Revelations from Comparative Mitochondrial Genome Analysis in Four Orders of Class Insecta

Authors

  • Manprit Kaur Department of Biotechnology, Chaudhary Bansi Lal University, Bhiwani 127021, Haryana
  • Arvind Sharma Department of Biochemistry and Molecular biology, University of Nevada, Reno
  • Neelam Sehrawat Department of Genetics, M D University, Rohtak 124001, Haryana
  • Surendra Gakhar Centre for Biotechnology, M.D. University, Rohtak 124001, Haryana
  • Ashwani Kumar Department of Biotechnology, Chaudhary Bansi Lal University, Bhiwani 127021, Haryana

DOI:

https://doi.org/10.55446/IJE.2024.1569

Keywords:

Mitochondrial genome, insects, gene order, nucleotide composition, PCGs, tRNAs, RNA secondary structures, A+T-rich region, gene rearrangement, AT-skew, GC-skew, Diptera, Lepidoptera, Orthoptera, Hemiptera

Abstract

The largest and most diverse group of organisms in the animal kingdom are insects. Molecular markers are powerful tools that can tackle a wide range of insect ecological research issues. These provide a more effective way to study the massive unexplored genetic diversity and gene pool of insects. Recent trends of use of DNA marker techniques in varied domains of insect ecological studies demonstrate that mitochondrial DNA has made a significant contribution towards advancing our knowledge of genetic basis of insect diversity. To shed light on various aspects such as genome organization, base composition, gene rearrangements, and other features, we integrated 165 mitochondrial genomes (mitogenomes) consisting of 37 genes and a noncoding control region, from four major insect orders (Diptera, Lepidoptera, Orthoptera and Hemiptera) for comparative genomic analysis. The same 37 genes were found in the majority of mitochondrial genomes, however the order of genes was found disturbed in a few mitochondrial genomes. The nucleotide composition was found strongly biased towards AT content. Usually, protein-coding genes prefer ATA, ATT and ATG as a canonical start codon. However, inconsistency was observed for few PCGs particularly for COI. The loss of DHU arm was found specific to trnS1 gene. In Zeugodacus tau (Pumpkin fruit fly), trnF gene lacked the TΨC arm. Majority of the mismatches (G-U (most common), U-U, U-C, A-A, A-C, A-G and T-T) were found within the acceptor arm, DHU arm and anticodon stem of tRNA genes but few in TΨC stem. Interestingly, a unique gene rearrangement from trnW (W codes for Tryptophan) to trnU (U codes for Selenocysteine) in the mitochondrial genome of Boettcherisca peregrine (Flesh fly) was observed. AT-rich control region remains highly variable among most of the insects. The review is aimed to draw conclusions for better interpretations of mitochondrial DNA evolution.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Downloads

Published

2024-04-05

How to Cite

Kaur, M., Sharma, A., Sehrawat, N., Gakhar, S., & Kumar, A. (2024). Revelations from Comparative Mitochondrial Genome Analysis in Four Orders of Class Insecta. Indian Journal of Entomology, 86(2), 649–662. https://doi.org/10.55446/IJE.2024.1569

Issue

Section

Review Articles

References

Ballard J W O. 2000. Comparative genomics of mitochondrial DNA in members of the Drosophila melanogaster subgroup. Journal of molecular evolution 51: 48-63.

Beckenbach A T, Joy J B. 2009. Evolution of the mitochondrial genomes of gall midges (Diptera: Cecidomyiidae): rearrangement and severe truncation of tRNA genes. Genome biology and evolution 1: 278-287.

Beckenbach A T. 2012. Mitochondrial genome sequences of Nematocera (lower Diptera): evidence of rearrangement following a complete genome duplication in a winter crane fly. Genome Biology and Evolution 4(2): 89-101.

Behura S K, Lobo N F, Haas B, DeBruyn B, Lovin D D, Shumway M F, Puiu D, Romero-Severson, J, Nene V, Severson D W. 2011. Complete sequences of mitochondria genomes of Aedes aegypti and Culex quinquefasciatus and comparative analysis of mitochondrial DNA fragments inserted in the nuclear genomes. Insect Biochemistry and Molecular Biology 41(10): 770-777.

Bian D, Dai M, Ye W, Lu Z, Li M, Fang Y, Qu J, Su W, Li F, Sun H, Li B. 2020. Complete mitochondrial genome of Spilosoma lubricipedum (Noctuoidea: Erebidae) and implications for phylogeny of noctuid insects. Genomics 112(6): 4577-4584.

Boore J L, Brown W M. 1998. Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Current Opinion in Genetics and Development 8(6): 668-674.

Boore J L. 1999. Animal mitochondrial genomes. Nucleic Acids Research 27(8): 1767-1780.

Buckley T R, Simon C, Flook P K, Misof B. 2000. Secondary structure and conserved motifs of the frequently sequenced domains IV and V of the insect mitochondrial large subunit rRNA gene. Insect Molecular Biology 9(6): 565-580.

