Switzer C (2008) An alternative nucleobase code: characterization of purine-purine DNA double helices bearing guanine-isoguanine and diaminopurine-7-deaza-xanthine base pairs. Chembiochem 9:2779–2783PubMedCrossRefPubMedCentralGoogle Scholar
  62. Hoogsteen K (1959) The structure of crystals containing a hydrogen-bonded complex of 1-methylthymine and 9-methyladenine. Acta Crystallogr 12:822–823CrossRefGoogle Scholar
  63. Horowitz ED, Lilavivat S, Holladay BW, Germann MW, Hud NV (2009) Solution structure and thermodynamics of 2′,5′ RNA intercalation. J Am Chem Soc 131:5831–5838PubMedCrossRefPubMedCentralGoogle Scholar
  64. Howard FB, Miles HT (1977) Interaction of poly(A) and poly(I), a reinvestigation. Biochemistry 16:4647–4650PubMedCrossRefPubMedCentralGoogle Scholar
  65. Hud NV (2017) Our odyssey to find a plausible prebiotic path to RNA: the first twenty years. Synlett 28:36–55CrossRefGoogle Scholar
  66. Hud NV, Anet FAL (2000) Intercalation-mediated synthesis and replication: a new approach to the origin of life. J Theor Biol 205:543–562PubMedCrossRefPubMedCentralGoogle Scholar
  67. Hud NV, Jain SS, Li X, Lynn DG (2007) Addressing the problems of base pairing and strand cyclization in template-directed synthesis. Chem Biodivers 4:768–783PubMedCrossRefGoogle Scholar
  68. Hud NV, Cafferty BJ, Krishnamurthy R, Williams LD (2013) The origin of RNA and ‘My grandfather’s axe’. Chem Biol 20:466–474PubMedCrossRefGoogle Scholar
  69. Johnson AP, Cleaves HJ, Dworkin JP, Glavin DP, Lazcano A, Bada JL (2008) The Miller volcanic spark discharge experiment. Science 322:404–404PubMedCrossRefPubMedCentralGoogle Scholar
  70. Joyce GF, Schwartz AW, Miller SL, Orgel LE (1987) The case for an ancestral genetic system involving simple analogs of the nucleotides. Proc Natl Acad Sci U S A 84:4398–4402PubMedPubMedCentralCrossRefGoogle Scholar
  71. Kim HJ, Benner SA (2015) Prebiotic glycosylation of uracil with electron-donating substituents. Astrobiology 15:301–306PubMedCrossRefGoogle Scholar
  72. Kim HJ, Ricardo A, Illangkoon HI, Kim MJ, Carrigan MA, Frye F, Benner SA (2011) Synthesis of carbohydrates in mineral-guided prebiotic cycles. J Am Chem Soc 133:9457–9468PubMedCrossRefGoogle Scholar
  73. Kolb VM, Dworkin JP, Miller SL (1994) Alternative bases in the RNA world: the prebiotic synthesis of urazole and its ribosides. J Mol Evol 38:549–557PubMedCrossRefPubMedCentralGoogle Scholar
  74. Krishnamurthy R (2015) On the emergence of RNA. Isr J Chem 55:837–850CrossRefGoogle Scholar
  75. Krishnamurthy R, Pitsch S, Minton M, Miculka C, Windhab N, Eschenmoser A (1996) Pyranosyl-RNA: base pairing between homochiral oligonucleotide strands of opposite sense of chirality. Angew Chem Int Ed Engl 35:1537–1541CrossRefGoogle Scholar
  76. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR (1982) Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31:147–157PubMedCrossRefPubMedCentralGoogle Scholar
  77. Kurland CG (2010) The RNA dreamtime. BioEssays 32:866–871PubMedCrossRefPubMedCentralGoogle Scholar
  78. Kuruvilla E, Schuster GB, Hud NV (2013) Enhanced non-enzymatic ligation of homo-purine miniduplexes: Support for greater base stacking in a pre-RNA world. Chembiochem 14(1):45–48.  https://doi.org/10.1002/cbic.201200601CrossRefPubMedPubMedCentralGoogle Scholar
  79. Larralde R, Robertson MP, Miller SL (1995) Rates of decomposition of ribose and other sugars: implications for chemical evolution. Proc Natl Acad Sci U S A 92:8158–8160PubMedPubMedCentralCrossRefGoogle Scholar
  80. Lehn J-M, Mascal M, Decian A, Fischer J (1990) Molecular recognition directed self-assembly of ordered supramolecular strands by cocrystallization of complementary molecular components. J Chem Soc Chem Commun:479–481Google Scholar
