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A comparison of RNA (left) with DNA (right), showing the helices and nucleobases each employs. The RNA world hypothesis proposes that life based on ribonucleic acid (RNA) predates the current world of life based on deoxyribonucleic acid (DNA), RNA and proteins. RNA is able both to store genetic information, like DNA, and to catalyze chemical reactions, like an enzyme protein. It may therefore have supported pre-cellular life and been a major step in the evolution of cellular life. In a recent review of the evidence, Thomas Čech suggests that multiple self-replicating molecular systems probably preceded RNA. Proteins large enough to self-fold and have useful activities came about only after RNA was available to catalyze peptide ligation or amino acid polymerization, although amino acids and short peptides were present in the earlier mixtures.[1] Čech proposes that the RNA world evolved into a world of RNP enzymes, such as the ribosome and ribozymes, before giving rise to the DNA, RNA and protein world of today. DNA is thought to have taken over the role of data storage due to its increased stability, while proteins, through a greater variety of monomers (amino acids), replaced RNA's role in specialized biocatalysis. The RNA world hypothesis suggests that RNA in modern cells is an evolutionary remnant of the RNA world that preceded ours. Contents 1 History 2 Properties of RNA 2.1 RNA as an enzyme 2.2 RNA in information storage 2.2.1 Comparison of DNA and RNA structure 2.2.2 Limitations of information storage in RNA 2.3 RNA as a regulator 3 Support and difficulties 4 Prebiotic RNA synthesis 5 Further developments 6 Alternative hypotheses 7 Implications of the RNA world 8 See also 9 References 10 Further reading 11 External links History The phrase "RNA World" was first used by Nobel laureate Walter Gilbert in 1986, in a commentary on recent observations of the catalytic properties of various forms of RNA.[2] However, the concept of RNA as a primordial molecule[1] is older and can be found in papers by Crick[3] and Orgel,[4] as well as in Woese's 1967 book The Genetic Code.[5] In 1962, the molecular biologist Alexander Rich, of the Massachusetts Institute of Technology, had posited much the same idea in an article he contributed to a volume issued in honor of Nobel-laureate physiologist Albert Szent-Györgyi.[6] Properties of RNA The properties of RNA make the idea of the RNA world hypothesis conceptually plausible, although its general acceptance as an explanation for the origin of life will require further evidence.[6] RNA is known to form efficient catalysts and its similarity to DNA makes its ability to store information clear. Opinions vary, however, as to whether RNA comprised the first autonomous self-replicating system or was a derivative of an earlier system.[1] One version of the hypothesis is that a different type of nucleic acid, termed pre-RNA, was the first one to emerge as a self-reproducing molecule, to be replaced by RNA only later. On the other hand, the recent finding that activated pyrimidine ribonucleotides can be synthesized under plausible prebiotic conditions[7] means that it is premature to dismiss the RNA-first scenarios.[1] Suggestions for 'simple' pre-RNA nucleic acids have included Peptide nucleic acid (PNA), Threose nucleic acid (TNA) or Glycerol nucleic acid (GNA).[8][9] Despite their structural simplicity and possession of properties comparable with RNA, the chemically plausible generation of "simpler" nucleic acids under prebiotic conditions has yet to be demonstrated.[10] RNA as an enzyme Further information: ribozyme RNA enzymes, or ribozymes, are still found in today's DNA-based life and could be examples of living fossils. Ribozymes play vital roles, such as those in the ribosome, which is vital for protein synthesis. Many other ribozyme functions exist; for example, the Hammerhead ribozyme performs self-cleavage[11] and an RNA polymerase ribozyme can autocatalyse its own synthesis.