Abstract

BackgroundOrthoptera, the largest polyneopteran insect order, contains 2 suborders and 235 subfamilies. Orthoptera mitochondrial genomes (mitogenomes) follow the ancestral insect gene order, with the exception of a trnD-trnK rearrangement in Acridomorphs and rare tRNA inversions. A question still remains regarding whether a long thymine-nucleotide stretch (T-stretch) involved in the recognition of the replication origin exists in the control region (CR) of Orthoptera mitochondrial DNA (mtDNA). Herein, we completed the sequencing of whole mitogenomes of two congeners (Sinochlora longifissa and S. retrolateralis), which possess overlapping distribution areas. Additionally, we performed comparative mitogenomic analysis to depict evolutionary trends of Orthoptera mitogenomes.ResultsBoth Sinochlora mitogenomes possess 37 genes and one CR, a common gene orientation, normal structures of transfer RNA and ribosomal RNA genes, rather low A+T bias, and significant C skew in the majority strand (J-strand), resembling all the other sequenced ensiferans. Both mitogenomes are characterized by (1) a large size resulting from multiple copies of an approximately 175 bp GC-rich tandem repeat within CR; (2) a novel gene order (rrnS-trnI-trnM-nad2-CR-trnQ-trnW), compared to the ancestral order (rrnS-CR-trnI-trnQ-trnM-nad2-trnW); and (3) redundant trnS(UCN) pseudogenes located between trnS(UCN) and nad1. Multiple independent duplication events followed by random and/or non-random loss occurred during Sinochlora mtDNA evolution. The Orthoptera mtDNA recognition sequence of the replication origin may be one of two kinds: a long T-stretch situated in or adjacent to a possible stem-loop structure or a variant of a long T-stretch located within a potential stem-loop structure.ConclusionsThe unique Sinochlora mitogenomes reveal that the mtDNA architecture within Orthoptera is more variable than previously thought, enriching our knowledge on mitogenomic genetic diversities. The novel genome rearrangements shed light on mtDNA evolutionary patterns. The two kinds of recognition sequences of replication origin suggest that the regulatory sequences involved in the replication initiation process of mtDNA have diverged through Orthoptera evolution.

Highlights

  • Orthoptera, the largest polyneopteran insect order, contains 2 suborders and 235 subfamilies

  • Genome organization We sequenced the complete mitogenome of S. longifissa (18,133 bp) and the nearly complete mitogenome of S. retrolateralis (17,209 bp) with a partial control region (CR)

  • They are currently the largest Orthoptera mitogenomes on GenBank. Their large sizes are due to two large noncoding regions, i.e., the CR and one intergenic spacer (IGS) located between trnS(UCN) and nad1

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Summary

Introduction

Orthoptera, the largest polyneopteran insect order, contains 2 suborders and 235 subfamilies. Orthoptera mitochondrial genomes (mitogenomes) follow the ancestral insect gene order, with the exception of a trnD-trnK rearrangement in Acridomorphs and rare tRNA inversions. Insect mitogenomes are generally compact with few intergenic spacers and possess stable gene content and organization. They are usually about 16 kb in size and bear 13 protein-coding genes (PCGs), 2 ribosomal RNA genes (rRNAs), 22 transfer RNA genes (tRNAs), and one control region (CR) that includes replication and transcription origins [1]. Extensive studies have revealed that gene order rearrangement and size variation that results from the presence of tandem repeats (TRs) and other non-coding regions occur more often than previously expected. In spite of the large number of insect species, the limited availability of complete mitogenomic sequence data, including those of congeneric species, impedes a thorough understanding of the insect mitogenomes

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