Liu C et al. (2021), tRNA copy number and codon usage in the sea cuc...

ECB-ART-50700

Open Biol 2021 Nov 01;1111:210190. doi: 10.1098/rsob.210190.

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tRNA copy number and codon usage in the sea cucumber genome provide insights into adaptive translation for saponin biosynthesis.

Liu C , Yuan J , Zhang X , Jin S , Li F , Xiang J .

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Genomic tRNA copy numbers determine cytoplasmic tRNA abundances, which in turn influence translation efficiency, but the underlying mechanism is not well understood. Using the sea cucumber Apostichopus japonicus as a model, we combined genomic sequence, transcriptome expression and ecological food resource data to study its codon usage adaptation. The results showed that, unlike intragenic non-coding RNAs, transfer RNAs (tRNAs) tended to be transcribed independently. This may be attributed to their specific Pol III promoters that lack transcriptional regulation, which may underlie the correlation between genomic copy number and cytoplasmic abundance of tRNAs. Moreover, codon usage optimization was mostly restrained by a gene's amino acid sequence, which might be a compromise between functionality and translation efficiency for stress responses were highly optimized for most echinoderms, while enzymes for saponin biosynthesis (LAS, CYPs and UGTs) were especially optimized in sea cucumbers, which might promote saponin synthesis as a defence strategy. The genomic tRNA content of A. japonicus was positively correlated with amino acid content in its natural food particles, which should promote its efficiency in protein synthesis. We propose that coevolution between genomic tRNA content and codon usage of sea cucumbers facilitates their saponin synthesis and survival using food resources with low nutrient content.

