Abstract
In this study, the complete mitochondrial genomes of five noctuoid moth species, namely, Paectes cristatrix, Hemichloridia euprepia, Trigonodes hyppasia, Mythimna unipuncta, and Risoba obstructa, were newly sequenced and characterized. Based on our investigations, the five mitogenomes showed sizes of 15409, 15619, 15654, 15403, and 15233 bp, respectively, and encoded 37 genes (13 protein-coding, 2 ribosomal RNA, and 22 transfer RNA genes) and a control region. All protein-coding genes (PCGs) in these mitogenomes had typical ATN start codons except for cox1 and nad1. The non-canonical codon CGA was the starter in H. euprepia and M. unipuncta and TTG was the starter in T. hyppasia for cox1. The unusual codon GTG was the starter in R. obstructa for nad1. All tRNA genes showed distinctive putative cloverleaf structures except trnS1 (AGN), which lacked the dihydrouridine (DHU) stem. Bayesian inference (BI) and maximum likelihood (ML) analyses were employed based on 13 PCGs using 159 taxa among the five families of the superfamily Noctuoidea, and the results showed the monophyly of this superfamily with well-supported values. Phylogenetic analyses showed that the newly sequenced endemic species Hemichloridia euprepia clustered separately along with the subfamilies Cuculliinae and Acronictinae with fairly supported values.
Similar content being viewed by others
Data availability statement
The datasets generated during and/or analysed during the current study are available in the NCBI-National Center for Biotechnology Information repository (https://www.ncbi.nlm.nih.gov). The dataset for all the five species has been submitted to NCBI (Trigonodes hyppasia and Risoba obstructa Paectes cristatrix, Hemichloridia euprepia, and Mythimna unipuncta) and are publicly available at https://www.ncbi.nlm.nih.gov/nuccore/2166682 965; https://www.ncbi.nlm.nih.gov/nuccore/2166683019; https://www.ncbi.nlm.nigo/nuccore/MW846303.1; https://www.ncbi.nlm.nih.gov/nuccore/MW8657 54.1, and https://www.ncbi.nlm.nih.gov/nuccore/MW802209.1.
Abbreviations
- Ala:
-
alanine
- Arg:
-
arginine
- Arg:
-
arginine
- Asn:
-
asparagine
- Asp:
-
aspartic acid
- BP:
-
bootstrap proportion
- Cys:
-
cysteine
- Gln:
-
glutamine
- Glu:
-
glutamic acid
- Gly:
-
glycine
- His:
-
histidine
- Ile:
-
isoleucine
- Leu:
-
leucine
- Lys:
-
lysine
- Met:
-
methionine
- PCGs:
-
protein-coding genes
- Phe:
-
phenylalanine
- PP:
-
posterior probability
- Pro:
-
proline
- rRNAs:
-
ribosomal RNA
- RSCU:
-
relative synonymous codon usage
- Ser:
-
serine
- tRNAs:
-
transfer RNAs
- Trp:
-
tryptophan
- Tyr:
-
tyrosine
- Val:
-
valine
References
Anderson S, Bankier AT, Barrell BG, et al. 1981 Sequence and organization of the human mitochondrial genome. Nature 290 457–465
Bernt M, Daniel M, Kai R, et al. 2007 CREx: inferring genomic rearrangements based on common intervals. Bioinformatics 23 2957–2958
Bernt M, Donath A, Jühling F, et al. 2013 MITOS: improved de novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol. 69 313–319
Boore JL 1999 Animal mitochondrial genomes. Nucleic Acids Res. 27 1767–1780
Brown WM, George M and Wilson AC 1979 Rapid evolution of animal mitochondrial DNA. Proc. Natl. Acad. Sci. USA 76 1967–1971
Cameron SL 2014 Insect mitochondrial genomics: implications for evolution and phylogeny. Annu. Rev. Entomol. 59 95–117
