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

Abstract

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.

Dissecting cricket genomes for the advancement of entomology and entomophagy

“…Studies on CpG depletion, considered a reliable indicator of DNA methylation, have revealed that DNA methylated genes tend to perform housekeeping functions across insects including holometabolous and hemimetabolous ones (Ylla et al 2021). In addition to the epigenomics described above, the genome and transcriptome in crickets have been used for studying the sex-biased gene expression regulation, which is linked to protein sequence evolution (Whittle et al 2021a) and the relationship between codon usage frequency and expression level in different tissues and sexes (Whittle et al 2021b).…”

oskaracts with the transcription factor Creb to regulate long-term memory in crickets

“…These were osk , Tdrd5 , Tdrd7 , limkain b1 , and an uncharacterized gene with annotation ID GBI_15344 (Supplementary File 2). In transcriptomes previously generated from the adult brain (55), we detected levels of all four non- oskar genes at levels at least as high as that detected for osk (Suppl. Figure S4, Suppl.…”

“…This search retrieved five genes (GBI_01840 “ oskar ”, GBI_13502 “ TDRD5/tejas ”, GBI_15344 “ uncharacterized ”, GBI_15604 “ limkain b1 ”, GBI_03370 “ TDRD7/tapas ”). We assessed expression of these genes in brains and gonads using previously published RNA-seq libraries (55) available at NCBI (PRJNA564136). We analyzed the RNA-seq data as in (16), including removing adapters and reads shorter than 20 nucleotides with Cutadapt v3.4 (65) and quantifying the gene expression in transcripts per million (TPM) with RSEM v1.2.29 (66), using STAR v2.7.0e1 (67) as read mapper against the G. bimaculatus genome (36) (Suppl.…”

Comparative analysis of transcriptomic data shows the effects of multiple evolutionary selection processes on codon usage in Marsupenaeus japonicus and Marsupenaeus pulchricaudatus

“…The FPKM of the S1|c21076_g1 and the S2|c17052_g1 sequences indicated low and high expression levels, respectively. Genes using the codons that are recognized by more abundant tRNA molecules may be translated more efficiently and with fewer mistakes than genes that use less frequent codons [ 54 , 55 ]. Nelson et al found that the high frequency of AGA/AGG codons present in the HCcAg and HU IFNa2 genes could be one of the factors limiting its expression in Escherichia coli [ 47 ].…”