Hypothesis: Spontaneous Advent of the Prebiotic Translation System via the Accumulation of L-Shaped RNA Elements

Agmon, Ilana

doi:10.3390/ijms19124021

Cited by 6 publications

(11 citation statements)

References 44 publications

(58 reference statements)

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“…The kissing contacts were experimentally detected in the case of bacterial and viral systems, where they are prevalent in regulatory complexes [ 25 , 26 ]. This is also in line with the self-referential hypothesis for genetic code origins that assumes “kissing” between complementary tRNA anticodons [ 27 , 28 ], forming a structure similar to the ribosomal peptide elongation core [ 29 ]. The complementary hairpin kissing complexes are relatively stable.…”

Section: Discussionsupporting

confidence: 79%

Combinatorial Fusion Rules to Describe Codon Assignment in the Standard Genetic Code

Nesterov‐Mueller

Popov

Seligmann

2020

Life

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We propose combinatorial fusion rules that describe the codon assignment in the standard genetic code simply and uniformly for all canonical amino acids. These rules become obvious if the origin of the standard genetic code is considered as a result of a fusion of four protocodes: Two dominant AU and GC protocodes and two recessive AU and GC protocodes. The biochemical meaning of the fusion rules consists of retaining the complementarity between cognate codons of the small hydrophobic amino acids and large charged or polar amino acids within the protocodes. The proto tRNAs were assembled in form of two kissing hairpins with 9-base and 10-base loops in the case of dominant protocodes and two 9-base loops in the case of recessive protocodes. The fusion rules reveal the connection between the stop codons, the non-canonical amino acids, pyrrolysine and selenocysteine, and deviations in the translation of mitochondria. Using fusion rules, we predicted the existence of additional amino acids that are essential for the development of the standard genetic code. The validity of the proposed partition of the genetic code into dominant and recessive protocodes is considered referring to state-of-the-art hypotheses. The formation of two aminoacyl-tRNA synthetase classes is compatible with four-protocode partition.

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Section: Discussionsupporting

confidence: 79%

Combinatorial Fusion Rules to Describe Codon Assignment in the Standard Genetic Code

Nesterov‐Mueller

Popov

Seligmann

2020

Life

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“…The periodicity property in the 16S 3ʹ region largely corresponds to the 'proto-SSU' that has been proposed to represent the primordial ribosomal SSU [49,50,57,58]. Thus, our results provide additional support for the hypothesis that the primordial coding system was RNA-based, and this RNA translation template then evolved to form the modern tRNA, mRNA and rRNA sequences [59,60].…”

Section: Discussionsupporting

confidence: 73%

“…Notably, the 3ʹ major domain contains the decoding centre and interacts with both tRNA and mRNA. The decoding centre is widely accepted to be an essential building block of the primaeval 'proto-ribosome' that was already present in the Last Universal Common Ancestor (LUCA) [49,50], where it may have simply been a location to bind RNAs in an open structure configuration [51].…”

Section: Structural and Functional Analysis Of Circular Code Periodicity In 16s Rrnamentioning

confidence: 99%

Identification of a circular code periodicity in the bacterial ribosome: origin of codon periodicity in genes?

Michel

Thompson

2020

RNA Biology

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Three-base periodicity (TBP), where nucleotides and higher order n-tuples are preferentially spaced by 3, 6, 9, etc. bases, is a well-known intrinsic property of protein-coding DNA sequences. However, its origins are still not fully understood. One hypothesis is that the periodicity reflects a primordial coding system that was used before the emergence of the modern standard genetic code (SGC). Recent evidence suggests that the X circular code, a set of 20 trinucleotides allowing the reading frames in genes to be retrieved locally, represents a possible ancestor of the SGC. Motifs from the X circular code have been found in the reading frame of protein-coding regions in extant organisms from bacteria to eukaryotes, in many transfer RNA (tRNA) genes and in important functional regions of the ribosomal RNA (rRNA), notably in the peptidyl transferase centre and the decoding centre. Here, we have used a powerful correlation function to search for periodicity patterns involving the 20 trinucleotides of the X circular code in a large set of bacterial proteincoding genes, as well as in the translation machinery, including rRNA and tRNA sequences. As might be expected, we found a strong circular code periodicity 0 modulo 3 in the protein-coding genes. More surprisingly, we also identified a similar circular code periodicity in a large region of the 16S rRNA. This region includes the 3ʹ major domain corresponding to the primordial proto-ribosome decoding centre and containing numerous sites that interact with the tRNA and messenger RNA (mRNA) during translation. Furthermore, 3D structural analysis shows that the periodicity region surrounds the mRNA channel that lies between the head and the body of the SSU. Our results support the hypothesis that the X circular code may constitute an ancestral translation code involved in reading frame retrieval and maintenance, traces of which persist in modern mRNA, tRNA and rRNA despite their long evolution and adaptation to the SGC.

