Full-Length Transcriptome Profiling of the Complete Mitochondrial Genome of Sericothrips houjii (Thysanoptera: Thripidae: Sericothripinae) Featuring Extensive Gene Rearrangement and Duplicated Control Regions

The mitochondrial genome (mitogenome) of Thysanoptera has extensive gene rearrangement, and some species have repeatable control regions. To investigate the characteristics of the gene expression, transcription and post-transcriptional processes in such extensively gene-rearranged mitogenomes, we sequenced the mitogenome and mitochondrial transcriptome of <i>Sericothrips houjii</i> to analyze. The mitogenome was 14,965 bp in length and included two CRs contains 140 bp repeats between <i>COIII-trnN</i> (CR1) and <i>trnT-trnP</i> (CR2). Unlike the putative ancestral arrangement of insects, <i>S. houjii</i> exhibited only six conserved gene blocks encompassing 14 genes (<i>trnL2-COII</i>, <i>trnD-trnK</i>, <i>ND2-trnW</i>, <i>ATP8-ATP6</i>, <i>ND5-trnH-ND4-ND4L</i> and <i>trnV-lrRNA</i>). A quantitative transcription map showed the gene with the highest relative expression in the mitogenome was <i>ND4-ND4L</i>. Based on analyses of polycistronic transcripts, non-coding RNAs (ncRNAs) and antisense transcripts, we proposed a transcriptional model of this mitogenome. Both CRs contained the transcription initiation sites (TISs) and transcription termination sites (TTSs) of both strands, and an additional TIS for the majority strand (J-strand) was found within antisense <i>lrRNA</i>. The post-transcriptional cleavage processes followed the "tRNA punctuation" model. After the cleavage of transfer RNAs (tRNAs), <i>COI</i> and <i>ND3</i> matured as bicistronic mRNA <i>COI/ND3</i> due to the translocation of intervening tRNAs, and the 3' untranslated region (UTR) remained in the mRNAs for <i>COII, COIII, CYTB</i> and <i>ND5</i>. Additionally, isoform RNAs of <i>ND2</i>, <i>srRNA</i> and <i>lrRNA</i> were identified. In summary, the relative mitochondrial gene expression levels, transcriptional model and post-transcriptional cleavage process of <i>S. houjii</i> are notably different from those insects with typical mitochondrial gene arrangements. In addition, the phylogenetic tree of Thripidae including <i>S. houjii</i> was reconstructed. Our study provides insights into the phylogenetic status of Sericothripinae and the transcriptional and post-transcriptional regulation processes of extensively gene-rearranged insect mitogenomes.