Evolution of Nucleotide Punctuation Marks: From Structural to Linear Signals

Abstract

We present an evolutionary hypothesis assuming that signals marking nucleotide synthesis (DNA replication and RNA transcription) evolved from multi- to unidimensional structures, and were carried over from transcription to translation. This evolutionary scenario presumes that signals combining secondary and primary nucleotide structures are evolutionary transitions. Mitochondrial replication initiation fits this scenario. Some observations reported in the literature corroborate that several signals for nucleotide synthesis function in translation, and vice versa. (a) Polymerase-induced frameshift mutations occur preferentially at translational termination signals (nucleotide deletion is interpreted as termination of nucleotide polymerization, paralleling the role of stop codons in translation). (b) Stem-loop hairpin presence/absence modulates codon-amino acid assignments, showing that translational signals sometimes combine primary and secondary nucleotide structures (here codon and stem-loop). (c) Homopolymer nucleotide triplets (AAA, CCC, GGG, TTT) cause transcriptional and ribosomal frameshifts. Here we find in recently described human mitochondrial RNAs that systematically lack mono-, dinucleotides after each trinucleotide (delRNAs) that delRNA triplets include 2x more homopolymers than mitogenome regions not covered by delRNA. Further analyses of delRNAs show that the natural circular code X (a little-known group of 20 translational signals enabling ribosomal frame retrieval consisting of 20 codons {AAC, AAT, ACC, ATC, ATT, CAG, CTC, CTG, GAA, GAC, GAG, GAT, GCC, GGC, GGT, GTA, GTC, GTT, TAC, TTC} universally overrepresented in coding versus other frames of gene sequences), regulates frameshift in transcription and translation. This dual transcription and translation role confirms for X the hypothesis that translational signals were carried over from transcriptional signals.

Genome Improvement and Core Gene Set Refinement of Fugacium kawagutii

“…Secondly, the RNA-Seq reads might also contain the reads of non-coding genes, e.g., long noncoding RNA (lncRNA). Thirdly, non-canonical transcriptions might make the mature mRNA not match to the genome, e.g., alternative transcriptions [36], delRNAs [37,38]. To find out the exact reason, efforts to further understand the genome structure and gene transcription mechanisms of F. kawagutii are needed.…”

When transfer‐messenger RNA scars reveal its ancient origins

“…Interestingly, the tmRNA termination codon is always embedded within a conserved H5 hairpin stem‐loop. The primitive punctuation of this termination signal in the RNA world consisted of such multidimensional structures allowing for recognition by nucleic acid polymerases . These punctuation marks were then certainly hijacked for translation.…”

“…The primitive punctuation of this termination signal in the RNA world consisted of such multidimensional structures allowing for recognition by nucleic acid polymerases. 33 These punctuation marks were then certainly hijacked for translation. The tmRNA H5 helix, located at the end of the internal ORF, could thus be a remnant of an ancient termination signal now including a modern stop codon.…”

Syntenies Between Cohosted Mitochondrial, Chloroplast, and Phycodnavirus Genomes: Functional Mimicry and/or Common Ancestry?

“…Secondary structures formed by mitochondrial tRNAs within long primary mitochondrial RNAs punctuate mitochondrial RNA splicing (Ojala et al, 1981;Shimpi et al, 2017). Secondary structure signals (El Houmami and Seligmann, 2017) also punctuate processing of noncanonical mitochondrial RNAs (Seligmann, 2016a(Seligmann, , 2016b. Megavirales (Mimivirus) (Raoult et al, 2004) and their virophages (La Scola et al, 2008) use similar secondary structure punctuation during posttranscriptional splicing (Byrne et al, 2009;Claverie and Abergel, 2009).…”