Cameron S L, Whiting M F. 2008. The complete mitochondrial genome of the tobacco hornworm, Manduca sexta, (Insecta: Lepidoptera: Sphingidae), and an examination of mitochondrial gene variability within butterflies and moths. Gene 408(1-2): 112-123.

Cameron S L, 2014. Insect mitochondrial genomics: implications for evolution and phylogeny. Annual review of entomology 59: 95-117.

Cannone J J, Subramanian S, Schnare M N, Collett J R, D'Souza L M, Du Y, Feng B, Lin N, Madabusi L V, Müller K M and Pande N. 2002. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3: 1-31.

Chen J, Qiu D, Yue Q, Wang C, Li X. 2016 a. The complete mitochondria genome of Chrysomya phaonis (Seguy, 1928) (Diptera: Calliphoridae). Mitochondrial DNA Part B 1(1): 951-953.

Chen Y, Shi X, Li D, Chen B, Zhang P, Wu N, Xu Z. 2016b. The complete nucleotide sequence of the mitochondrial genome of Calliphora chinghaiensis (Diptera: Calliphoridae). Mitochondrial DNA Part B 1(1): 397-398.

Chen Y H, Huang D Y, Wang Y L, Zhu C D, Hao J S. 2014. The complete mitochondrial genome of the endangered Apollo butterfly, Parnassius apollo (Lepidoptera: Papilionidae) and its comparison to other Papilionidae species. Journal of Asia-Pacific Entomology 17(4): 663-671.

Cheng M, Liu Y, Zheng X, Zhang R, Feng K, Yue B, Du C, Zhou C. 2022. Characterization of Seventeen Complete Mitochondrial Genomes: Structural Features and Phylogenetic Implications of the Lepidopteran Insects. Insects 13(11): 998.

Chowdhury S, Dubey V K, Choudhury S, Das A, Jeengar D, Sujatha B, Kumar A, Kumar N, Semwal A, Kumar V. 2023. Insects as bioindicator: A hidden gem for environmental monitoring. Frontiers in Environmental Science 11: p.273.

Clary D O, Goddard J M, Martin S C, Fauron C M R, Wolstenholme D R. 1982. Drosophila mitochondrial DNA: a novel gene order. Nucleic Acids Research 10(21): 6619-6637.

Dai L S, Zhu B J, Liu Q N, Wei G Q, Liu C L. 2013. Characterization of the complete mitochondrial genome of Bombyx mori strain H9 (Lepidoptera: Bombycidae). Gene 519(2): 326-334.

Ding Y R, Li B, Zhang Y J, Mao Q M, Chen B. 2018. Complete mitogenome of Anopheles sinensis and mitochondrial insertion segments in the nuclear genomes of 19 mosquito species. PLoS One 13(9): p.e0204667.

Dong J J, Guan D L, Xu S Q. 2016. Complete mitogenome of the semiaquatic grasshopper Oxya intricate (Stal.) (Insecta: Orthoptera: Catantopidae). Mitochondrial DNA Part A 27(5): 3233-3234.

Dowton M, Cameron S L, Dowavic J I, Austin A D, Whiting M F. 2009. Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Molecular Biology and Evolution 26(7): 1607-1617.

Dowton M, Castro L R, Austin A D. 2002. Mitochondrial gene rearrangements as phylogenetic characters in the invertebrates: the examination of genome 'morphology'. Invertebrate Systematics 16(3): 345-356.

Du Z, Hasegawa H, Cooley J R, Simon C, Yoshimura J, Cai W, Sota T, Li H. 2019. Mitochondrial genomics reveals shared phylogeographic patterns and demographic history among three periodical cicada species groups. Molecular Biology and Evolution 36(6): 1187-1200.

Drosopoulou E, Syllas A, Goutakoli P, Zisiadis G A, Konstantinou T, Pangea D, Sentis G, Van Sauers-Muller A, Wee S L, Augustinos A A, Zacharopoulou A. 2019. The complete mitochondrial genome of Bactrocera carambolae (Diptera: Tephritidae): genome description and phylogenetic implications. Insects 10(12): 429.

Elameen A, Maduna S N, Mageroy M H, van Eerde A, Knudsen G, Hagen S B, Eiken H G. 2024. Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family Argyresthiidae. BMC Genomics 25(1): 21.

Elyasigorji Z, Izadpanah M, Hadi F, Zare M. 2023. Mitochondrial genes as strong molecular markers for species identification. The Nucleus 66(1): 81-93.

Evans N M, Shao S. 2022. Mycotoxin metabolism by edible insects. Toxins 14(3): 217.

Fei M, Gols R, Harvey J A. 2023. The biology and ecology of parasitoid wasps of predatory arthropods. Annual Review of Entomology 68: 109-128.

Fenn J D, Cameron S L, Whiting M F. 2007. The complete mitochondrial genome sequence of the Mormon cricket (Anabrus simplex: Tettigoniidae: Orthoptera) and an analysis of control region variability. Insect Molecular Biology 16(2): 239-252.

