Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes

Background For multicellular organisms, much remains unknown about the dynamics of synonymous codon and amino acid use in highly expressed genes, including whether their use varies with expression in different tissue types and sexes. Moreover, specific codons and amino acids may have translational functions in highly transcribed genes, that largely depend on their relationships to tRNA gene copies in the genome. However, these relationships and putative functions are poorly understood, particularly in multicellular systems. Results Here, we studied codon and amino acid use in highly expressed genes from reproductive and nervous system tissues (male and female gonad, somatic reproductive system, brain and ventral nerve cord, and male accessory glands) in the cricket Gryllus bimaculatus. We report an optimal codon, defined as the codon preferentially used in highly expressed genes, for each of the 18 amino acids with synonymous codons in this organism. The optimal codons were mostly shared among tissue types and both sexes. However, the frequency of optimal codons was highest in gonadal genes. Concordant with translational selection, a majority of the optimal codons had abundant matching tRNA gene copies in the genome, but sometimes obligately required wobble tRNAs. We suggest the latter may comprise a mechanism for slowing translation of abundant transcripts, particularly for cell-cycle genes. Non-optimal codons, defined as those least commonly used in highly transcribed genes, intriguingly often had abundant tRNAs, and had elevated use in a subset of genes with specialized functions (gametic and apoptosis genes), suggesting their use promotes the translational upregulation of particular mRNAs. In terms of amino acids, we found evidence suggesting that amino acid frequency, tRNA gene copy number, and amino acid biosynthetic costs (size/complexity) had all interdependently evolved in this insect model, potentially for translational optimization. Conclusions Collectively, the results suggest a model whereby codon use in highly expressed genes, including optimal, wobble, and non-optimal codons, and their tRNA abundances, as well as amino acid use, have been influenced by adaptation for various functional roles in translation within this cricket. The effects of expression in different tissue types and the two sexes are discussed.

Evolution of the genetic code; Evidence from serine codon use disparity inEscherichia coli

Among the 20 amino acids, three of them—leucine (Leu), arginine (Arg), and serine (Ser)—are encoded by six different codons. In comparison, all of the other 17 amino acids are encoded by either 4, 3, 2, or 1 codon. Peculiarly, Ser is separated into two disparate Ser codon boxes, differing by at least two-base substitutions, in contrast to Leu and Arg, of which codons are mutually exchangeable by a single-base substitution. We propose that these two different Ser codons independently emerged during evolution. In this hypothesis, at the time of the origin of life there were only seven primordial amino acids: Valine (coded by GUX [X = U, C, A or G]), alanine (coded by GCX), aspartic acid (coded by GAY [Y = U or C]), glutamic acid (coded by GAZ [Z = A or G]), glycine (coded by GGX), Ser (coded by AGY), and Arg (coded by CGX and AGZ). All of these were derived from GGX for glycine by single-base substitutions. Later in evolution, another class of Ser codons, UCX, were derived from alanine codons, GCX, distinctly different from the other primordial Ser codon, AGY. From the analysis of theEscherichia coligenome, we find extensive disparities in the usage of these two Ser codons, as some genes use only AGY for Ser in their genes. In contrast, others use only UCX, pointing to distinct differences in their origins, consistent with our hypothesis.

Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes

BackgroundFor multicellular organisms, much remains unknown about the dynamics of synonymous codon and amino acid use in highly expressed genes, including whether their use varies with expression in different tissue types and sexes. Moreover, specific codons and amino acids may have translational functions in highly transcribed genes, that largely depend on their relationships to tRNA gene copies in the genome. However, these relationships and putative functions are poorly understood, particularly in multicellular systems.ResultsHere, we rigorously studied codon and amino acid use in highly expressed genes from reproductive and nervous system tissues (male and female gonad, somatic reproductive system, brain, ventral nerve cord, and male accessory glands) in the cricket Gryllus bimaculatus. We report an optimal codon, defined as the codon preferentially used in highly expressed genes, for each of the 18 amino acids with synonymous codons in this organism. The optimal codons were largely shaped by selection, and their identities were mostly shared among tissue types and both sexes. However, the frequency of optimal codons was highest in gonadal genes. Concordant with translational selection, a majority of the optimal codons had abundant matching tRNA gene copies in the genome, but sometimes obligately required wobble tRNAs. We suggest the latter may comprise a mechanism for slowing translation of abundant transcripts, particularly for cell-cycle genes. Non-optimal codons, defined as those least commonly used in highly transcribed genes, intriguingly often had abundant tRNAs, and had elevated use in a subset of genes with specialized functions (gametic and apoptosis genes), suggesting their use promotes the upregulation of particular mRNAs. In terms of amino acids, we found evidence suggesting that amino acid frequency, tRNA gene copy number, and amino acid biosynthetic costs (size/complexity) had all interdependently evolved in this insect model, potentially for translational optimization.ConclusionsCollectively, the results strongly suggest that codon use in highly expressed genes, including optimal, wobble, and non-optimal codons, and their tRNAs abundances, as well as amino acid use, have been adapted for various functional roles in translation within this cricket. The effects of expression in different tissue types and the two sexes are discussed.

Phylogenomics of Ichneumonoidea (Hymenoptera) and implications for evolution of mode of parasitism and viral endogenization

Ichneumonoidea is one of the most diverse lineages of animals on the planet with more than 48,000 described species and many more undescribed. Parasitoid wasps of this superfamily are beneficial insects that attack and kill other arthropods and are important for understanding diversification and the evolution of life history strategies related to parasitoidism. Further, some lineages of parasitoids within Ichneumonoidea have acquired endogenous virus elements (EVEs) that are permanently a part of the wasp’s genome and benefit the wasp through host immune disruption and behavioral control. Unfortunately, understanding the evolution of viral acquisition, parasitism strategies, diversification, and host immune disruption mechanisms, is deeply limited by the lack of a robust phylogenetic framework for Ichneumonoidea. Here we design probes targeting 541 genes across 91 taxa to test phylogenetic relationships, the evolution of parasitoid strategies, and the utility of probes to capture polydnavirus genes across a diverse array of taxa. Phylogenetic relationships among Ichneumonoidea were largely well resolved with most higher-level relationships maximally supported. We noted codon use biases between the outgroups, Braconidae, and Ichneumonidae and within Pimplinae, which were largely solved through analyses of amino acids rather than nucleotide data. These biases may impact phylogenetic reconstruction and caution for outgroup selection is recommended. Ancestral state reconstructions were variable for Braconidae across analyses, but consistent for reconstruction of idiobiosis/koinobiosis in Ichneumonidae. The data suggest many transitions between parasitoid life history traits across the whole superfamily. The two subfamilies within Ichneumonidae that have polydnaviruses are supported as distantly related, providing strong evidence for two independent acquisitions of ichnoviruses. Polydnavirus capture using our designed probes was only partially successful and suggests that more targeted approaches would be needed for this strategy to be effective for surveying taxa for these viral genes. In total, these data provide a robust framework for the evolution of Ichneumonoidea.

Selection shapes synonymous stop codon use in mammals

Phylogenetic models of the evolution of protein-coding sequences can provide insights into the selection pressures that have shaped them. In the application of these models synonymous nucleotide substitutions, which do not alter the encoded amino acid, are often assumed to have limited functional consequences and used as a proxy for the neutral rate of evolution. The ratio of nonsynonymous to synonymous substitution rates is then used to categorize the selective regime that applies to the protein (e.g. purifying selection, neutral evolution, diversifying selection). Here, we extend the Muse \& Gaut model of codon evolution to explore the extent of purifying selection acting on substitutions between synonymous stop codons. Using a large collection of coding sequence alignments we estimate that a high proportion (approximately 57%) of mammalian genes are affected by selection acting on stop codon preference. This proportion varies substantially by codon, with UGA stop codons far more likely to be conserved. Genes with evidence of selection acting on synonymous stop codons have distinctive characteristics, compared to unconserved genes with the same stop codon, including longer 3' UTRs and shorter mRNA half-life. The coding regions of these genes are also much more likely to be under strong purifying selection pressure. Our results suggest that the preference for UGA stop codons found in many multicellular eukaryotes is selective rather than mutational in origin.