[12] Among the enzymatic properties important for the beginning of life are: The ability to self-duplicate, or duplicate other RNA molecules. Relatively short RNA molecules that can duplicate others have been artificially produced in the lab. The shortest was 165-bases long, though it has been estimated that only part of the molecule was crucial for this function. One version, 189-bases long, had fidelity of 98.9%,[13] which would mean it would make an exact copy of an RNA molecule as long as itself in one of every eight copies. This 189 base pair ribozyme could polymerize a template of at most 14 nucleotides in length, which is too short for replication, but a potential lead for further investigation. The longest primer extension performed by a ribozyme polymerase was 20 bases.[14] The ability to catalyze simple chemical reactions which would enhance the creation of molecules which are building blocks of RNA molecules—i.e., a strand of RNA which would make creating more strands of RNA easier. Relatively short RNA molecules with such abilities have been artificially formed in the lab.[15][16] The ability to catalyse the formation of peptide bonds, in order to produce short peptides or longer proteins. This is done in modern cells by ribosomes, a complex of several RNA molecules known as rRNA and many proteins. The rRNA molecules are thought to be responsible for its enzymatic activity, as no amino acid atoms exist within 18Å of the enzyme's active site.[6] A much shorter RNA molecule has been formed in the laboratory with the ability to form peptide bonds, and it has been suggested that rRNA has evolved from a similar molecule.[17] It has also been suggested that amino acids may have initially been involved with RNA molecules as cofactors enhancing or diversifying their enzymatic capabilities, before evolving to more complex peptides. Similarly, tRNA is suggested to have evolved from RNA molecules that began to catalyze amino acid transfer.[18] RNA in information storage RNA is a very similar molecule to DNA, and only has two chemical differences. The overall structure of RNA and DNA are immensely similar—one strand of DNA and one of RNA can bind to form a double helical structure. This makes the storage of information in RNA possible in a very similar way to the storage of information in DNA. Comparison of DNA and RNA structure Main articles: RNA and DNA The major difference between RNA and DNA is the presence of a hydroxyl group at the 2'-position of the ribose sugar in RNA.[6] This group makes the molecule less stable because when not constrained in a double helix, the 2' hydroxyl can chemically attack the adjacent phosphodiester bond to cleave the phosphodiester backbone. The hydroxyl group also forces the ribose into the C3'-endo sugar conformation unlike the C2'-endo conformation of the deoxyribose sugar in DNA. This forces an RNA double helix to change from a B-DNA structure to one more closely resembling A-DNA. RNA also uses a different set of bases than DNA—adenine, guanine, cytosine and uracil, instead of adenine, guanine, cytosine and thymine. Chemically, uracil is similar to thymine, differing only by a methyl group, and its production requires less energy.[19] In terms of base pairing this has no effect, adenine will readily bind uracil or thymine. Uracil is, however, one product of damage to cytosine making RNA particularly susceptible to mutations which can replace a GC base pair with a GU (wobble) or AU base pair. Limitations of information storage in RNA The chemical properties of RNA make large RNA molecules inherently fragile, and they can easily be broken down into their constituent nucleotides through hydrolysis. The aromatic bases also absorb strongly in the ultraviolet region, and would have been susceptible to damage and breakdown by background radiation.[20][21] These limitations do not make use of RNA as an information storage system impossible, simply energy intensive (to repair or replace damaged RNA molecules) and prone to mutation. While this makes it unsuitable for current 'DNA optimised' life, it may have been acceptable for more primitive life. RNA as a regulator Main article: riboswitch Riboswitches have been found to act as regulators of gene expression, particularly in bacteria, but also in plants and archaea. Riboswitches alter their secondary structure in response to the binding of a metabolite. This change in structure can result in the formation or disruption of a terminator, truncating or permitting transcription respectively.