Flook P K, Rowell C H F. 1997. The effectiveness of mitochondrial rRNA gene sequences for the reconstruction of the phylogeny of an insect order (Orthoptera). Molecular Phylogenetics and Evolution 8(2): 177-192.

Fu X, Che K, Zhu Z, Liu J, Guo Y. 2016. The complete mitochondria genome of Sarcophaga africa (Diptera: Sarcophagidae). Mitochondrial DNA Part A 27(3): 2115-2116.

Gao S, Chen J J, Jiang G F. 2018. Complete mitochondrial genome of bamboo grasshopper, Ceracris fasciata, and the phylogenetic analyses and divergence time estimation of Caelifera (Orthoptera). Bulletin of Entomological Research 108(3): 321-336.

Garey J R, Wolstenholme D R. 1989. Platyhelminth mitochondrial DNA: Evidence for early evolutionary origin of a tRNA ser AGN that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. Journal of Molecular Evolution 28: 374-387.

Guo J, Xie K, Che K, Hu Z, Guo Y. 2016. The complete mitochondria genome of Ravinia pernix (Diptera: Sarcophagidae). Mitochondrial DNA Part A 27(3): 2069-2070.

Guo J, Yan Z T, Fu W B, Yuan H, Li X D, Chen B. 2021. Complete mitogenomes of Anopheles peditaeniatus and Anopheles nitidus and phylogenetic relationships within the genus Anopheles inferred from mitogenomes. Parasites and Vectors 14(1): 1-14.

Hao J, Sun Q, Zhao H, Sun X, Gai Y, Yang, Q. 2012. The complete mitochondrial genome of Ctenoptilum vasava (Lepidoptera: Hesperiidae: Pyrginae) and its phylogenetic implication. Comparative and Functional Genomics 2012.

Hao X, Liu J, Chiba H, Xiao J, Yuan X, 2021. Complete mitochondrial genomes of three skippers in the tribe Aeromachini (Lepidoptera: Hesperiidae: Hesperiinae) and their phylogenetic implications. Ecology and Evolution 11(12): 8381-8393.

Hardy C M, Court L N, Morgan M J, Webb C E. 2016. The complete mitochondrial DNA genomes for two lineages of Aedes notoscriptus (Diptera: Culicidae). Mitochondrial DNA Part A 27(3): 2024-2025.

Hassanin A, Leger N E L L Y, Deutsch J. 2005. Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. Systematic Biology 54(2): 277-298.

Hickson R E, Simon C, Cooper A, Spicer G S, Sullivan J, Penny D. 1996. Conserved sequence motifs, alignment, and secondary structure for the third domain of animal 12S rRNA. Molecular Biology and Evolution 13(1): 150-169.

Hong G, Jiang S, Yu M., Yang, Y, Li F, Xue F, Wei Z. 2009. The complete nucleotide sequence of the mitochondrial genome of the cabbage butterfly, Artogeia melete (Lepidoptera: Pieridae). Acta Biochim Biophys Sin 41(6): 446-455.

Hong M Y, Lee E M., Jo Y H, Park H C, Kim S R, Hwang J S, Jin B R, Kang P D, Kim K G, Han Y S, Kim I. 2008. Complete nucleotide sequence and organization of the mitogenome of the silk moth Caligula boisduvalii (Lepidoptera: Saturniidae) and comparison with other lepidopteran insects. Gene 413(1-2): 49-57.

Hou P, Gao S, Li X., Yang D, Zhang C. 2019. The mitochondrial genome of Janthicuomyia sp. (Diptera, Tachinidae). Mitochondrial DNA Part B 4(1): 1601-1602.

Hu P, Wang R. 2019. The complete mitochondrial genome of Parantica sita sita (Lepidoptera: Nymphalidae: Danainae) revealing substantial genetic divergence from its sibling subspecies P. s. niphonica. Gene 686: 76-84.

Hua J, Li M, Dong P, Cui Y, Xie Q, Bu W. 2008. Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics 9: 1-15.

Hua Y Q, Ding Y R, Yan Z T, Si F L, Luo Q C, Chen B. 2016. The complete mitochondrial genome of Anopheles minimus (Diptera: Culicidae) and the phylogenetics of known Anopheles mitogenomes. Insect Science 23(3): 353-365.

Huang J, Ma T. 2018. Comparative analysis of two mitochondrial genomes of flesh flies (Sarcophaga antilope and Sarcophaga dux) with phylogeny and evolutionary timescale for Sarcophagidae. International Journal of Biological Macromolecules 120: 1955-1964.

Ji L W, Hao J S, Wang Y, Huang D Y, Zhao J L, Zhu C D. 2012. The complete mitochondrial genome of the dragon swallowtail, Sericinus montela Gray (Lepidoptera: Papilionidae) and its phylogenetic implication. Acta Entomologica Sinica 55(1): 91-100.

