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

- Adaptation of codon and amino acid use for translational functions in highly.
- 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.
- 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.
- 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.
- The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material.
- If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
- When optimal codons co- occur with a high count of iso-accepting tRNA gene copies in the genome, which reflects an organism’s tRNA abundance it suggests a history of selection favoring translational optimization .
- We recently found, for example, that some optimal co- dons of highly transcribed genes differed among males and females for the testis, ovaries, gonadectomized- males and gonadectomized females, which may suggest adaptation of codon use to local tRNA populations in the beetle Tribolium castaneum [20].
- In addition, a study in Drosophila melanogaster showed that certain codons were preferentially used in the testis (CAG (Gln), AAG (Lys), CCC (Pro), and CGU (Arg)) as compared to other tissues such as the midgut, ovaries, and salivary glands, a result that was taken as support for the existence of tissue-specific tRNA populations [38] (see also an ana- lysis of codon bias by [37.
- Similarly, non-optimal codons, defined as those codons that are least commonly used in highly transcribed genes (or sometimes defined as “rare” codons), particularly those non-optimal codons with few or no tRNAs in the cellular tRNA pool [20], may decelerate translation and thereby prevent riboso- mal jamming [26] and also allow proper co-translational protein folding .
- In this regard, wobble co- dons, and non-optimal codons with few matching tRNA gene copies in the genome, may have significant transla- tional roles, including roles in slowing translation..
- In the red flour beetle, we recently reported that some non-optimal codons have abundant matching tRNA genes in the genome [20], and these codons are concentrated in a subset of highly transcribed genes with specific, non-random, biological functions (e.g., olfactory or stress roles), which may together allow preferential translation of mRNAs of those particular genes [20]..
- of the biosynthetic costs of amino acid synthesis (size/.
- complexity score for each of 20 amino acids as quanti- fied by Dufton [58]) has shown that those amino acids with low costs tend to be more commonly used in genes with high transcription levels in the beetle T.
- In the present study, we rigorously assess codon and amino acid use in highly transcribed genes of G.
- For our study, codon and amino acid use in G.
- The male accessory glands were included for study, but were separated from the other male reproductive system elements to prevent overwhelming, or skewing, the types of transcripts detected in the former tissues [66].
- In the following sections, we first thoroughly describe the optimal codons identified in this cricket species at the organism-wide level, and within each of the individ- ual tissue types, and consider the relative role of selec- tion versus mutation in shaping the optimal codons..
- Subsequently, we evaluate the relationships between op- timal codons and non-optimal codons and their match- ing tRNA gene counts in the genome to ascertain plausible functional roles.
- We then consider the amino acid use and tRNA relationships in highly expressed genes of this taxon..
- As shown in Table 2, the 777 genes in the top 5% average expression category (organism- wide analysis) were enriched for ribosomal protein genes and had mitochondrial and protein folding functions..
- Thus, the present analysis using large-scale RNA-seq from nine divergent tissues (Add- itional file 1: Table S1) and using a complete annotated genome [67] support a strong preference for AT3 co- dons in the most highly transcribed genes of this cricket..
- Thus, for some amino acids there is mild variation in primary and secondary status among tissues of the AT3 codons, which may re- flect modest differences in the tRNA abundances among tissues [20, 38].
- However, the overall patterns suggest there is remarkably high consistency in the identity of AT3 optimal codons across diverse tissues in this taxon (Additional file 1: Table S2)..
- Amino acid Codon (DNA).
- bimaculatus gen- ome contains repetitive A and T rich non-coding DNA [67], including in the introns.
- (Continued) Amino acid Codon.
- The status categories are further described in the main text.
- thus suggesting that selection is also a signifi- cant force that shapes AT3 in the genome [8], a factor that may be particularly apt to influence AT3 in the most highly expressed genes..
- further supports the interpretation that selection sub- stantially shapes optimal codon use in the highly expressed genes of G.
- highly expressed genes (top 5% expression levels when averaged FPKM across all nine tissues).
- Thus, this suggests that genes linked to these fundamental sexual structures and functions are prone to elevated optimal codon use that could, in principle, be due to their essential roles in reproduction and fitness, and cost-efficient translation may be particularly beneficial in the contained haploid meiotic cells [20].
- that this may reflect the essential and fitness-related roles of genes involved in the insect female structures since they transport and house the male sex cells and seminal fluids after mating [89, 90], possibly making translational optimization more consequential to repro- ductive success for the female than male genes.
- These patterns are consistent with a hypothesis that selection for translational optimization has been higher for genes involved in the gonads and male accessory glands, than those from the nervous system..
- This pattern may be due to Hill-Robertson interference arising from adaptive evolution at linked amino acid sites in the males, dragging slightly deleterious codon mutations to fixation [37].