[22] Alternatively, riboswitches may bind or occlude the Shine-dalgarno sequence, affecting translation.[23] It has been suggested that these originated in an RNA-based world.[24] In addition, RNA thermometers regulate gene expression in response to temperature changes.[25] Support and difficulties The RNA World hypothesis is supported by RNA's ability to store, transmit, and duplicate genetic information, as DNA does. RNA can also act as a ribozyme, a special type of enzyme. Because it can perform the tasks of both DNA and enzymes, RNA is believed to have once been capable of supporting independent life forms.[6] In fact, some viruses still use RNA as their genetic material, rather than DNA.[26] Further, while nucleotides were not found in Miller-Urey's origins of life experiments, their formation in prebiotically plausible conditions has now been reported, as noted above;[7] the purine base known as adenine is merely a pentamer of hydrogen cyanide. Experiments with basic ribozymes, like Bacteriophage Qβ RNA, have shown that simple self-replicating RNA structures can withstand even strong selective pressures (e.g., opposite-chirality chain terminators).[27] Additionally, a given RNA molecule in the past might have survived longer than it can today. Ultraviolet light can cause RNA to polymerize while at the same time breaking down other types of organic molecules that could have the potential of causing the breakdown of RNA, suggesting that RNA may have been a relatively common substance on early Earth.[citation needed] This aspect of the theory is still untested and is based on a constant concentration of sugar-phosphate molecules. Since there were no known chemical pathways for the abiogenic synthesis of nucleotides from pyrimidine nucleobases cytosine and uracil under prebiotic conditions, it is thought by some that nucleic acids did not contain these nucleobases seen in life's nucleic acids.[28] The nucleoside cytosine has a half-life in isolation of 19 days at 100 °C (212 °F) and 17,000 years in freezing water, which has been argued to be too short on the geologic time scale for accumulation.[29] Others have questioned whether ribose and other backbone sugars could be stable enough to be found in the original genetic material,[30] and have raised the issue that ribose must all be the same enantiomer as any nucleotide of the wrong chirality acts as a chain terminator.[31] Pyrimidine ribonucleosides and their respective nucleotides have been prebiotically synthesised by a sequence of reactions which by-pass the free sugars, and is assembled in a stepwise fashion by going against the dogma that nitrogenous and oxygenous chemistries should be avoided. In a series of publications, The Sutherland Group at the School of Chemistry, University of Manchester have demonstrated high yielding routes to cytidine and uridine ribonucleotides built from small 2 and 3 carbon fragments such as glycolaldehyde, glyceraldehyde or glyceraldehyde-3-phosphate, cyanamide and cyanoacetylene. One of the steps in this sequence allows the isolation of enantiopure ribose aminooxazoline if the enantiomeric excess of glyceraldehyde is 60 % or greater, of possible interest towards biological homochirality.[32] This can be viewed as a prebiotic purification step, where the said compound spontaneously crystallised out from a mixture of the other pentose aminooxazolines. Aminooxazolines can react with cyanoacetylene in a mild and highly efficient manner, controlled by inorganic phosphate, to give the cytidine ribonucleotides. Photoanomerization with UV light allows for inversion about the 1' anomeric centre to give the correct beta stereochemistry, one problem with this chemistry is the selective phosphorylation of alpha-cytidine at the 2' position.[33] However, in 2009 they showed that the same simple building blocks allow access, via phosphate controlled nucleobase elaboration, to 2',3'-cyclic pyrimidine nucleotides directly, which are known to be able to polymerise into RNA.