Jiang F, Pan X, Li X, Yu Y, Zhang J, Jiang H, Dou L, Zhu S. 2016. The first complete mitochondrial genome of Dacus longicornis (Diptera: Tephritidae) using next-generation sequencing and mitochondrial genome phylogeny of Dacini tribe. Scientific Reports 6(1): 1-9.

Jiang S T, Hong G Y, Yu M, Li N, Yang Y, Liu Y Q, Wei Z J. 2009. Characterization of the complete mitochondrial genome of the giant silkworm moth, Eriogyna pyretorum (Lepidoptera: Saturniidae). International Journal of Biological Sciences 5(4): 351.

Junqueira A C M, Lessinger A C, Torres T T, Da Silva F R, Vettore A L, Arruda P, Espin A M L A. 2004. The mitochondrial genome of the blowfly Chrysomya chloropyga (Diptera: Calliphoridae). Gene 339: 7-15.

Kim I, Lee E M, Seol K Y, Yun E Y, Lee Y B, Hwang J S, Jin B R. 2006. The mitochondrial genome of the Korean hairstreak, Coreana raphaelis (Lepidoptera: Lycaenidae). Insect Molecular Biology 15(2): 217-225.

Kim S R, Kim M I, Hong M Y, Kim K Y, Kang P D, Hwang J S, Han Y S, Jin B R and Kim I. 2009. The complete mitogenome sequence of the Japanese oak silkmoth, Antheraea yamamai (Lepidoptera: Saturniidae). Molecular Biology Reports 36: 1871-1880.

Le Z, Gang L. 2020. The first complete mitochondrial genome of the tribe Rhingiini (Diptera: Syrphidae) and phylogenetic analysis. Mitochondrial DNA Part B 5(3): 3489-3491.

Lee E S, Shin K S, Kim M S, Park H, Cho S, Kim C B. 2006. The mitochondrial genome of the smaller tea tortrix Adoxophyes honmai (Lepidoptera: Tortricidae). Gene 373: 52-57.

Lee W, Kang J, Jung C, Hoelmer K, Lee S H, Lee S. 2009. Complete mitochondrial genome of brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae), and phylogenetic relationships of hemipteran suborders. Molecules and Cells 28: 155-165.

Lessinger A C, Martins Junqueira A C, Lemos T A, Kemper E L, Da Silva F R, Vettore A L, Arruda P L, Azeredo-Espin A M. 2000. The mitochondrial genome of the primary screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae). Insect Molecular Biology 9(5): 521-529.

Lewis O L, Farr C L, Kaguni L S. 1995. Drosophila melanogaster mitochondrial DNA: completion of the nucleotide sequence and evolutionary comparisons. Insect Molecular Biology 4(4): 263-278.

Li H, Liu H, Cao L., Shi A, Yang H, Cai W. 2012 a. The complete mitochondrial genome of the damsel bug Alloeorhynchus bakeri (Hemiptera: Nabidae). International Journal of Biological Sciences 8(1): p.93.

Li H, Liu H, Shi A, Stys P, Zhou X, Cai W. 2012 b. The complete mitochondrial genome and novel gene arrangement of the unique-headed bug Stenopirates sp. (Hemiptera: Enicocephalidae). PloS one 7(1): p.e29419.

Li J, Lv Q, Zhang X M, Han H L, Zhang A B. 2021. Characterization and Phylogenetic Analysis of the Complete Mitochondrial Genome of Laelia suffusa (Lepidoptera: Erebidae, Lymantriinae). Journal of Insect Science 21(1): p.5.

Li R, Shu X, Deng W A, Meng L, Li B, 2020 a. Complete mitochondrial genome of Atractomorpha sagittaris (Orthoptera: Pyrgomorphidae) and its phylogenetic analysis for Acrididea. Biologia 75: 1571-1583.

Li R, Shu X, Li X, Meng L, Li B. 2019. Comparative mitogenome analysis of three species and monophyletic inference of Catantopinae (Orthoptera: Acridoidea). Genomics 111(6): 1728-1735.

Li R, Wang Y, Shu X, Meng L, Li B. 2020 b. Complete mitochondrial genomes of three Oxya grasshoppers (Orthoptera) and their implications for phylogenetic reconstruction. Genomics 112(1): 289-296.

Li T, Gao C, Cui Y, Xie Q, Bu W. 2013. The complete mitochondrial genome of the stalk-eyed bug Chauliops fallax Scott, and the monophyly of Malcidae (Hemiptera: Heteroptera). PLoS One 8(2): p.e55381.

Liao F, Wang L, Wu S, Li Y P, Zhao L, Huang G M, Niu C J, Liu Y Q, Li M G. 2010. The complete mitochondrial genome of the fall webworm, Hyphantria cunea (Lepidoptera: Arctiidae). International Journal of Biological Sciences 6(2): 172.

Liu C, Chang J, Ma C, Li L, Zhou S. 2013 a. Mitochondrial genomes of two Sinochlora species (Orthoptera): novel genome rearrangements and recognition sequence of replication origin. BMC Genomics 14: 1-13.