Cao SS and Du YZ 2014 Characterization of the complete mitochondrial genome of Chilo auricilius and comparison with three other rice stem borers. Gene 548 270–276
Cao Y, Hao JS, Sun XY, et al. 2016 Molecular phylogenetic and dating analysis of pierid butterfly species using complete mitochondrial genomes. Genet. Mol. Res. 15 gmr15049196
Chai HN and Du YZ 2012 The complete mitochondrial genome of the pink stem borer, Sesamia inferens, in comparison with four other noctuid moths. Int. J. Mol. Sci. 13 10236–10256
Chen ZS, Xu Z, Ma L, et al. 2018 The complete mitochondrial genome of Paragabara curvicornuta (Lepidoptera: Noctuoidea: Erebidae). Mitochondrial DNA B Resour. 3 78–80
Cheng XF, Zhang LP, Yu DN, et al. 2016 The complete mitochondrial genomes of four cockroaches (Insecta: Blattodea) and phylogenetic analyses within cockroaches. Gene 586 115–122
Curole JP and Kocher TD 1999 Mitogenomics: Digging deeper with complete mitochondrial genomes. Trends Ecol. Evol. 14 394–398
Dai LS, Zhu BJ, Zhao Y, et al. 2016 Comparative mitochondrial genome analysis of Eligma narcissus and other lepidopteran insects reveals conserved mitochondrial genome organization and phylogenetic relationships. Sci. Rep. 6 26387
de Souza BR, Tay WT, Czepak C, et al. 2016 The complete mitochondrial DNA genome of a Chloridea (Heliothis) subflexa (Lepidoptera: Noctuidae) morpho-species. Mitochondrial DNA A 27 4532–4533
Dierckxsens N, Mardulyn P and Smits G 2017 NOVOPlasty: denovo assembly of organelle genomes from whole-genome data. Nucleic Acids Res. 45 e18
Djoumad A, Nisole A, Zahiri R, et al. 2017 Comparative analysis of mitochondrial genomes of geographic variants of the gypsy moth, Lymantria dispar, reveals a previously undescribed genotypic entity. Sci. Rep. 7 14245
Fang QQ, Mitchell A, Regier JC, et al. 2000 Phylogenetic utility of the nuclear gene dopa decarboxylase in noctuoid moths (Insecta: Lepidoptera: Noctuoidea). Mol. Phylogenet. Evol. 15 473–486
Fibiger M and Lafontaine JD 2005 A review of the higher classification of the Noctuoidea (Lepidoptera) with special reference to the Holarctic fauna. Esperiana 11 7–92
Garey JR and Wolstenholme DR 1989 Platyhelminth mitochondrial DNA: Evidence for early evolutionary origin of a tRNAser AGN that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. J. Mol. Evol. 28 374–387
Ghanavi HR, Twort V, Hartman TJ, et al. 2022 The (non) accuracy of mitochondrial genomes for family-level phylogenetics in Erebidae (Lepidoptera). Zoologica Scripta 51 695–707
Gong YJ, Wu QL and Wei SJ 2013 Complete mitogenome of the Argyrogramma agnata (Lepidoptera: Noctuidae). Mitochondrial DNA 24 391–393
Greiner S, Lehwark P and Bock R 2019 Expanded toolkit for the graphical visualization of organellar genomes. research version 1.3.1. Organellar genome DRAW (OGDRAW). Expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 47 59–64
Hampson GF 1902 The moths of India. Supplementary paper to the volumes in “The Fauna of British India”. Series II, Part VI. J. Bombay Nat. Hist. Soc. 14 197–219
Hampson GF 1926 Descriptions of new genera and species of Lepidoptera (Phalaenae) of the family Noctuidae (subfamily Noctuinae). (British Museum of Natural History)
Hao JJ, Hao JS, Sun XY, et al. 2014 The complete mitochondrial genomes of the Fenton’s wood white, Leptidea morsei, and the lemon emigrant, Catopsilia pomona. J. Insect Sci. 14 130