  81. Levy M, Miller SL (1998) The stability of the RNA bases: implications for the origin of life. Proc Natl Acad Sci U S A 95:7933–7938PubMedPubMedCentralCrossRefGoogle Scholar
  82. Li C, Cafferty BJ, Karunakaran SC, Schuster GB, Hud NV (2016) Formation of supramolecular assemblies and liquid crystals by purine nucleobases and cyanuric acid in water: Implications for the possible origins of RNA. Phys Chem Chem Phys 18:20091–20096Google Scholar
  83. Ma M, Bong D (2011) Determinants of cyanuric acid and melamine assembly in water. Langmuir 27:8841–8853PubMedCrossRefPubMedCentralGoogle Scholar
  84. Martins Z, Botta O, Fogel ML, Sephton MA, Glavin DP, Watson JS, Dworkin JP, Schwartz AW, Ehrenfreund P (2008) Extraterrestrial nucleobases in the Murchison meteorite. Earth Planet Sci Lett 270:130–136CrossRefGoogle Scholar
  85. Menor-Salván C, Marin-Yaseli MR (2013) A new route for the prebiotic synthesis of nucleobases and hydantoins in water/ice solutions involving the photochemistry of acetylene. Chem Eur J 19:6488–6497PubMedCrossRefPubMedCentralGoogle Scholar
  86. Menor-Salván C, Ruiz-Bermejo DM, Guzman MI, Osuna-Esteban S, Veintemillas-Verdaguer S (2009) Synthesis of pyrimidines and triazines in ice: implications for the prebiotic chemistry of nucleobases. Chem Eur J 15:4411–4418PubMedCrossRefPubMedCentralGoogle Scholar
  87. Miller SL (1953) A production of amino acids under possible primitive Earth conditions. Science 117:528–529PubMedCrossRefPubMedCentralGoogle Scholar
  88. Miller SL (1957) The mechanism of synthesis of amino acids by electric discharges. Biochim Biophys Acta 23:480–489PubMedCrossRefPubMedCentralGoogle Scholar
  89. Miller SL, Urey HC (1959) Organic compound synthesis on the primitive Earth. Science 130:245–251PubMedCrossRefPubMedCentralGoogle Scholar
  90. Mittapalli GK, Osornio YM, Guerrero MA, Reddy KR, Krishnamurthy R, Eschenmoser A (2007) Mapping the landscape of potentially primordial informational oligomers: oligodipeptides tagged with 2,4-disubstituted 5-aminopyrimidines as recognition elements. Angew Chem Int Ed Engl 46:2478–2484PubMedCrossRefPubMedCentralGoogle Scholar
  91. Monnard P-A (2016) Taming prebiotic chemistry: the role of heterogeneous and interfacial catalysis in the emergence of a prebiotic catalytic/information polymer system. Life 6:E40PubMedCrossRefPubMedCentralGoogle Scholar
  92. Nielsen PE (2007) Peptide nucleic acids and the origin of life. Chem Biodivers 4:1996–2002PubMedCrossRefPubMedCentralGoogle Scholar
  93. Nuevo M, Milam SN, Sandford SA (2012) Nucleobases and prebiotic molecules in organic residues produced from the ultraviolet photo-irradiation of pyrimidine in NH3 and H2O+NH3 ices. Astrobiology 12:295–314PubMedCrossRefPubMedCentralGoogle Scholar
  94. Olby R (2003) Quiet debut for the double helix. Nature 421:402–405PubMedCrossRefPubMedCentralGoogle Scholar
  95. Onimaru K, Kuraku S, Takagi W, Hyodo S, Sharpe J, Tanaka M (2015) A shift in anterior–posterior positional information underlies the fin-to-limb evolution. elife 4:e07048PubMedCentralCrossRefGoogle Scholar
  96. Orgel LE (1968) Evolution of the genetic apparatus. J Mol Biol 38:381–393PubMedCrossRefPubMedCentralGoogle Scholar
  97. Orgel LE (1998) The origin of life – a review of facts and speculations. TIBS 23:491–495PubMedPubMedCentralGoogle Scholar
  98. Orgel LE (2004) Prebiotic chemistry and the origin of the RNA world. Crit Rev Biochem Mol Biol 39:99–123PubMedCrossRefPubMedCentralGoogle Scholar
  99. Oró J (1960) Synthesis of adenine from ammonium cyanide. Biochem Biophys Res Commun 2:407–412CrossRefGoogle Scholar