Liu N, Huang Y. 2010. Complete mitochondrial genome sequence of Acrida cinerea (Acrididae: Orthoptera) and comparative analysis of mitochondrial genomes in Orthoptera. Comparative and Functional Genomics 2010.

Liu N, Fang L, Zhang Y. 2021. The complete mitochondrial genomes of four species in the subfamily limenitidinae (Lepidoptera, Nymphalidae) and a Phylogenetic Analysis. Insects 13(1): 16.

Liu Q N, Zhu B J, Dai L S, Liu C L. 2013 b. The complete mitogenome of Bombyx mori strain Dazao (Lepidoptera: Bombycidae) and comparison with other lepidopteran insects. Genomics 101(1): 64-73.

Liu W P, Zhang P Y, Xu S, Tang J X, Zhou H Y, Li J L, Wang D J, Liu Y Y, Fang Q, Xia H, Zhu G D. 2022. The complete mitochondrial genome of major malaria vector Anopheles anthropophagus (Diptera: Culicidae) in China. Mitochondrial DNA Part B 7(3): 482-484.

Liu Y, Xin Z Z, Zhu X Y, Zhao X M, Wang Y, Tang B P, Zhang H B, Zhang D Z, Zhou C L, Liu Q N. 2017. The complete mitochondrial genome of Euproctis similis (Lepidoptera: Noctuoidea: Erebidae) and phylogenetic analysis. International Journal of Biological Macromolecules 105: 219-227.

Lu C, Huang X, Deng J. 2023. Mitochondrial genomes of soft scales (Hemiptera: Coccidae): features, structures and significance. BMC Genomics 24(1): 1-14.

Luo Q C, Hao Y J, Meng F, Li T J, Ding Y R, Hua Y Q, Chen B. 2016. The mitochondrial genomes of Culex tritaeniorhynchus and Culex pipiens pallens (Diptera: Culicidae) and comparison analysis with two other Culex species. Parasites and vectors 9: 1-11.

Ma C, Liu C, Yang P, Kang L. 2009. The complete mitochondrial genomes of two band-winged grasshoppers, Gastrimargus marmoratus and Oedaleus asiaticus. BMC genomics 10(1): 1-12.

Ma T, Huang J. 2018. Characterization of the complete mitochondrial genome of Hydrotaea spinigera (Diptera: Muscidae) with phylogenetic implications. Journal of Asia-Pacific Entomology 21(4): 1416-1423.

Mancini E, De Biase A, Mariottini P, Bellini A, Audisio P. 2008. Structure and evolution of the mitochondrial control region of the pollen beetle Meligethes thalassophilus (Coleoptera: Nitidulidae). Genome 51(3): 196-207.

Manikandan S, Mathivanan A, Bora B, Hemaladkshmi P, Abhisubesh V, Poopathi S. 2023. A review on vector borne disease transmission: Current strategies of mosquito vector control. Indian Journal of Entomology pp.503-513.

Martinez-Villegas L, Assis-Geraldo J, Koerich L B, Collier T C, Lee Y, Main B J, Rodrigues N B, Orfano A S, Pires A C, Campolina T B, Nacif-Pimenta R. 2019. Characterization of the complete mitogenome of Anopheles aquasalis, and phylogenetic divergences among Anopheles from diverse geographic zones. PLoS One 14(9): p.e0219523.

Masta S E, Boore J L. 2004. The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Molecular Biology and Evolution 21(5): pp.893-902.

Matsumoto Y, Yanase T, Tsuda T, Noda H. 2009. Species-specific mitochondrial gene rearrangements in biting midges and vector species identification. Medical and Veterinary Entomology 23(1): 47-55.

Milián-García Y, Hempel C A, Janke L A, Young R G, Furukawa-Stoffer T, Ambagala A, Steinke D, Hanner, R H. 2022. Mitochondrial genome sequencing, mapping, and assembly benchmarking for Culicoides species (Diptera: Ceratopogonidae). BMC Genomics 23(1): 1-18.

Moreno M, Marinotti O, Krzywinski J, Tadei W P, James A A, Achee N L, Conn J E. 2010. Complete mtDNA genomes of Anopheles darlingi and an approach to anopheline divergence time. Malaria Journal 9(1): 1-13.

Morgan B, Wang T Y, Chen Y Z, Moctezuma V, Burgos O, Le M H, Huang J P. 2022. Long-read sequencing data reveals dynamic evolution of mitochondrial genome size and the phylogenetic utility of mitochondrial DNA in Hercules beetles (Dynastes; Scarabaeidae). Genome Biology and Evolution 14(10): evac147.

Nikolaou C, Almirantis Y. 2006. Deviations from Chargaff's second parity rule in organellar DNA: Insights into the evolution of organellar genomes. Gene 381: 34-41.