[34] This was hailed as strong evidence for the RNA world.[35] The paper also highlighted the possibility for the photo-sanitization of the pyrimidine-2',3'-cyclic phosphates.[34] A potential weakness of these routes is the generation of enantioenriched glyceraldehyde, or its 3-phosphate derivative (glyceraldehyde prefers to exist as its keto tautomer dihydroxyacetone).[citation needed] Prebiotic RNA synthesis Nucleotides are the fundamental molecules that combine in series to form RNA. They consist of a nitrogenous base attached to a sugar-phosphate backbone. RNA is made of long stretches of specific nucleotides arranged so that their sequence of bases carries information. The RNA world hypothesis holds that in the primordial soup (or sandwich), there existed free-floating nucleotides. These nucleotides regularly formed bonds with one another, which often broke because the change in energy was so low. However, certain sequences of base pairs have catalytic properties that lower the energy of their chain being created, causing them to stay together for longer periods of time. As each chain grew longer, it attracted more matching nucleotides faster, causing chains to now form faster than they were breaking down. These chains are proposed as the first, primitive forms of life. In an RNA world, different forms of RNA compete with each other for free nucleotides and are subject to natural selection. The most efficient molecules of RNA, the ones able to efficiently catalyze their own reproduction, survived and evolved, forming modern RNA. Such an RNA enzyme, capable of self replication in about an hour, has been identified. It was produced by molecular competition (in vitro evolution) of candidate enzyme mixtures.[36] Competition between RNA may have favored the emergence of cooperation between different RNA chains, opening the way for the formation of the first proto-cell. Eventually, RNA chains randomly developed with catalytic properties that help amino acids bind together (a process called peptide-bonding). These amino acids could then assist with RNA synthesis, giving those RNA chains that could serve as ribozymes the selective advantage. The ability to catalyze one step in protein synthesis, aminoacylation of RNA, has been demonstrated in a short (five-nucleotide) segment of RNA.[37] Further developments Patrick Forterre has been working on a novel hypothesis: that viruses were instrumental in the transition from RNA to DNA and the evolution of Bacteria, Archaea, and Eukaryota. He believes the last common ancestor was RNA-based and evolved RNA viruses. Some of the viruses evolved into DNA viruses to protect their genes from attack. Through the process of viral infection into hosts the three domains of life evolved.[38][39] Another interesting proposal is the idea that RNA synthesis might have been driven by temperature gradients, in the process of thermosynthesis.[40] Recently, Atul Kumar has been the first to demonstrate that single nucleotides have the ability to catalyze organic reactions. This single-nucleotide catalysis has immense impact on many fields of science such as chemistry, biochemistry, and prebiotic studies, especially the RNA world and DNA world hypothesis for understanding the origin of life on Earth.[41] Alternative hypotheses As mentioned above, a different version of the same hypothesis is "Pre-RNA world", where a different nucleic acid is proposed to pre-date RNA. A candidate nucleic acid is peptide nucleic acid (PNA) which uses simple peptide bonds to link nucleobases.[42] PNA is more stable than RNA, but its ability to be generated under prebiological conditions has yet to be demonstrated experimentally. Threose nucleic acid (TNA) has also been proposed as a starting point, as has glycol nucleic acid (GNA), and like PNA, also lack experimental evidence for their respective abiogenesis. An alternative—or complementary— theory of RNA origin is proposed in the PAH world hypothesis, whereby polycyclic aromatic hydrocarbons (PAHs) mediates the synthesis of RNA molecules.[43] PAHs are the most common and abundant of the known polyatomic molecules in the visible Universe, and are a likely constituent of the primordial sea.