- However, we found an oppos- ite pattern in the mosquito Aedes aegypti where optimal codon use was higher in male than in female gonads [11].
- Moreover, the relatively low Fop observed in the brain (Fig.
- It is worth noting that the finding that the degree of optimal codon use is particularly pronounced for genes transcribed in the gonads in Fig.
- thought to be substantiated by associations between op- timal codon use in highly expressed genes and their matching tRNA gene copy numbers in the genome .
- Given this context, to allow a precise interpretation of the codon-tRNA relationships in Table 1, and given some variation in terminology in the literature, we explicitly describe the codons using their ΔRSCU status and their tRNA abundances as fol- lows: Opt-codon ↑ tRNAs are those optimal codons (ele- vated use in highly expressed genes) that have relatively high tRNA gene copy numbers.
- To assess the relationships between the codon use and tRNA gene numbers for each amino acid in Table 1, we first determined the number of tRNA genes per amino acid in the G.
- Seven of the 18 identified optimal codons in Table 1 had Opt-codon wobble status, and had no exact matching tRNAs in the genome.
- The inefficiency of wob- ble interactions between codons and tRNAs, including chemically modified wobble tRNAs (e.g., adenosine to inosine, I34) in the anticodon loop [70, 71] appears to act as a mechanism to decelerate translation as com- pared to codons with exact tRNA matches [45, 46].
- In this re- gard, our collective results suggest a hypothesis that wobble codons in highly transcribed genes may slow translation and effectively assist in the process of protein folding..
- of the codon per codon family) in the organism-wide data- set (Table 1), and for the genes with Top5 One-tissue status in the gonads (Additional file 1: Table S2), which had the largest N values of genes of any tissue type (Additional file 1: Table S2.
- For the gonads, we found that the top GO clusters for genes with elevated use of GAT that were expressed in the ovaries (with Top5 One-tissue sta- tus) and of TAT in the testes (with Top5 One-tissue status) were involved in mitosis and cell cycle functions (Add- itional file 1: Table S3).
- Taken together, our results are sug- gestive that the use of Opt-codon wobble codons in highly expressed cricket genes may act to slow translation as a means to regulate the level of cellular proteins, and to en- sure proper co-translational folding, particularly affecting genes involved in the cell cycle (Additional file 1: Table S3) and ribosomal and mitochondrial proteins (Table 2)..
- This suggests their in- frequent use in highly expressed genes may be due to the rarity or absence of matching tRNAs in the cellular tRNA pools.
- Moreover, these codons were not only non- optimal, and thus by definition are rare in highly tran- scribed genes, but their exact matching tRNAs were ab- sent in the genome, and thus require wobble tRNAs, a combination that would in theory make them especially prone to slowing down translation.
- Thus, the infre- quent use of those non-optimal codons in the highly expressed genes is not likely to be due to a role in slowing translation.
- This proposed mechanism of up-translation using non-optimal (or rare) codons has been recently suggested for stress genes in yeast [48], and for highly expressed genes in the red flour beetle, wherein genes with an elevated frequency of Nonopt-codon ↑ tRNAs.
- For each of these codons, we examined those Top5 One-tissue genes (only in the top 5% expression in one tissue type) in the gonads that had RSCU value ≥1.5, indicating enhanced use.
- santa-maria each had high use of all three of these Nonopt-codon ↑ tRNAs codons, which by definition have abundant matching tRNA genes, suggests their gene tran- scripts may be preferentially translated in the ovary as compared to other transcripts in the transcript pool.
- For CTG (Leu), the Top5 One-tissue genes in the ovaries prefer- entially using this codon with Nonopt-codon ↑ tRNAs status included another apoptosis gene, apoptosis inducing factor (AIF) [101], which also had elevated use of GGC for Gly, suggesting these codons may facilitate apoptosis in the fe- male gonad cells.
- With respect to the testis, GTG (Val) was preferentially used in genes such as belle, which is in- volved in male germ-line stem cell development and no child left behind (nclb), involved in male gonad development [104], suggesting that use of this non- optimal codon may promote translation of these particular transcripts in the male gonadal mRNA pools.
- Enhanced use of GGC and CTG in testes was found for genes matching Dual-specificity tyrosine phosphorylation- regulated kinase 2 (Dyrk2), which is involved in apoptosis and sensory roles and short spindle 3 (ssp3), in- volved in male meiosis [107] (Table 3), infers that these two codons may promote translation of apoptosis and meiotic proteins in the testes.
- Next, we asked whether amino acid use in the highly expressed genes in G.
- Table 3 Examples of genes that exhibit the top 5% expression levels in the ovaries and top 5% expression levels in the testes (but are not in the top 5% of any other tissue type, Top5 One-tissue ) in G.