Pan M, Yu Q, Xia Y, Dai F, Liu Y, Lu C, Zhang Z, Xiang Z. 2008. Characterization of mitochondrial genome of Chinese wild mulberry silkworm, Bomyx mandarina (Lepidoptera: Bombycidae). Science in China Series C: Life Sciences 51(8): 693-701.

Park J S, Kim M J, Jeong S Y, Kim S S, Kim I. 2016. Complete mitochondrial genomes of two gelechioids, Mesophleps albilinella and Dichomeris ustalella (Lepidoptera: Gelechiidae), with a description of gene rearrangement in Lepidoptera. Current Genetics 62: 809-826.

Pei W, Xu W, Li H, Yan L, Gai Y, Yang N, Yang J, Chen J, Peng H, Pape T, Zhang D. 2024. Unusual rearrangements of mitogenomes in Diptera revealed by comparative analysis of 135 tachinid species (Insecta, Diptera, Tachinidae). International Journal of Biological Macromolecules 258: p.128997.

Perna N T, Kocher T D. 1995. Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution 41: 353-358.

Piacenza N, Kaltner F, Maul R, Gareis M, Schwaiger K, Gottschalk C. 2021. Distribution of T-2 toxin and HT-2 toxin during experimental feeding of yellow mealworm (Tenebrio molitor). Mycotoxin Research 37: 11-21.

Pons J, Bauza-Ribot M M, Jaume D, Juan C. 2014. Next-generation sequencing, phylogenetic signal and comparative mitogenomic analyses in Metacrangonyctidae (Amphipoda: Crustacea). BMC Genomics 15: 1-16.

Rokas A, Holland P W. 2000. Rare genomic changes as a tool for phylogenetics. Trends in Ecology & Evolution 15(11): 454-459.

Shi J, Guo Y, Zhang C, Zhou Y, Yan J, Liao H, Lagabaiyila Z. 2016. The complete mitochondrial genome of the flesh fly, Parasarcophaga portschinskyi (Diptera: Sarcophagidae). Mitochondrial DNA Part A, 27(3): 1910-1911.

Song N, Liang A. 2009. The complete mitochondrial genome sequence of Geisha distinctissima (Hemiptera: Flatidae) and comparison with other hemipteran insects. Acta Biochim Biophys Sin 41: 206-216.

Song S L, Yong H S, Suana I W, Lim P E. 2018. Complete mitochondrial genome of Bactrocera ritsemai (Insecta: Tephritidae) and phylogenetic relationship with its congeners and related tephritid taxa. Journal of Asia-Pacific Entomology 21(1): 252-257.

Song W, Li H U, Song F, Liu L I, Wang P, Xun H, Dai X, Chang J, Cai W. 2013. The complete mitochondrial genome of a tessaratomid bug, Eusthenes cupreus (Hemiptera: Heteroptera: Pentatomomorpha: Tessaratomidae). Zootaxa 3620(2): 260-272.

Stewart J B, Beckenbach A T. 2003. Phylogenetic and genomic analysis of the complete mitochondrial DNA sequence of the spotted asparagus beetle Crioceris duodecimpunctata. Molecular Phylogenetics and Evolution 26(3): 513-526.

Stewart J B, Beckenbach A T. 2009. Characterization of mature mitochondrial transcripts in Drosophila, and the implications for the tRNA punctuation model in arthropods. Gene 445(1-2): 49-57.

Su T, Liang A. 2018. Characterization of the complete mitochondrial genome of Phymatostetha huangshanensis (Hemiptera: Cercopidae) and phylogenetic analysis. International Journal of Biological Macromolecules 119: 60-69.

Sun Y X, Wang L, Wei G Q, Qian C, Dai L S, Sun Y, Abbas M N, Zhu B J, Liu C L. 2016. Characterization of the complete mitochondrial genome of Leucoma salicis (Lepidoptera: Lymantriidae) and comparison with other lepidopteran insects. Scientific Reports 6(1): p.39153.

Tang J, Huang W, Zhang Y. 2020. The complete mitochondrial genome of four Hylicinae (Hemiptera: Cicadellidae): Structural features and phylogenetic implications. Insects 11(12): p.869.

Tihelka E, Cai C, Giacomelli M, Lozano-Fernandez J, Rota-Stabelli O, Huang D, Engel M S, Donoghue P C, and Pisani D. 2021. The evolution of insect biodiversity. Current Biology 31(19): pp. R1299-R1311.

Thao M L, Baumann L, Baumann P. 2004. Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha). BMC Evolutionary Biology 4(1): 1-13.

Truman J W. 2019. The evolution of insect metamorphosis. Current Biology 29(23): pp. R1252-R1268.

Varani G, McClain W H. 2000. The G· U wobble base pair. EMBO Reports 1(1): 18-23.

Wang A, Du Z, Luo X, Zhang F, Zhang J, Li H. 2019. The conserved mitochondrial genomes of Drosophila mercatorum (Diptera: Drosophilidae) with different reproductive modes and phylogenetic implications. International Journal of Biological Macromolecules 138: 912-918.

