Full-length transcriptome profiling of Aphidius gifuensis mitochondrial genome with gene rearrangement and control region duplication

Xinjie Zhao; Shiwen Xu; Jingrui Li; Hailin Yang; Li Tian; Fan Song; Wanzhi Cai; Zhonglong Lin; Hu Li

doi:10.1016/j.heliyon.2023.e17070

Full-length transcriptome profiling of Aphidius gifuensis mitochondrial genome with gene rearrangement and control region duplication

Heliyon. 2023 Jun 8;9(6):e17070. doi: 10.1016/j.heliyon.2023.e17070. eCollection 2023 Jun.

Authors

Xinjie Zhao¹, Shiwen Xu¹, Jingrui Li², Hailin Yang³, Li Tian¹, Fan Song¹, Wanzhi Cai¹, Zhonglong Lin⁴, Hu Li¹

Affiliations

¹ Department of Entomology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, 100193, China.
² State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100193, China.
³ Yuxi Branch of Yunnan Tobacco Company, Yuxi, 653100, China.
⁴ Yunnan Tobacco Company of China National Tobacco Corporation, Kunming, 650011, China.

Abstract

Although mitochondrial gene rearrangement has been observed in many insect lineages, little is known about how it affects mitochondrial gene transcription. To address this question, we first constructed a quantitative transcription map for Aphidius gifuensis, a species of parasitoid wasp known to have a highly rearranged mitochondrial genome (mitogenome) and two potential control regions (CRs). Based on this transcription map, we assessed the models of the mitochondrial transcription and post-transcription cleavage. We found that the J and N strand of this mitogenome differ significantly in transcriptional regulation. On the J strand, we found two transcription initiation sites (TISs), five transcription termination sites (TTSs), and six polycistronic primary transcripts whereas only one TIS, one TTS and one polycistronic primary transcript can be found on the N strand. Most of the non-coding regions of both strands were transcribed into primary transcripts and cleaved after transcription. The proposed mode of transcription of A. gifuensis was similar to that of Drosophila, a model organism with no gene rearrangement. And two rearranged gene clusters (trnI-CR1-trnM-CR2-trnQ and trnW-trnY-trnC) seemed to have little effects on the mode of transcription. In addition, our results revealed the presence of TISs in CR1 and CR2, implying that both CRs maybe required for transcriptional regulation. Analysis of the post-transcriptional cleavage process showed that there were both "forward cleavage" and "reverse cleavage" models in A. gifuensis, and more than one way of cleavages were found in three regions. The incomplete transcripts suggested that the direction of mitochondrial RNA degradation was from 5' to 3' end and supported the view of polyadenylation-dependent RNA degradation. Our study provides insights into the transcriptional and post-transcriptional regulation processes of highly rearranged insect mitogenomes.

Keywords: Aphidius gifuensis; Mitochondrial gene transcription; Post-transcriptional cleavage process; full-length transcriptome.