Abstract: Simple Summary: A total of 37 mitochondrial genes appears in a certain arrangement in most insects, and the transcription of this conserved mitochondrial genome (mitogenome) has been well-studied in species like Drosophila melanogaster, Erthesina fullo and Coridius chinensis. However, transcription of the mitogenome with extensive gene rearrangement has rarely been studied. In this research, we sequenced the mitogenome and mitochondrial transcriptome of Sericothrips houjii (Thysanoptera: Thripidae: Sericothripinae). The mitogenome of S. houjii exhibited extensive gene rearrangement and contained two control regions (CRs) with sequence repeats. Compared to the insect mitogenome with a typical gene order, the mitogenomic feature, relative gene expression level, transcriptional model and post-transcriptional cleavage of S. houjii were quite different. Unlike other insects where ribosomal RNA (rRNA) is typically highly expressed, ND4/ND4L in S. houjii exhibits the highest expression. Both strands of this mitogenome were entirely transcribed and the bicistronic messenger RNA (mRNA) COI/ND3 was reported for the first time in insects. Our study provides new insights into the transcriptional and post-transcriptional regulation processes in the insect mitogenome with extensive gene rearrangement and duplicated CRs. 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 Sericothrips houjii to analyze. The mitogenome was 14,965 bp in length and included two CRs contains 140 bp repeats between COIII-trnN (CR1) and trnT-trnP (CR2). Unlike the putative ancestral arrangement of insects, S. houjii exhibited only six conserved gene blocks encompassing 14 genes (trnL2-COII, trnD-trnK, ND2-trnW, ATP8-ATP6, ND5-trnH-ND4-ND4L and trnV-lrRNA). A quantitative transcription map showed the gene with the highest relative expression in the mitogenome was ND4-ND4L. 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 lrRNA. The post-transcriptional cleavage processes followed the "tRNA punctuation" model. After the cleavage of transfer RNAs (tRNAs), COI and ND3 matured as bicistronic mRNA COI/ND3 due to the translocation of intervening tRNAs, and the 3′ untranslated region (UTR) remained in the mRNAs for COII, COIII, CYTB and ND5. Additionally, isoform RNAs of ND2, srRNA and lrRNA were identified. In summary, the relative mitochondrial gene expression levels, transcriptional model and post-transcriptional cleavage process of S. houjii are notably different from those insects with typical mitochondrial gene arrangements. In addition, the phylogenetic tree of Thripidae including S. houjii 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. [ABSTRACT FROM AUTHOR]
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