[44] PAHs, along with fullerenes (also implicated in the origin of life),[45] have been recently detected in nebulae.[46] The iron-sulfur world theory proposes that simple metabolic processes developed before genetic materials did, and these energy-producing cycles catalyzed the production of genes. Yet another alternative theory to the RNA world hypothesis is the panspermia hypothesis. It discusses the possibility that the earliest life on this planet was carried here from somewhere else in the galaxy, possibly on meteorites similar to the Murchison meteorite.[47] This does not invalidate the concept of an RNA world, but posits that this world was not Earth but rather another, probably older, planet. Implications of the RNA world The RNA world hypothesis, if true, has important implications for the definition of life. For the majority of the time following the elucidation of the structure of DNA by Watson and Crick, life was considered as being largely defined in terms of DNA and proteins: DNA and proteins seemed to be the dominant macromolecules in the living cell, with RNA serving only to aid in creating proteins from the DNA blueprint. The RNA world hypothesis places RNA at center-stage when life originated. This has been accompanied by many studies in the last ten years demonstrating important aspects of RNA function that were not previously known, and support the idea of a critical role for RNA in the functionality of life. In 2001, the RNA world hypothesis was given a boost with the deciphering of the 3-dimensional structure of the ribosome, which revealed the key catalytic sites of ribosomes to be composed of RNA and for the proteins to hold no major structural role, and to be of peripheral functional importance. Specifically, the formation of the peptide bond, the reaction that binds amino acids together into proteins, is now known to be catalyzed by an adenine residue in the rRNA: the ribosome is a ribozyme. This finding suggests that RNA molecules were most likely capable of generating the first proteins. Other interesting discoveries demonstrating a role for RNA beyond a simple message or transfer molecule include the importance of small nuclear ribonucleoproteins (snRNPs) in the processing of pre-mRNA and RNA editing and reverse transcription from RNA in Eukaryotes in the maintenance of telomeres in the telomerase reaction.[citation needed] See also Abiogenesis Autocatalytic set The Major Transitions in Evolution Panspermia References ^ a b c d Cech, T.R. (2011). The RNA Worlds in Context. Source: Department of Chemistry and Biochemistry, University of Colorado, Boulder, Colorado 80309-0215. Cold Spring Harb Perspect Biol. 2011 Feb 16. pii: cshperspect.a006742v1. doi: 10.1101/cshperspect.a006742. [Epub ahead of print] ^ Gilbert, Walter (February 1986). "The RNA World". Nature 319 (6055): 618. Bibcode 1986Natur.319..618G. doi:10.1038/319618a0.  ^ Crick FH (1968). "The origin of the genetic code". J Mol Biol 38: 367–379.  ^ Orgel LE (1968). "Evolution of the genetic apparatus". J Mol Biol 38: 381–393.  ^ Woese C.R. (1967). The genetic code: The molecular basis for genetic expression. p. 186. Harper & Row ^ a b c d e Atkins, John F.; Gesteland, Raymond F.; Cech, Thomas (2006). The RNA world: the nature of modern RNA suggests a prebiotic RNA world. Plainview, N.Y: Cold Spring Harbor Laboratory Press. ISBN 0-87969-739-3.  ^ a b Powner M.W., Gerland B, Sutherland J.D. (2009). "Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions". Nature 459: 239–242.  ^ Orgel, Leslie (November 2000). "A Simpler Nucleic Acid". Science 290 (5495): 1306–7. doi:10.1126/science.290.5495.1306. PMID 11185405.  ^ Nelson, K.E.; Levy, M.; Miller, S.L. (April 2000). "Peptide nucleic acids rather than RNA may have been the first genetic molecule". Proc. Natl. Acad. Sci. USA 97 (8): 3868–71. doi:10.1073/pnas.97.8.3868. PMC 18108. PMID 10760258.  ^ Sutherland, J.D; Anastasi, C., Buchet F.F, Crower M.A, Parkes A.L, Powner M. W., Smith J.M. (April 2007). "RNA: Prebiotic Product, or Biotic Invention". Chemistry & Biodiversity 4 (4): 721–739. doi:10.1002/cbdv.200790060. PMID 17443885.  ^ Forster AC, Symons RH (1987). "Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites". Cell 49 (2): 211–220. doi:10.1016/0092-8674(87)90562-9. PMID 2436805.  ^ Johnston W, Unrau P, Lawrence M, Glasner M, Bartel D (2001). "RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension" (PDF). Science 292 (5520): 1319–25. doi:10.1126/science.1060786. PMID 11358999. http://web.wi.mit.edu/bartel/pub/publication_reprints/Johnston_Science01.pdf.  ^ W. K. Johnston, P. J. Unrau, M. S. Lawrence, M. E. Glasner and D. P. Bartel RNA-Catalyzed RNA Polymerization: Accurate and General RNA-Templated Primer Extension. Science 292, 1319 (2001) ^ Hani S. Zaher and Peter J. Unrau, Selection of an improved RNA polymerase ribozyme with superior extension and fidelity. RNA (2007), 13:1017-1026 ^ Huang, Yang, and Yarus, RNA enzymes with two small-molecule substrates. Chemistry & Biology, Vol 5, 669-678, November 1998 ^ Unrau, P. J.; Bartel, D. P. (1998). "RNA-catalysed nucleotide synthesis". Nature 395 (6699): 260–263. doi:10.1038/26193. PMID 9751052.  ^ Zhang, Biliang; Cech, Thomas R. (1997). "Peptide bond formation by in vitro selected ribozymes". Nature 390 (6655): 96–100. doi:10.1038/36375. PMID 9363898.  ^ Szathmary, E. (1999). "The origin of the genetic code: amino acids as cofactors in an RNA world". Trends in Genetics 15 (6): 223–229. doi:10.1016/S0168-9525(99)01730-8. PMID 10354582.  ^ http://www.humpath.com/uracil ^ Lindahl, T (April 1993). "Instability and decay of the primary structure of DNA". Nature 362 (6422): 709–15. doi:10.1038/362709a0. PMID 8469282.  ^ Pääbo, S (November 1993). "Ancient DNA". Scientific American 269 (5): 60–66.  ^ Nudler E, Mironov AS (2004). "The riboswitch control of bacterial metabolism". Trends Biochem Sci 29 (1): 11–7. doi:10.1016/j.tibs.2003.11.004. PMID 14729327.  ^ Tucker BJ, Breaker RR (2005). "Riboswitches as versatile gene control elements". Curr Opin Struct Biol 15 (3): 342–8. doi:10.1016/j.sbi.2005.05.003. PMID 15919195.  ^ Switching the light on plant riboswitches. Samuel Bocobza and Asaph Aharoni Trends in Plant Science Volume 13, Issue 10, October 2008, Pages 526-533 doi:10.1016/j.tplants.2008.07.004 ^ Narberhaus F, Waldminghaus T, Chowdhury S (January 2006). "RNA thermometers". FEMS Microbiol. Rev. 30 (1): 3–16. doi:10.1111/j.1574-6976.2005.004.x. PMID 16438677. http://onlinelibrary.wiley.com/resolve/openurl?genre=article&sid=nlm:pubmed&issn=0168-6445&date=2006&volume=30&issue=1&spage=3. Retrieved 2011-04-23.  ^ Patton, John T. Editor (2008). Segmented Double-stranded RNA Viruses: Structure and Molecular Biology. Caister Academic Press. Editor's affiliation: Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, MD 20892-8026. ISBN 978-1-904455-21-9 ^ Bell, Graham: The Basics of Selection. Springer, 1997. ^ Orgel, L. (1994). "The origin of life on earth". Scientific American 271 (4): 81.  ^ Levy, Matthew; Miller, Stanley L. (1998). "The stability of the RNA bases: Implications for the origin of life". PNAS 95 (14): 7933–7938. doi:10.1073/pnas.95.14.7933. PMC 20907. PMID 9653118. http://www.pnas.org/content/95/14/7933.abstract.  ^ Larralde, R.; Robertson, M. P.; Miller, S. L. (1995). "Rates of decomposition of ribose and other sugars: implications for chemical evolution". PNAS 92 (18): 8158–8160. doi:10.1073/pnas.92.18.8158. PMC 41115. PMID 7667262. http://www.pnas.org/content/92/18/8158.abstract.  ^ Joyce GF; et al. (1984). "Chiral selection in poly(C)-directed synthesis of oligo(G)". Nature 310 (5978): 602–604. doi:10.1038/310602a0. PMID 6462250.  ^ Direct Assembly of Nucleoside Precursors from Two- and Three-Carbon Units Carole Anastasi, Michael A. Crowe, Matthew W. Powner, John D. Sutherland Angewandte Chemie International Edition Volume 45, Issue 37 , Pages 6176 - 6179 ^ Potentially Prebiotic Synthesis of Pyrimidine β-D-Ribonucleotides by Photoanomerization/Hydrolysis of α-D-Cytidine-2′-Phosphate Matthew W. Powner, John D. Sutherland ChemBioChem Volume 9, Issue 15 , Pages 2386 - 2387 ^ a b Powner MW, Gerland B, Sutherland JD (2009). "Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions". Nature 459 (7244): 239–242. doi:10.1038/nature08013. PMID 19444213.  ^ Van Noorden R (2009). "RNA world easier to make". Nature. doi:10.1038/news.2009.471. http://www.nature.com/news/2009/090513/full/news.2009.471.html. [dead link] ^ Lincoln, Tracey A.; Joyce, Gerald F. (January 8, 2009). "Self-Sustained Replication of an RNA Enzyme". Science (New York: American Association for the Advancement of Science) 323 (5918): 1229–32. doi:10.1126/science.1167856. PMC 2652413. PMID 19131595. http://www.sciencemag.org/cgi/content/abstract/1167856. Retrieved 2009-01-13. Lay summary – Medical News Today (January 12, 2009).  ^ Rebecca M. Turk, Nataliya V. Chumachenko, and Michael Yarus (February 22, 2010). "Multiple translational products from a five-nucleotide ribozyme.". Proceedings of the National Academy of Sciences (10): 4585–9. doi:10.1073/pnas.0912895107. ISSN 1091-6490. PMC 2826339. PMID 20176971. Lay summary – ScienceDaily (February 24, 2010).  ^ Zimmer C. (2006). "Did DNA come from viruses?". Science 312 (5775): 870–2. doi:10.1126/science.312.5775.870. PMID 16690855.  ^ Forterre, Patrick. "Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: A hypothesis for the origin of cellular domain" ^ Anthonie W.J. Muller (2005). "Thermosynthesis as energy source for the RNA World: a model for the bioenergetics of the origin of life". Biosystems 82 (1): 93–102. doi:10.1016/j.biosystems.2005.06.003. PMID 16024164.  ^ Kumar, Atul; Siddharth Sharma, Ram Awatar Maurya (2010). "Single Nucleotide-Catalyzed Biomimetic Reductive Amination". Advanced Synthesis and Catalyst 352 (13): 2227. doi:10.1002/adsc.201000178. http://onlinelibrary.wiley.com/doi/10.1002/adsc.201000178/abstract.  ^ Egholm M, Buchardt O, Christensen L, Behrens C, Freier SM, Driver DA, Berg RH, Kim SK, Nordén B, and Nielsen PE (1993). "PNA Hybridizes to Complementary Oligonucleotides Obeying the Watson-Crick Hydrogen Bonding Rules". Nature 365 (6446): 566–8. doi:10.1038/365566a0. PMID 7692304.  ^ Platts, Simon Nicholas, "The PAH World - Discotic polynuclear aromatic compounds as a mesophase scaffolding at the origin of life" ^ Allamandola, Louis et Al. "Cosmic Distribution of Chemical Complexity" ^ Atkinson, Nancy (2010-10-27). "Buckyballs Could Be Plentiful in the Universe". Universe Today. http://www.universetoday.com/76732/buckyballs-could-be-plentiful-in-the-universe. Retrieved 2010-10-28.  ^ García-Hernández, D. A.; Manchado, A.; García-Lario, P.; Stanghellini, L.; Villaver, E.; Shaw, R. A.; Szczerba, R.; Perea-Calderón, J. V. (2010-10-28). "Formation Of Fullerenes In H-Containing Planetary Nebulae". The Astrophysical Journal Letters 724. doi:10.1088/2041-8205/724/1/L39.  ^ Bernstein MP, Sandford SA, Allamandola LJ, Gillette JS, Clemett SJ, Zare RN (February 1999). "UV irradiation of polycyclic aromatic hydrocarbons in ices: production of alcohols, quinones, and ethers". Science (journal) 283 (5405): 1135–8. doi:10.1126/science.283.5405.1135. PMID 10024233.  Further reading Cairns-Smith, A. G. (1993). Genetic Takeover: And the Mineral Origins of Life. Cambridge University Press. ISBN 0-521-23312-7.  Orgel, L. E. (October 1994). "The origin of life on the Earth". Scientific American 271 (4): 76–83. doi:10.1038/scientificamerican1094-76. PMID 7524147.  Orgel, L. E. (2004). "Prebiotic Chemistry and the Origin of the RNA World". Critical Reviews in Biochemistry and Molecular Biology 39 (2): 99–123. doi:10.1080/10409230490460765. ISSN 1549-7798. PMID 15217990.  Woolfson, Adrian (September 2000). Life Without Genes. London: Flamingo. ISBN 978-0006548744.  Vlassov, Alexander V.; Kazakov, Sergei A.; Johnston, Brian H.; Landweber, Laura F. (July 2005). "The RNA World on Ice: A New Scenario for the Emergence of RNA Information". Journal of Molecular Evolution 61 (2): 264–273. doi:10.1007/s00239-004-0362-7. PMID 16044244.  External links "The RNA world" (2001) by Sidney Altman, on the Nobel prize website "Exploring the new RNA world" (2004) by Thomas R. Cech, on the Nobel prize website "The Formation of the RNA World" by James P. Ferris "Exploring Life's Origins: a Virtual Exhibit" http://www.hhmi.org/bulletin/pdf/june2002/RNA.pdf HHMI bulletin v · d · eOrigin of life Quasispecies model · Protobiont · Universal common descent · Last universal ancestor · RNA world hypothesis · Iron–sulfur world theory · PAH world hypothesis · Miller–Urey experiment · Panspermia