Hydrolytic stability of helical RNA: a selective advantage for the natural 3',5'-bond.

Usher, D. A.; McHale, A H

doi:10.1073/pnas.73.4.1149

Cited by 167 publications

(111 citation statements)

References 25 publications

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“…In particular, 2 ,3 cyclic phosphate bridges were reported to promote the formation of phosphodiester bonds connecting preformed oligonucleotides bound to the appropriate sequence-complementary strands in the absence of catalysts [108]. In this system, in addition to the capacity to form phosphate bridges, the higher stability of 3 ,5 bonds relative to 2 ,3 bonds in double-stranded RNA structures was observed [109]. In the presence of 1-2 diamino ethane at alkaline pH the self-polymerization of 2 ,3 cyclic adenosine mono-phosphate (2 ,5 cAMP) was described [110].…”

Section: Abiotic Rnamentioning

confidence: 91%

Formamide and the origin of life

Saladino

Crestini

Pino

et al. 2012

Physics of Life Reviews

257

234

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The complexity of life boils down to the definition: "self-sustained chemical system capable of undergoing Darwinian evolution" (Joyce, 1994) [1]. The term "self-sustained" implies a set of chemical reactions capable of harnessing energy from the environment, using it to carry out programmed anabolic and catabolic functions. We briefly present our opinion on the general validity of this definition.Running anabolic and catabolic functions entails complex chemical information whose stability, reproducibility and evolution constitute the core of what is dubbed genetics.Life as-we-know-it is made of the intimate interaction of metabolism and genetics, both built around the chemistry of the most common elements of the Universe (hydrogen, oxygen, nitrogen, carbon). Other elements like phosphorus and sulphur play important but ancillary and potentially replaceable roles.The reproducible interaction of metabolic and genetic cycles results in the hypercycles of organization and de-organization of chemical information that we consider living entities. In order to approach the problem of the origin of life it is therefore reasonable to start from the assumption that both metabolism and genetics had a common origin, shared a common chemical frame, were embedded in physical-chemical conditions favourable for the onset of both.The most abundant three-atoms organic compound in interstellar environment is hydrogen cyanide HCN, the most abundant three-atoms inorganic compound is water H 2 O. The combination of the two results in the formation of formamide H 2 NCOH. We have explored the chemistry of formamide in conditions compatible with the synthesis and the stability of compounds of potential pre-genetic and pre-metabolic interest. We discuss evidence showing (i) that all the compounds necessary for the build-up of nucleic acids are easily obtained abiotically, (ii) that essentially all the steps leading to the spontaneous generation of RNA are abiotically possible, (iii) that the key compounds of extant metabolic cycles are obtained in the same chemical frame, often in the same test tube.How close are these observations to a plausible scenario for the origin of life?

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Section: Abiotic Rnamentioning

confidence: 91%

Formamide and the origin of life

Saladino

Crestini

Pino

et al. 2012

Physics of Life Reviews

257

234

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“…The 2′-5′ linkage is an alternative form of nucleic acid backbone in addition to the 3′-5′ linkage during molecular evolution (42,43). Previous studies have demonstrated that a mixture of 2′-5′ and 3′-5′ phosphodiester linkage can be obtained during nonenzymatic RNA replication, suggesting a high probability of mixture of phosphodiester linkages in the early evolution of life (3)(4)(5)(6)(7)(8)(9). It is conceivable that RNA in early evolution of life may have contained a mixture of 2′-5′ and 3′-5′ phosphodiester linkages.…”

Section: Insights Into Molecular Evolution Of Phosphodiester Linkagementioning

confidence: 99%

“…Indeed, previous studies revealed that nonenzymatic RNA replication would lead to a mixture of 2′-5′ and 3′-5′ linkages (Fig. 1A) (3)(4)(5)(6)(7)(8)(9). The 2′-5′-linked nucleic acids can form duplex structures by themselves or by pairing with natural nucleic acids (10)(11)(12)(13)(14)(15).…”

mentioning

confidence: 96%

Strand-specific (asymmetric) contribution of phosphodiester linkages on RNA polymerase II transcriptional efficiency and fidelity