Huang Y, Liu Y, Zhu XY, et al. 2019 Comparative mitochondrial genome analysis of Grammodes geometrica and other noctuid insects reveals conserved mitochondrial genome organization and phylogeny. Int. J. Biol. Macromol. 125 1257–1265
Katoh K and Toh H 2010 Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26 1899–1900
Kitching IJ and Rawlins JE 1998 The Noctuoidea; in The Noctuoidea (Ed.) NP Kristensen (W. de Gruyter, Berlin) pp 355–401
Kong W and Yang J 2015 The complete mitochondrial genome of Rondotia menciana (Lepidoptera: Bombycidae). J. Insect Sci. 15 48
Kononenko VS and Pinratana A 2013 Moth of Thailand; in Noctuoidea. An illustrated catalogue of Erebidae, Nolidae, Euteliidae and Noctuidae (Insecta, Lepidoptera) in Thailand (Brothers of St. Gabriel in Thailand, Bangkok)
Kumar S, Stecher G, Li M, et al. 2018 MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 351547–1549
Lafontaine JD and Fibiger M 2006 Revised higher classification of the Noctuoidea (Lepidoptera). Can. Entomol. 138 610–635
Lavrov DV, Brown WM and Boore JL 2000 A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proc. Natl. Acad. Sci. USA 97 13738–13742
Li FB, Zhang HX, Shen WF, et al. 2015 Complete mitochondrial genome of the common cutworm Spodoptera litura (Lepidoptera: Noctuidae). Mitochondrial DNA 26 838–839
Li B, Zhou L, Liu G, et al. 2016 Complete mitochondrial genome of Naumann’s thrush Turdus naumanni (Passeriformes: Turdidae). Mitochondrial DNA PART A, DNA Mapp. Seq. Anal. 27 1117–1118
Li W, Wang Z and Che Y 2017 The complete mitogenome of the wood-feeding cockroach Cryptocercus meridianus (Blattodea: Cryptocercidae) and its phylogenetic relationships among cockroach families. Int. J. Mol. Sci. 18 2397
Li J, Zhao Y, Lin R, et al. 2019 Mitochondrial genome characteristics of Somena scintillans (Lepidoptera: Erebidae) and comparison with other Noctuoidea insects. Genomics 111 1239–1248
Liu QN, Bian DD, Jiang SH, et al. 2015 Characterization of the complete mitochondrial genome of the Oriental armyworm, Mythimna separata (Lepidoptera: Noctuidae). Eur. J. Entomol. 112 399–408
Liu H, Yang Y, Xu N, et al. 2019 Characterization and comparison of complete mitogenomes of three parrot species (Psittaciformes: Psittacidae). Mitochondrial DNA B 4 1851–1852
Lu HF, Su TJ, Luo AR, et al. 2013 Characterization of the complete mitochondrion genome of diurnal moth Amata emma (Butler) (Lepidoptera: Erebidae) and its phylogenetic implications. PLoS One 8 e72410
Ma Y, He K, Yu PP, et al. 2015 The complete mitochondrial genomes of three bristletails (Insecta: Archaeognatha): the paraphily of Machilide and insights into Archaeognathan phylogeny. PLoS One 10 e0117669
Mitchell A, Cho S, Regier JC, et al. 1997 Phylogenetic utility of elongation factor-1 alpha in Noctuoidea (Insecta: Lepidoptera): the limits of synonymous substitution. Mol. Biol. Evol. 14 381–390
Mitchell A, Mitter C and Regier JC 2006 Systematics and evolution of the cutworm moths (Lepidoptera: Noctuidae): evidence from two protein-coding nuclear genes. Syst. Entomol. 31 21–46
Nardi F, Carapelli A, Dallai R, et al. 2003 The mitochondrial genome of the olive fly Bactroceraoleae: Two haplotypes from distant geographical locations. Insect Mol. Biol. 12 605–611
Ojala D, Montoya J and Attardi G 1981 tRNA punctuation model of RNA processing in human mitochondria. Nature 290 470–474