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	Figure 1. . tRNA copy number in the A. japonicus genome. (a) Fraction of the different anticodons within each isoacceptor family. (b) tRNA copy numbers. (c) Distribution of non-coding RNAs according to their relation with protein-coding genes. (d) tRNAs are scarce in introns of coding genes in different deuterostomes. (SKO, Saccoglossus kowalevskii; DRE, Danio rerio; AJA, A. japonicus). (e) tRNA copy number in different Ambulacraria groups. (AJA, A. japonicus; APL, Acanthaster planci; SPU, Strongylocentrotus purpuratus; LVA, Lytechinus variegatus; PPA, Parastichopus parvimensis; PMI, Patiria miniata; SKO, S. kowalevskii).
	Figure 2. . Correlation between isoaccepting tRNA gene frequencies and synonymous codon usage in the transcriptome of A. japonicus. (a) Correlations computed by weighting codons according to mRNA expression level and using the Watson–Crick base pairing rules (U : A; A : U; C : G; G : C). Notice that codons deviating from correlation were those potentially applied to G : U wobble and ADAT modifications. (b) Increased correlation after correction according to G : U wobble and ADAT modifications. (c) Weighting codons according to mRNA expression level increased the correlation only slightly. (d) Genes with the highest and lowest expression levels showed similar correlation levels between isoaccepting tRNA frequencies and synonymous codon usage.
	Figure 3. . Relationships between synonymous codons and isoaccepting tRNAs suggested the existence of G : U wobbling and ADAT activity. Calculation of anticodon frequency (TFij) and transcriptome codon frequency (TCFij) can be found in the Methods. The loss of anticodons for which mRNA codons are abundant is shown in red. The alternative matches enabled by tRNA wobble are shown with arrows. Solid arrows indicate G : U wobble. Dashed arrows indicate pairing resulting from ADAT modifications. Data used in this figure can be found in electronic supplementary material, table S1.
	Figure 4. . Correlation between genomic tRNA frequency and transcriptome amino acid frequency of A. japonicus. (a) Weighting amino acid frequency according to average mRNA expression level increased the correlation only slightly. (b) Genes with the highest and lowest expression levels showed similar correlation patterns between tRNA gene frequency and amino acid frequency.
	Figure 5. . Co-adaption between tRNA gene frequency and codon usage at the synonymous codon level and the amino acid level of individual genes of A. japonicus. CSI: coefficient of synonymous codon usage to isoaccepting tRNA frequency; TAAI: tRNA gene copy number and amino acid usage accordance index [17]; stAI: tRNA adaptation index [18]. Data used in this figure can be found in electronic supplementary material, dataset S2. (a) Positive coefficients were observed for the majority of genes between codon usage and genomic tRNA content at the synonymous codon level (CSI), amino acid level (TAAI) and overall level (stAI). (b) The difference in adaptation in amino acid usage (TAAI) contributed the majority of the differences in overall adaptation of codon usage (stAI). (c) mRNA abundance was calculated as the average FPKM (fragments per kilobase per million mapped fragments) using transcriptome data from whole-body samples at 45 days, 75 days and nine months of age. mRNA abundance did not show a clear influence on codon usage adaptation. (d) Gene length has significant influences on codon usage adaptation.
	Figure 6. . Correlation between TAAI, stAI and mRNA length in different deuterostomes. Data used in this figure can be found in electronic supplementary material, dataset S3. (a) A positive correlation was observed between TAAI (codon usage adaptation at the amino acid level) and stAI (overall codon usage adaptation level) for different deuterostomes. (b) The influence of gene length on codon usage adaptation is consistent among most deuterostomes.
	Figure 7. . Enzymes in the saponin biosynthesis pathway of A. japonicus co-adapted with genomic tRNA content for efficient translation. Relative TAAI is calculated as the ranking of a gene's TAAI among all genes in the species. (a) Co-adaptation between amino acid usage in the metabolic pathway and genomic tRNA contents. The section for terpenoid backbone biosynthesis is encircled with a dashed line. A larger version of the figure can be found in electronic supplementary material, figure S3. (b) Translation adaptation in the pathway of terpenoid backbone biosynthesis and the downstream pathway of steroid biosynthesis. (AJA, A. japonicus; APL, A. planci; BFL, Branchiostoma floridae; CIN, Ciona intestinalis; HSA, Homo sapiens; PPA, P. parvimensis; SKO, S. kowalevskii; SPU, S. purpuratus). (c) Translation adaptation in sea cucumber-specific cytochrome P450 (CYP) gene families and their closest homologues. (d) Translation adaptation in sea cucumber-specific UDP-glycosyltransferase (UGT) genes and their closest homologues. Sequences of the CYPs and UGTs can be found in electronic supplementary material, dataset S4. (e) Comparison of translation adaptation in genes involved in saponin biosynthesis between sea cucumbers and other animal groups (two-tailed t-test for unequal variances). (f) Summary of the saponin biosynthesis pathway in A. japonicus. The enzyme catalysing each reaction is represented by an arrow dyed in the colour gradient according to its relative TAAI. (g) Phylogenetic analysis of sea cucumber-specific cytochrome P450 gene families and their closest homologues. Sea cucumber genes are shown by red lines and labels. Differences in branch lengths indicate that the sea cucumber genes evolved much faster than their homologues in other animals. (h) Phylogenetic analysis of sea cucumber-specific UGT gene families and their closest homologues. Sea cucumber genes are shown in red.
	Figure 8. . Correlation between tRNA gene numbers of A. japonicus and amino acid content of particulate organic matter in seawater on the east coast of China near the Yangtze Estuary.
	Figure 9. . Comparison of co-adaptation between amino acid usage and genomic tRNA contents among gene categories across different deuterostomes. Relative TAAI (ranking of a gene's TAAI among all genes in the species) was averaged among genes in a GO category. Numbers in the heat map represent the number of gene families belonging to each GO category. (AJA, A. japonicus; APL, A. planci; BFL, B. floridae; CIN, C. intestinalis; HSA, H. sapiens; PMI, P. miniata; PPA, P. parvimensis; SPU, S. purpuratus).

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