Zhang

Chong

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Nonenzymatic RNA polymerization in early life is likely to introduce backbone heterogeneity with a mixture of 2′-5′ and 3′-5′ linkages. On the other hand, modern nucleic acids are dominantly composed of 3′-5′ linkages. RNA polymerase II (pol II) is a key modern enzyme responsible for synthesizing 3′-5′-linked RNA with high fidelity. It is not clear how modern enzymes, such as pol II, selectively recognize 3′-5′ linkages over 2′-5′ linkages of nucleic acids. In this work, we systematically investigated how phosphodiester linkages of nucleic acids govern pol II transcriptional efficiency and fidelity. Through dissecting the impacts of 2′-5′ linkage mutants in the pol II catalytic site, we revealed that the presence of 2′-5′ linkage in RNA primer only modestly reduces pol II transcriptional efficiency without affecting pol II transcriptional fidelity. In sharp contrast, the presence of 2′-5′ linkage in DNA template leads to dramatic decreases in both transcriptional efficiency and fidelity. These distinct effects reveal that pol II has an asymmetric (strand-specific) recognition of phosphodiester linkage. Our results provided important insights into pol II transcriptional fidelity, suggesting essential contributions of phosphodiester linkage to pol II transcription. Finally, our results also provided important understanding on the molecular basis of nucleic acid recognition and genetic information transfer during molecular evolution. We suggest that the asymmetric recognition of phosphodiester linkage by modern nucleic acid enzymes likely stems from the distinct evolutionary pressures of template and primer strand in genetic information transfer during molecular evolution.2′-5′ phosphodiester linkage | trigger loop | synthetic nucleic acid analogues T he remarkable capacity of RNA as the functional catalyst as well as the genetic information carrier provides a strong support for the RNA world hypothesis, in which RNA is proposed to play a key role in the early evolution of primitive life before DNA and protein (enzyme) evolved (1, 2). One critical issue for RNA replication in early life is backbone heterogeneity because RNA contains both 2′-OH and 3′-OH, in which both can form phosphodiester bond during RNA polymerization. Indeed, previous studies revealed that nonenzymatic RNA replication would lead to a mixture of 2′-5′ and 3′-5′ linkages (Fig. 1A) (3-9). The 2′-5′-linked nucleic acids can form duplex structures by themselves or by pairing with natural nucleic acids (10-15). The 2′-5′ linkage substitutions in some functional RNAs retain molecular recognition and catalytic properties (16)(17)(18)(19). These discoveries suggested that the 2′-5′ linkage in nucleic acids could be an important alternative linkage during early evolution.This backbone heterogeneity problem is largely eliminated during evolution. Modern nucleic acids are dominated by 3′-5′ linkages. The 2′-5′ RNA linkages are only present in a few specific processes. One example is the formation of lariat RNA intron during splicing, where the 2′-OH of an...

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“…Nevertheless, the question of how RNA might have evolved to the exclusively 3′,5′‐linked material that is primarily employed by extant biology remains largely unanswered. The well‐known preferential hydrolysis of 2′,5′‐bonds in a helical context11, 13 might have played a key role in this transition, with 3′,5′‐linkages becoming enriched simply through the depletion of 2′,5′‐linked material. However, rather than just degrading RNA, a more plausible scenario would embrace recycling, with formation of new 3′,5′‐bonds through repair of the broken linkages.…”

mentioning

confidence: 99%

“…Under these conditions, both the intact oligomers and the produced fragments are expected to be mainly helical (as estimated by melting point measurements; Figure S2), thereby preventing any degradation of single‐stranded RNA 13. The HPLC was performed under denaturing conditions, however, to allow separation and quantitation of the various species.…”

mentioning

confidence: 99%

Non‐Enzymatic RNA Backbone Proofreading through Energy‐Dissipative Recycling

Mariani

Sutherland

2017

Angew Chem Int Ed

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Non‐enzymatic oligomerization of activated ribonucleotides leads to ribonucleic acids that contain a mixture of 2′,5′‐ and 3′,5′‐linkages, and overcoming this backbone heterogeneity has long been considered a major limitation to the prebiotic emergence of RNA. Herein, we demonstrate non‐enzymatic chemistry that progressively converts 2′,5′‐linkages into 3′,5′‐linkages through iterative degradation and repair. The energetic costs of this proofreading are met by the hydrolytic turnover of a phosphate activating agent and an acylating agent. With multiple rounds of this energy‐dissipative recycling, we show that all‐3′,5′‐linked duplex RNA can emerge from a backbone heterogeneous mixture, thereby delineating a route that could have driven RNA evolution on the early earth.

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Hydrolytic stability of helical RNA: a selective advantage for the natural 3',5'-bond.

Cited by 167 publications

References 25 publications

Formamide and the origin of life

Formamide and the origin of life

Strand-specific (asymmetric) contribution of phosphodiester linkages on RNA polymerase II transcriptional efficiency and fidelity

Non‐Enzymatic RNA Backbone Proofreading through Energy‐Dissipative Recycling

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