The first A-to-I RNA editome of hemipteran species Coridius chinensis reveals overrepresented recoding and prevalent intron editing in early-diverging insects

Abstract

Background Metazoan adenosine-to-inosine (A-to-I) RNA editing resembles A-to-G mutation and increases proteomic diversity in a temporal-spatial manner, allowing organisms adapting to changeable environment. The RNA editomes in many major animal clades remain unexplored, hampering the understanding on the evolution and adaptation of this essential post-transcriptional modification. Methods We assembled the chromosome-level genome of Coridius chinensis belonging to Hemiptera, the fifth largest insect order where RNA editing has not been studied yet. We generated ten head RNA-Seq libraries with DNA-Seq from the matched individuals. Results We identified thousands of high-confidence RNA editing sites in C. chinensis. Overrepresentation of nonsynonymous editing was observed, but conserved recoding across different orders was very rare. Under cold stress, the global editing efficiency was down-regulated and the general transcriptional processes were shut down. Nevertheless, we found an interesting site with “conserved editing but non-conserved recoding” in potassium channel Shab which was significantly up-regulated in cold, serving as a candidate functional site in response to temperature stress. Conclusions RNA editing in C. chinensis largely recodes the proteome. The first RNA editome in Hemiptera indicates independent origin of beneficial recoding during insect evolution, which advances our understanding on the evolution, conservation, and adaptation of RNA editing.

Conserved A-to-I RNA editing with non-conserved recoding expands the candidates of functional editing sites

“…This conformational change might affect the dynamics of the potassium channel where larger diameter enables higher ion permeability. More amazingly, similar to our previous finding in C. chinensis that this recoding level elevated under cold stress [ 24 ], in Drosophila the editing level at this site was also anti-correlated with temperature [ 43 ]. Thus, the recoded Shab protein with putatively higher ion permeability represents the cold-specific isoform ( Figure 5b ).…”

“…Given sufficient time for selection, drift, and speciation, one might observe that an A-to-I editing event is conserved between two species, but it recodes different AAs in different species. Indeed, this is what we actually saw in gene Shab between Drosophila melanogaster and a hemipteran species Coridius chinensis ( Figure 1c ) [ 24 ]. Although only one case was found between the two species, we defined this case as ‘conserved editing with non-conserved recoding’.…”

“…Next, we used AlphaFold to construct the structures of the pre-editing and post-edited protein isoforms. In our previous study in C. chinensis , the Ser>Gly recoding in Shab did not seem to drastically change the protein structure, but since the assembly and annotation in C. chinensis was not as perfect as in model organisms, we reserve the possibility that the Shab protein function might be fine-tuned by this recoding event [ 24 ]. Here, we study the potential effect of Thr>Ala recoding in D. melanogaster Shab gene.…”

“…(b) The DNA mutation next to an existing RNA editing site leads to a different codon change by RNA editing. (c) The known case of conserved editing with non-conserved recoding between D. melanogaster (Diptera) and C. chinensis (Hemiptera) [ 24 ]. Codon alignment is shown.…”