Wang J, Dai R, Li H, Zhan H. 2017 a. Characterization of the complete mitochondrial genome of Japanagallia spinosa and Durgades nigropicta (Hemiptera: Cicadellidae: Megophthalminae). Biochemical Systematics and Ecology 74: 33-41.

Wang J, Li H, Dai R. 2017b. Complete mitochondrial genome of Taharana fasciana (Insecta, Hemiptera: Cicadellidae) and comparison with other Cicadellidae insects. Genetica 145(6): 593-602.

Wang K, Li X., Ding S, Wang N, Mao M, Wang M, Yang D. 2016. The complete mitochondrial genome of the Atylotus miser (Diptera: Tabanomorpha: Tabanidae), with mitochondrial genome phylogeny of lower Brachycera (Orthorrhapha). Gene 586(1): 184-196.

Wang Y, Huang X L, Qiao G X. 2013. Comparative analysis of mitochondrial genomes of five aphid species (Hemiptera: Aphididae) and phylogenetic implications. PLoS One 8(10): p.e77511.

Wang Y, Huang X L, Qiao G X. 2014. The complete mitochondrial genome of Cervaphis quercus (Insecta: Hemiptera: Aphididae: Greenideinae). Insect Science 21(3): 278-290.

Weigl S, Testini G, Parisi A, Dantas-Torres F, Traversa D, Colwell D D, Otranto D. 2010. The mitochondrial genome of the common cattle grub, Hypoderma lineatum. Medical and Veterinary Entomology 24(3): 329-335.

Wolstenholme D R. 1992. Animal mitochondrial DNA: structure and evolution. International Review of Cytology 141: 173-216.

Wu Y, Dai R, Zhan H, Qu L. 2016. Complete mitochondrial genome of Drabescoides nuchalis (Hemiptera: Cicadellidae). Mitochondrial DNA Part A 27(5): 3626-3627.

Xu Q, Hao Y, Mei K, Yin H, Zhang D. 2016. The complete mitochondrial genome of Ceracris versicolor (Orthoptera: Acridoidea: Arcypteridae). Mitochondrial DNA Part A 27(1): 512-513.

Yan J, Liao H, Zhu Z, Xie K, Guo Y, Cai J. 2016. The complete mitochondria genome of Parasarcophaga similis (Diptera: Sarcophagidae). Mitochondrial DNA Part A 27(3): 1642-1643.

Yang J, Huang X, Wang Y, Yang H, Zhang X, Zheng X. 2023. Complete mitochondrial genome of Penicillidia jenynsii (Diptera: Hippoboscoidea: Nycteribiidae) and phylogenetic relationship. Parasitology 150(7): 623-630.

Yang J, Ren Q, Huang Y. 2016 a. Complete mitochondrial genomes of three crickets (Orthoptera: Gryllidae) and comparative analyses within Ensifera mitogenomes. Zootaxa, 4092(4): 529-547.

Yang J, Ye F, Huang Y. 2016 b. Mitochondrial genomes of four katydids (Orthoptera: Phaneropteridae): New gene rearrangements and their phylogenetic implications. Gene 575(2): 702-711.

Yang L, Dai J, Gao Q, Yuan G, Liu J, Sun Y, Sun Y, Wang L, Qian C, Zhu B, Liu C. 2020. Characterization of the complete mitochondrial genome of Orthaga olivacea Warre (Lepidoptera Pyralidae) and comparison with other Lepidopteran insects. PLoS One 15(3): p.e0227831.

Yang L, Wei Z J, Hong G Y, Jiang S T, Wen L P. 2009. The complete nucleotide sequence of the mitochondrial genome of Phthonandria atrilineata (Lepidoptera: Geometridae). Molecular Biology Reports 36: 1441-1449.

Yang M, Song L, Shi Y, Yin Y, Wang Y, Zhang P, Chen J, Lou L, Liu X. 2019. The complete mitochondrial genome of a medicinal insect, Hydrillodes repugnalis (Lepidoptera: Noctuoidea: Erebidae), and related phylogenetic analysis. International Journal of Biological Macromolecules 123: 485-493.

Yang M R, Zhou Z J, Chang Y L, Zhao L H. 2012. The mitochondrial genome of the quiet-calling katydids, Xizicus fascipes (Orthoptera: Tettigoniidae: Meconematinae). Journal of Genetics 91: pp.141-153.

Ye H Y, Xiao L L, Zhou Z J, Huang Y. 2012. Complete mitochondrial genome of Locusta migratoria migratoria (Orthoptera: Oedipodidae): three tRNA-like sequences on the N-strand. Zoological Science 29(2): pp.90-96.

Yi J, Liu J, Mao Y, Cheng Y, Lin M, Xu H, An Y, Li J, Wu H. 2024. The complete mitochondrial genome of Chilo infuscatellus (Lepidoptera: Pyralidae), and related phylogenetic analysis. Biochemical Genetics. pp.1-16.

