Analysis of SD sequences in completed microbial genomes: Non-SD-led genes are as common as SD-led genes

Chang, Bill C.H.; Halgamuge, Saman K.; Tang, Sen‐Lin

doi:10.1016/j.gene.2006.01.033

Cited by 105 publications

(110 citation statements)

References 37 publications

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“…This figure is similar to the estimated rate of 20% in 5ʹ UTRs from annotated CDS [43,44] and above the 10% rate found for random 20-mer sequences inside CDS. Unsupervised search for novel motifs did not yield any significant pattern (data not shown).…”

Section: Resultssupporting

confidence: 86%

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

et al. 2018

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Prokaryotic genomes show a high level of information compaction often with different molecules transcribed from the same locus. Although antisense RNAs have been relatively well studied, RNAs in the same strand, internal RNAs (intraRNAs), are still poorly understood. The question of how common is the translation of overlapping reading frames remains open. We address this question in the model archaeon Halobacterium salinarum. In the present work we used differential RNA-seq (dRNA-seq) in H. salinarum NRC-1 to locate intraRNA signals in subsets of internal transcription start sites (iTSS) and establish the open reading frames associated to them (intraORFs). Using C-terminally flagged proteins, we experimentally observed isoforms accurately predicted by intraRNA translation for kef1, acs3 and orc4 genes. We also recovered from the literature and mass spectrometry databases several instances of protein isoforms consistent with intraRNA translation such as the gas vesicle protein gene gvpC1. We found evidence for intraRNAs in horizontally transferred genes such as the chaperone dnaK and the aerobic respiration related cydA in both H. salinarum and Escherichia coli. Also, intraRNA translation evidence in H. salinarum, E. coli and yeast of a universal elongation factor (aEF-2, fusA and eEF-2) suggests that this is an ancient phenomenon present in all domains of life.

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Section: Resultssupporting

confidence: 86%

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

et al. 2018

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“…A recent analysis of 162 completely sequenced prokaryotic genomes (with 141 of bacterial origin), revealed that an astonishingly large percent (46%) of mRNAs do not contain a SD sequence, with the corresponding value for Escherichia coli mRNA being 39% (40). However, it is well documented that a SD sequence is preferentially found in highly expressed genes (41), suggesting that accuracy during the first decoding step may be more important for high expression, although it is unclear exactly why.…”

Section: Discussionmentioning

confidence: 99%

Shine–Dalgarno interaction prevents incorporation of noncognate amino acids at the codon following the AUG

Giacco

Márquez

Qin

et al. 2008

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

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During translation, usually only one in Ϸ400 misincorporations affects the function of a nascent protein, because only chemically similar near-cognate amino acids are misincorporated in place of the cognate one. The deleterious misincorporation of a chemically dissimilar noncognate amino acid during the selection process is precluded by the presence of a tRNA at the ribosomal E-site. However, the selection of first aminoacyl-tRNA, directly after initiation, occurs without an occupied E-site, i.e., when only the P-site is filled with the initiator tRNA and thus should be highly error-prone. Here, we show how bacterial ribosomes have solved this accuracy problem: In the absence of a Shine-Dalgarno (SD) sequence, the first decoding step at the A-site after initiation is extremely error-prone, even resulting in the significant incorporation of noncognate amino acids. In contrast, when a SD sequence is present, the incorporation of noncognate amino acids is not observed. This is precisely the effect that the presence of a cognate tRNA at the E-site has during the elongation phase. These findings suggest that during the initiation phase, the SD interaction functionally compensates for the lack of codon-anticodon interaction at the E-site by reducing the misincorporation of near-cognate amino acids and prevents noncognate misincorporation. E-site ͉ translational errorsT he binding of aminoacyl-tRNAs to the ribosome is dictated by the complementarity between the anticodon of the tRNA and the codon of the mRNA. To ensure the high fidelity of translation, the correct stereochemistry of the mRNA-tRNA codon-anticodon interaction is monitored by components of the small ribosomal subunit in a process known as decoding (reviewed in ref. 1). During decoding, the first and second nucleotide positions (in terms of the codon) of the mRNA-tRNA duplex are closely monitored, whereas interaction at the third or wobble position is less strictly recognized. Consistently, the misincorporation of the wrong amino acids into polypeptide chains usually occurs through the binding of nearcognate aminoacyl-tRNAs, i.e., those tRNAs carrying an anticodon similar to that of the cognate aminoacyl-tRNA, rather than noncognate aminoacyl-tRNAs, which carry dissimilar anticodons. Nascent polypeptide chains are surprisingly tolerant to misincorporation, with only one in Ϸ400 misincorporations being deleterious for the protein's activity (reviewed in ref.2). The reason for this is that usually near-cognate aminoacyl-tRNAs are selected instead of the cognate aminoacyl-tRNA, and the genetic code lexicon is organized in such a way that near-cognate tRNAs bear amino acids that are chemically similar to those carried by the cognate tRNA. For example, the misincorporation of an aspartate (codon: GAU/C) by near-cognate Asp-tRNA, instead of glutamate (GAA/G) by the cognate Glu-tRNA, both incorporate acidic amino acids. The middle and, in most cases, the first position of a codon are almost never misread, even under error-inducing conditions such as high magnesiu...