- S1), but the correlation was stronger in the subset of highly expressed genes, suggesting that the connection between amino acid use and S/C scores is ameliorated with elevated transcription.
- We note this is consistent with an earlier analysis based on a partial transcriptome from one pooled ovary/embryo sample and without tRNA data in that study, where amino acids with intermediate S/C scores Glu, Asp, and Table 3 Examples of genes that exhibit the top 5% expression levels in the ovaries and top 5% expression levels in the testes (but are not in the top 5% of any other tissue type, Top5 One-tissue ) in G.
- Indeed, the S/C scores of the 20 amino acids showed a tendency to be inversely connected to the total tRNA counts per amino acid in the organism-wide.
- 3 The relationship between amino acid properties and amino acid use (percent per gene, averaged across genes) in the organism- wide highly expressed genes.
- Thus, the abundance of tRNAs in the genome is directly connected to how biochemically costly an amino acid is to produce by the organism.
- We therefore suggest the hypothesis that all three parameters, amino acid frequency, tRNA genes in the genome, and biochemical costs, have evolved interdependently for translational optimization in G.
- 4) and with amino acid frequency (Table 4).
- Variation in amino acid use with respect to sex and tissue type.
- For each sex, we found strong correlations in the frequency of amino acid use (across 20 amino acids) for all paired contrasts of tissues, with Spearman R values between 0.861 and 0.98 Table 4 The average amino acid use of the top 5% expressed genes (Top5 One-tissue ) in G.
- The number of predicted tRNAs in the genome per amino acid are shown.
- Amino acid (AA) S/C Score AA Freq.
- All P values for t-tests in the table withstand Bonferroni correction (P <.
- This suggests the relative amino acid use is largely consistent among highly expressed genes from all tissue types.
- 4 The predicted gene counts of tRNAs in the G.
- bimaculatus, and we do not exclude a role of BGC in the variation in GC/AT content among genes, the collective patterns are consist- ent with the hypothesis that translational selection sig- nificantly contributes to optimal codon use under high transcription.
- Accordingly, to identify optimal codons for each tissue type, we exam- ined those genes that were in the top 5% expression in that one tissue type and not in the top 5% expression for any of the remaining eight tissues (denoted as Top5 One-- tissue ) versus those with the lowest 5% expression (or all those tied with the FPKM cutoff of the lowest 5% [20])..
- Using these subsets of highly and lowly expressed genes within each tissue, the ΔRSCU was determined for each tissue type in the same manner described for the organism-wide optimal codons..
- Fop was then compared for genes with high tran- scription in the various tissue types in G.
- The number of tRNA genes per amino acid in the G..
- amino acid costs and amino acid frequency (see Discussion)..
- The filter acted to reduce the absolute counts of tRNAs per amino acid in the high confidence dataset.
- Amino acid use.
- Top5 One-tissue : genes with an expression level in the top 5% in one tissue type only, and not in the other studied tissues.
- Rapid evolution of ovarian-biased genes in the yellow fever mosquito (Aedes aegypti).
- tRNA gene number and codon usage in the C.
- Genome-wide selection on codon usage at the population level in the fungal model organism Neurospora crassa..
- Gene expression levels are correlated with synonymous codon usage, amino acid composition, and gene architecture in the red flour beetle, Tribolium castaneum.
- Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees.
- Brain control of mating behavior in the male cricket Gryllus bimaculatus DeGeer: brain neurons responsible for inhibition of copulation actions.
- Reproductive Behavior and Physiology in the Cricket Gryllus bimaculatus.
- Behavioural integration of auditory and antennal stimulation during phonotaxis in the field cricket Gryllus bimaculatus.
- Expression-linked patterns of codon usage, amino acid frequency, and protein length in the basally branching arthropod Parasteatoda tepidariorum.
- The transcriptional repressor Blimp-1 acts downstream of BMP signaling to generate primordial germ cells in the cricket Gryllus bimaculatus.
- Sex-biased genes expressed in the cricket brain evolve rapidly.
- Variation in the strength of selected codon usage bias among bacteria.
- Transcription-induced mutations: increase in C to T mutations in the nontranscribed strand during transcription in Escherichia coli.
- Belle is a Drosophila DEAD-box protein required for viability and in the germ line..
- Drosophila Dyrk2 plays a role in the development of the visual system.
- Trends of amino acid usage in the proteins from the human genome.
- Extreme recombination frequencies shape genome variation and evolution in the honeybee, Apis mellifera.
- Delta/notch signalling is not required for segment generation in the basally branching insect Gryllus bimaculatus.
- Mutation bias is the driving force of codon usage in the Gallus gallus genome

Xem thử không khả dụng, vui lòng xem tại trang nguồn
hoặc xem Tóm tắt