Yong H S, Song S L, Lim P E, Eamsobhana P. 2017. Complete mitochondrial genome of Zeugodacus tau (Insecta: Tephritidae) and differentiation of Z. tau species complex by mitochondrial cytochrome c oxidase subunit I gene. Plos one 12(12): p.e0189325.

Yu F, Liang A P. 2018. The complete mitochondrial genome of Ugyops sp. (Hemiptera: Delphacidae). Journal of Insect Science 18(3): 25.

Yuan M L, Zhang Q L, Guo Z L, Wang J, Shen Y Y, 2015 a. Comparative mitogenomic analysis of the superfamily Pentatomoidea (Insecta: Hemiptera: Heteroptera) and phylogenetic implications. BMC genomics 16(1): 1-16.

Yuan M L, Zhang Q L, Guo Z L, Wang J, Shen Y Y. 2015 b. The complete mitochondrial genome of Corizus tetraspilus (Hemiptera: Rhopalidae) and phylogenetic analysis of Pentatomomorpha. PLoS One 10(6): p.e0129003.

Yuan X, Li C, Song Y. 2020. Characterization of the complete mitochondrial genome of Mitjaevia protuberanta (Hemiptera: Cicadellidae: Typhlocybinae). Mitochondrial DNA Part B 5(1): 601-602.

Zhang D, Zhi Y, Yin H, Li X, Yin X. 2011. The complete mitochondrial genome of Thrinchus schrenkii (Orthoptera: Caelifera, Acridoidea, Pamphagidae). Molecular biology reports 38: 611-619.

Zhang D L, Gao J, Li M, Yuan J, Liang J, Yang H, Bu W. 2019. The complete mitochondrial genome of Tetraphleps aterrimus (Hemiptera: Anthocoridae): Genomic comparisons and phylogenetic analysis of Cimicomorpha. International Journal of Biological Macromolecules 130: 369-377.

Zhang D X, Hewitt G M. 1997. Insect mitochondrial control region: a review of its structure, evolution and usefulness in evolutionary studies. Biochemical Systematics and Ecology 25(2): 99-120.

Zhang D X, Szymura J M, Hewitt G M. 1995. Evolution and structural conservation of the control region of insect mitochondrial DNA. Journal of Molecular Evolution 40: 382-391.

Zhang H L, Zeng H H, Huang Y, Zheng Z M. 2013 a. The complete mitochondrial genomes of three grasshoppers, Asiotmethis zacharjini, Filchnerella helanshanensis and Pseudotmethis rubimarginis (Orthoptera: Pamphagidae). Gene 517(1): 89-98.

Zhang Q L, Yuan M L, Shen Y Y, 2013 b. The complete mitochondrial genome of Dolycoris baccarum (Insecta: Hemiptera: Pentatomidae). Mitochondrial DNA 24(5): 469-471.

Zhao L, Wei J, Zhao W, Chen C, Gao X, Zhao Q. 2021. The complete mitochondrial genome of Pentatoma rufipes (Hemiptera, Pentatomidae) and its phylogenetic implications. ZooKeys 1042: 51.

Zhao L, Zheng Z M, Huang Y, Sun H M, 2010. A comparative analysis of mitochondrial genomes in Orthoptera (Arthropoda: lnsecta) and genome descriptions of three grasshopper species. Zoological Science 27(8): 662-672.

Zhao Q, Wang J, Wang M Q, Cai B, Zhang H F, Wei J F. 2018. Complete mitochondrial genome of Dinorhynchus dybowskyi (Hemiptera: Pentatomidae: Asopinae) and phylogenetic analysis of Pentatomomorpha species. Journal of Insect Science 18(2): 44.

Zhao Z, Su T J, Chesters D, Wang S D, Ho S Y, Zhu C D, Chen X L, Zhang C T. 2013. The mitochondrial genome of Elodia flavipalpis Aldrich (Diptera: Tachinidae) and the evolutionary timescale of tachinid flies. PLoS One 8(4): p.e61814.

Zhong M, Wang X, Liu Q, Luo B, Wu C, Wen J. 2016. The complete mitochondrial genome of the flesh fly, Boettcherisca peregrine (Diptera: Sarcophagidae). Mitochondrial DNA Part A 27(1): 106-108.

Zhou Z, Huang Y, Shi F. 2007. The mitochondrial genome of Ruspolia dubia (Orthoptera: Conocephalidae) contains a short A+ T-rich region of 70 bp in length. Genome 50(9): 855-866.

Zhou Z, Liu H, Gang L, Dang L, Zhao L, Huo K. 2021. Characterization and phylogenetic analysis of the complete mitochondrial genome of Lathyrophthalmus quinquestriatus (Fabricius, 1794) (Diptera, Syrphidae). Mitochondrial DNA Part B 6(3): 1183-1185.

Zhu W, Yang L, Long J, Chang Z, Gong N, Mu Y, Lv S, Chen X. 2023. Characterizing the Complete Mitochondrial Genomes of Three Bugs (Hemiptera: Heteroptera) Harming Bamboo. Genes 14(2): 342.