  100. Oró J (2002) In: Schopf W (ed) Life’s origin: the beginnings of biological evolution. University of California, Berkeley, pp 7–45Google Scholar
  101. Petrov AS, Bernier CR, Hsiao CL, Norris AM, Kovacs NA, Waterbury CC, Stepanov VG, Harvey SC, Fox GE, Wartell RM et al (2014) Evolution of the ribosome at atomic resolution. Proc Natl Acad Sci U S A 111:10251–10256PubMedPubMedCentralCrossRefGoogle Scholar
  102. Pitsch S, Wendeborn S, Jaun B, Eschenmoser A (1993) Why pentose- and not hexose-nucleic acids? Part VII. Pyranosyl-RNA(‘p-RNA’). Helv Chim Acta 76:2161–2183CrossRefGoogle Scholar
  103. Pongs O, Ts’o POP (1971) Polymerization of unprotected 2′-deoxyribonucleoside 5′-phosphates at elevated temperature. J Am Chem Soc 93:5241–5250PubMedCrossRefPubMedCentralGoogle Scholar
  104. Powner MW, Gerland B, Sutherland JD (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459:239–242PubMedCrossRefGoogle Scholar
  105. Powner MW, Sutherland JD, Szostak JW (2011) The origins of nucleotides. Synlett 14:1956–1964CrossRefGoogle Scholar
  106. Prins LJ, Reinhoudt DN, Timmerman P (2001) Noncovalent synthesis using hydrogen bonding. Angew Chem Int Ed 40:2382–2426CrossRefGoogle Scholar
  107. Rajamani S, Vlassov A, Benner S, Coombs A, Olasagasti F, Deamer D (2008) Lipid-assisted synthesis of RNA-like polymers from mononucleotides. Orig Life Evol Biosph 38:57–74PubMedCrossRefPubMedCentralGoogle Scholar
  108. Rakotondradany F, Palmer A, Toader V, Chen BZ, Whitehead MA, Sleiman HF (2005) Hydrogen-bond self-assembly of DNA-analogues into hexameric rosettes. Chem Comm:5441–5443Google Scholar
  109. Rhodes D, Lipps HJ (2015) G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res 43:8627–8637PubMedPubMedCentralCrossRefGoogle Scholar
  110. Ricardo A, Carrigan MA, Olcott AN, Benner SA (2004) Borate minerals stabilize ribose. Science 303:196–196PubMedCrossRefGoogle Scholar
  111. Rich A (1962) In: Kasha M, Pullmann B (eds) Horizons in biochemistry. Academic Press, New York, pp 103–126Google Scholar
  112. Roberts C, Chaput JC, Switzer C (1997) Beyond guanine quartets: cation-induced formation of homogenous and chimeric DNA tetraplexes incorporating iso-guanine and guanine. Chem Biol 4:899–908PubMedCrossRefPubMedCentralGoogle Scholar
  113. Robertson MP, Miller SL (1995) An efficient prebiotic synthesis of cytosine and uracil (vol 375, pg 772, 1995). Nature 377:257–257CrossRefGoogle Scholar
  114. Rode BM (1999) Peptide and the origin of life. Peptides 20:773–786PubMedCrossRefPubMedCentralGoogle Scholar
  115. Sagi VN, Punna V, Hu F, Meher G, Krishnamurthy R (2012) Exploratory experiments on the chemistry of the “glyoxylate scenario”: Formation of ketosugars from dihydroxyfumarate. J Am Chem Soc 134:3577–3589PubMedPubMedCentralCrossRefGoogle Scholar
  116. Saladino R, Crestini C, Costanzo G, Negri R, DiMauro E (2001) A possible prebiotic synthesis of purine, adenine, cytosine, and 4(3H)-pyrimidinone from formamide: implications for the origin of life. Bioorgan Med Chem 9:1249–1253CrossRefGoogle Scholar
  117. Saladino R, Crestini C, Costanzo G, DiMauro E (2004) Advances in the prebiotic synthesis of nucleic acids bases: implications for the origin of life. Curr Org Chem 8:1425–1443CrossRefGoogle Scholar
  118. Saladino R, Šponer JE, Šponer J, Di Mauro E (2018) Rewarming the primordial soup: revisitations and rediscoveries in prebiotic chemistry. Chembiochem 19(1):22–25PubMedCrossRefGoogle Scholar
  119. Sanchez RA, Orgel LE (1970) Studies in prebiotic synthesis. V. Synthesis and photoanomerization of pyrimidine nucleosides. J Mol Biol 47:531–543PubMedCrossRefGoogle Scholar
  120. Sanchez RA, Ferris JP, Orgel LE (1968) Studies in prebiotic synthesis. 4. Conversion of 4-aminoimidazole-5-carbonitrile derivatives to purines. J Mol Biol 38:121–128PubMedCrossRefGoogle Scholar