Evidence of multifaceted functions of codon usage in translation within the model beetle Tribolium castaneum

Synonymous codon use is non-random. Codons most used in highly transcribed genes, often called optimal codons, typically have high gene counts of matching tRNA genes (tRNA abundance) and promote accurate and/or efficient translation. Non-optimal codons, those least used in highly expressed genes, may also affect translation. In multicellular organisms, codon optimality may vary among tissues. At present, however, tissue specificity of codon use remains poorly understood. Here, we studied codon usage of genes highly transcribed in germ line (testis and ovary) and somatic tissues (gonadectomized males and females) of the beetle Tribolium castaneum. The results demonstrate that: (i) the majority of optimal codons were organism-wide, the same in all tissues, and had numerous matching tRNA gene copies (Opt-codon↑tRNAs), consistent with translational selection; (ii) some optimal codons varied among tissues, suggesting tissue-specific tRNA populations; (iii) wobble tRNA were required for translation of certain optimal codons (Opt-codonwobble), possibly allowing precise translation and/or protein folding; and (iv) remarkably, some non-optimal codons had abundant tRNA genes (Nonopt-codon↑tRNAs), and genes using those codons were tightly linked to ribosomal and stress-response functions. Thus, Nonopt-codon↑tRNAs codons may regulate translation of specific genes. Together, the evidence suggests that codon use and tRNA genes regulate multiple translational processes in T. castaneum.

Evidence of multifaceted functions of codon usage in translation within the model beetle Tribolium castaneum

Synonymous codon use is non-random. Codons most used in highly transcribed genes, often called optimal codons, typically have high gene counts of matching tRNA genes (tRNA abundance) and promote accurate and/or efficient translation. Non-optimal codons, those least used in highly expressed genes, may also affect translation. In multicellular organisms, codon optimality may vary among tissues. At present however, codon use remains poorly understood in multicellular organisms. Here, we studied codon usage of genes highly transcribed in germ line (testis, ovary) and somatic tissues (gonadectomized males and females) of the beetle Tribolium castaneum. The results demonstrate that: 1) the majority of optimal codons were organism-wide, the same in all tissues, and had numerous matching tRNA gene copies (Opt-codon↑tRNAs), consistent with translational selection; 2) some optimal codons varied among tissues, suggesting tissue-specific tRNA populations; 3) wobble tRNA were required for translation of certain optimal codons (Opt-codonwobble), possibly allowing precise translation and/or protein folding; and 4) remarkably, some non-optimal codons had abundant tRNA genes (Nonopt-codon↑tRNAs), and genes using those codons were tightly linked to ribosomal and stress-response functions. Thus, Nonopt-codon↑tRNAs codons may regulate translation of specific genes. Together, the evidence suggests that codon use and tRNA genes regulate multiple translational processes in T. castaneum.

Collection of Mitochondrial tRNA Sequences and Anticodon Identification for Acheta domesticus

The mitochondria are organelles found within eukaryotic cell, possess own small circular DNA (mtDNA) apart from the most of DNA found in cell nucleus. The transcription and translation of mtDNA requires tRNA that often encoded by mtDNA itself. The mtDNA evolves faster than genomic DNA primary due to mitochondrial dysfunction and pathogenesis. The genes of mitochondria tRNA (mt tRNA) are prone to mutate that links to mitochondrial activity and protein synthesis machinery. It is important to understand the codon use by mt tRNA for Acheta domesticus to understand evolutionary relationship within closely related species and mitochondrial protein synthesis machinery. The present study uses the High throughput RNA sequencing data to identify mt tRNA genes using to examine the codon use for mitochondrial protein synthesis process. The conservative property of tRNA secondary structure assisted identified and confirmed anchored tRNA sequences with respective amino acid anticodon according to genetic code for tRNA in mtDNA. This study provides mt tRNA sequences to understand evolution of mitochondrial tRNA of Acheta domesticus with other related species to establish phylogeny. Moreover, mt tRNAs are the exons that provides partial sequences for mitochondria DNA. The novel approach for tRNA identification will guide other studies for PCR free in silico analysis.