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“…In a comprehensive analysis of ribosome structural data, we show that most of these universally conserved X motifs, denoted uX motifs, are located in important functional sites, including the decoding center and the peptidyl transferase center (PTC). Furthermore, these functional sites are widely accepted to be essential building blocks of the primeval "proto-ribosome" that was already present in the LUCA (Smith et al 2008;Bokov and Steinberg 2009;Hsiao et al 2009Hsiao et al , 2013Petrov et al 2015;Agmon 2017Agmon , 2018. Building on the previously described accretion models of ribosome growth (Hsiao et al 2009;Petrov et al 2015), we propose that error-correcting circular codes represent an important step in the coevolution of the genetic code and the ribosome, in which a single code allowed the simultaneous coding of amino acids and synchronization of the reading frame.…”

Section: Introductionmentioning

confidence: 88%

“…uX motifs were present in the primordial proto-ribosome It is generally assumed that the large and small subunits of the ribosome initially existed independently, although there is some debate as to whether the LSU or the SSU emerged first (Kunnev and Gospodinov 2018;Opron and Burton 2018). Based on comparative structural analyses, proto-LSU (Smith et al 2008;Bokov and Steinberg 2009;Hsiao et al 2009Hsiao et al , 2013Petrov et al 2015;Agmon 2017) and proto-SSU (Petrov et al 2015;Agmon 2018) models have been proposed (Fig. 7).…”

Section: Ux Motifs Map To Functional Centers Of Modern Ribosomesmentioning

confidence: 99%

Circular code motifs in the ribosome: a missing link in the evolution of translation?

Dila

Ripp

Mayer

et al. 2019

RNA

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The origin of the genetic code remains enigmatic five decades after it was elucidated, although there is growing evidence that the code coevolved progressively with the ribosome. A number of primordial codes were proposed as ancestors of the modern genetic code, including comma-free codes such as the RRY, RNY, or GNC codes (R = G or A, Y = C or T, N = any nucleotide), and the X circular code, an error-correcting code that also allows identification and maintenance of the reading frame. It was demonstrated previously that motifs of the X circular code are significantly enriched in the protein-coding genes of most organisms, from bacteria to eukaryotes. Here, we show that imprints of this code also exist in the ribosomal RNA (rRNA). In a large-scale study involving 133 organisms representative of the three domains of life, we identified 32 universal X motifs that are conserved in the rRNA of >90% of the organisms. Intriguingly, most of the universal X motifs are located in rRNA regions involved in important ribosome functions, notably in the peptidyl transferase center and the decoding center that form the original "proto-ribosome." Building on the existing accretion models for ribosome evolution, we propose that error-correcting circular codes represented an important step in the emergence of the modern genetic code. Thus, circular codes would have allowed the simultaneous coding of amino acids and synchronization of the reading frame in primitive translation systems, prior to the emergence of more sophisticated start codon recognition and translation initiation mechanisms.

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Hypothesis: Spontaneous Advent of the Prebiotic Translation System via the Accumulation of L-Shaped RNA Elements

Cited by 6 publications

References 44 publications

Combinatorial Fusion Rules to Describe Codon Assignment in the Standard Genetic Code

Combinatorial Fusion Rules to Describe Codon Assignment in the Standard Genetic Code

Identification of a circular code periodicity in the bacterial ribosome: origin of codon periodicity in genes?

Circular code motifs in the ribosome: a missing link in the evolution of translation?

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