  121. Schöning KU, Scholz P, Guntha S, Wu X, Krishnamurthy R, Eschenmoser A (2000) Chemical etiology of nucleic acid structure: the alpha-threofuranosyl-(3′->2′) oligonucleotide system. Science 290:1347–1351PubMedCrossRefPubMedCentralGoogle Scholar
  122. Schwartz AW (1997) Speculation on the RNA precursor problem. J Theor Biol 187:523–527PubMedCrossRefPubMedCentralGoogle Scholar
  123. Schwartz AW (2006) Phosphorus in prebiotic chemistry. Philos Trans R Soc Lond B:1743–1749Google Scholar
  124. Seto CT, Whitesides GM (1990) Self-assembly based on the cyanuric acid melamine lattice. J Am Chem Soc 112:6409–6411CrossRefGoogle Scholar
  125. Shapiro R (1988) Prebiotic ribose synthesis: a critical analysis. Orig Life Evol Biosph 18:71–85PubMedCrossRefPubMedCentralGoogle Scholar
  126. Shapiro R (1999) Prebiotic cytosine synthesis: a critical analysis and implications for the origin of life. Proc Natl Acad Sci U S A 96:4396–4401PubMedPubMedCentralCrossRefGoogle Scholar
  127. Sheng Y, Bean HD, Mamajanova I, Hud NV, Leszczynski J (2009) A comprehensive investigation of the energetics of pyrimidine nucleoside formation in a model prebiotic reaction. J Am Chem Soc 131:16088–16095PubMedCrossRefPubMedCentralGoogle Scholar
  128. Sheng J, Li L, Engelhart AE, Gan JH, Wang JW, Szostak JW (2014) Structural insights into the effects of 2′-5′ linkages on the RNA duplex. Proc Natl Acad Sci U S A 111:3050–3055PubMedPubMedCentralCrossRefGoogle Scholar
  129. Shubin N (2008) Your inner fish: a journey into the 3.5-billion-year history of the human body. Pantheon, New YorkGoogle Scholar
  130. Stoks PG, Schwartz AW (1979) Uracil in carbonaceous meteorites. Nature 282:709–710CrossRefGoogle Scholar
  131. Strecker A (1850) Ueber die künstliche Bildung der Milchsäure und einen neuen, dem Glycocoll homologen Körper. Justus Liebigs Ann Chem 75:27–45CrossRefGoogle Scholar
  132. Sun ZH, Chen DL, Lan T, McLaughlin LW (2002) Importance of minor groove functional groups for the stability of DNA duplexes. Biopolymers 65:211–217PubMedCrossRefPubMedCentralGoogle Scholar
  133. Watson JD, Crick FHC (1953) Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171:737–738PubMedCrossRefGoogle Scholar
  134. Weber AL (1992) Prebiotic sugar synthesis: hexose and hydroxy acid synthesis from glyceraldehyde catalyzed by iron(III) hydroxide oxide. J Mol Evol 35:1–6PubMedCrossRefPubMedCentralGoogle Scholar
  135. Westheimer FH (1987) Why nature chose phosphates. Science 235:1173–1178PubMedCrossRefGoogle Scholar
  136. Wimberly BT, Brodersen DE, Clemons WM, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V (2000) Structure of the 30S ribosomal subunit. Nature 407:327–339PubMedCrossRefPubMedCentralGoogle Scholar
  137. Woese C (1967) The genetic code. Harper & Row, New York, pp 179–195Google Scholar
  138. Wulff G, Clarkson G (1994) On the synthesis of C-glycosyl compounds containing double-bonds without the use of protecting groups. Carbohydr Res 257:81–95CrossRefGoogle Scholar
  139. Yang Y-W, Zhang S, McCullum EO, Chaput JC (2007) Experimental evidence that GNA and TNA were not sequential polymers in the prebiotic evolution of RNA. J Mol Evol 65:289–295PubMedCrossRefPubMedCentralGoogle Scholar
  140. Yu Y, Nakamura D, DeBoyace K, Neisius AW, McGown LB (2008) Tunable thermoassociation of binary guanosine gels. J Phys Chem B 112:1130–1134PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Brian J. Cafferty
    • 1
  • David M. Fialho
    • 1
  • Nicholas V. Hud
    • 1
  1. 1.School of Chemistry and Biochemistry, NSF-NASA Center for Chemical EvolutionGeorgia Institute of TechnologyAtlantaUSA

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