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“…An increasing number of non-SD-led genes (Chang et al 2006), including genes encoding leaderless mRNA completely lacking a 59 untranslated region (UTR) (Janssen 1993;Janssen 1996, 1997;Tedin et al 1997;Grill et al 2000Grill et al , 2001Moll et al 2002; and references therein), continue to be identified. Leaderless mRNAs have been reported to follow a novel pathway of translation initiation involving 70S ribosomes (Balakin et al 1992;O'Donnell and Janssen 2002;Moll et al 2004;Udagawa et al 2004) or 30S subunits free of IF3, which is reported to discriminate against a 59-terminal start codon (Moll et al 1998;Tedin et al 1999;Grill et al 2000Grill et al , 2001.…”

Section: Introductionmentioning

confidence: 99%

Ribosomes bind leaderless mRNA in Escherichia coli through recognition of their 5′-terminal AUG

Brock

Pourshahian²,

Giliberti³

et al. 2008

RNA

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Leaderless mRNAs are translated in the absence of upstream signals that normally contribute to ribosome binding and translation efficiency. In order to identify ribosomal components that interact with leaderless mRNA, a fragment of leaderless cI mRNA from bacteriophage l, with a 4-thiouridine (4 S -U) substituted at the +2 position of the AUG start codon, was used to form cross-links to Escherichia coli ribosomes during binary (mRNA+ribosome) and ternary (mRNA+ribosome+initiator tRNA) complex formation. Ribosome binding assays (i.e., toeprints) demonstrated tRNA-dependent binding of leaderless mRNA to ribosomes; however, cross-links between the start codon and 30S subunit rRNA and r-proteins formed independent of initiator tRNA. Toeprints revealed that a leaderless mRNA's 59-AUG is required for stable binding. Furthermore, the addition of a 59-terminal AUG triplet to a random RNA fragment can make it both competent and competitive for ribosome binding, suggesting that a leaderless mRNA's start codon is a major feature for ribosome interaction. Cross-linking assays indicate that a subset of 30S subunit r-proteins, located at either end of the mRNA tunnel, contribute to tRNA-independent contacts and/or interactions with a leaderless mRNA's start codon. The interaction of leaderless mRNA with ribosomes may reveal features of mRNA binding and AUG recognition that are distinct from known signals but are important for translation initiation of all mRNAs.

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Analysis of SD sequences in completed microbial genomes: Non-SD-led genes are as common as SD-led genes

Cited by 105 publications

References 37 publications

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

Shine–Dalgarno interaction prevents incorporation of noncognate amino acids at the codon following the AUG

Ribosomes bind leaderless mRNA in Escherichia coli through recognition of their 5′-terminal AUG

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