Perera OP, Walsh TK and Luttrell RG 2016 Complete mitochondrial genome of Helicoverpa zea (Lepidoptera: Noctuidae) and expression profiles of mitochondrial-encoded genes in early and late embryos. J. Insect Sci. 16 40
Poole RW 1989 Noctuidae. Lepidopterorum Catalogus (New Series) Fascicle 118 Noctuidae, Part 1-3. (New York, Brill)
Rambaut A 2012 FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/
Ramírez-Ríos V, Franco-Sierra ND, Alvarez JC, et al. 2016 Mitochondrial genome characterization of Tecia solanivora (Lepidoptera: Gelechiidae) and its phylogenetic relationship with other lepidopteran insects. Gene 581 107–116
Riyaz M, Shah RA, Savarimuthu I, et al. 2021 Comparative mitochondrial genome analysis of Eudocima salaminia (Cramer, 1777) (Lepidoptera: Noctuoidea), novel gene rearrangement and phylogenetic relationship within the superfamily Noctuoidea. Mol. Biol. Rep. 48 4449–4463
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, et al. 2017 DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34 3299–3302
Salvato P, Simonato M, Battisti A, et al. 2008 The complete mitochondrial genome of the bag-shelter moth Ochrogaster lunifer (Lepidoptera, Notodontidae). BMC Genomics 9 331
Sam KK, Lau NS, Shu-Chien AC, et al. 2021 Complete mitochondrial genomes of Paedocypris micromegethes and Paedocypris carbunculus reveal conserved gene order and phylogenetic relationships of miniaturized cyprinids. Front. Ecol. Evol. 9 662501
Sivasankaran K, Mathew P, Anand S, et al. 2017 Complete mitochondrial genome sequence of fruit-piercing moth Eudocima phalonia (Linnaeus, 1763) (Lepidoptera: Noctuoidea). Genomics Data 14 66–81
Sun QQ, Sun XY, Wang XC, et al. 2012 Complete sequence of the mitochondrial genome of the Japanese buff-tip moth, Phalera flavescens (Lepidoptera: Notodontidae). Genet. Mol. Res. 11 4213–4225
Sun Y, Tian S, Qian C, et al. 2016a Characterization of the complete mitochondrial genome of Spilarctia robusta (Lepidoptera: Noctuoidea: Erebidae) and its phylogenetic implications. Eur. J. Entomol. 113 558–570
Sun YX, Wang L, Wei GQ, et al. 2016b Characterization of the complete mitochondrial genome of Leucoma salicis (Lepidoptera: Lymantriidae) and comparison with other Lepidopteran insects. Sci. Rep. 6 39153
Sun C, Liu B and Lu C 2019 Complete mitochondrial genome of the Siberian thrush, Geokichla sibirica sibirica (Aves, Turdidae). Mitochondrial DNA B 4 1150–1151
Sun CH, Liu HY, Min X, et al. 2020a Mitogenome of the little owl Athene noctua and phylogenetic analysis of Strigidae. Int. J. Biol. Macromol. 151 924–931
Sun Y, Zhu Y, Chen C, et al. 2020b The complete mitochondrial genome of Dysgonia stuposa (Lepidoptera: Erebidae) and phylogenetic relationships within Noctuoidea. PeerJ 8 e8780
Sun Y, Huang H, Liu Y, et al. 2021 Organization and phylogenetic relationships of the mitochondrial genomes of Speiredonia retorta and other lepidopteran insects. Sci. Rep. 11 2957
Taanman JW 1999 The mitochondrial genome: structure, transcription, translation and replication. Biochim. Biophys. Acta 1410 103–123
Taylor MF, McKechnie SW, Pierce N, et al. 1993 The lepidopteran mitochondrial control region: structure and evolution. Mol. Biol. Evol. 10 1259–1272
Tillich M, Lehwark P, Pellizzer T, et al. 2017 GeSeq–versatile and accurate annotation of organelle genomes. Nucleic Acids Res. 45 6–11
van Nieukerken EJ, Kaila L, Kitching IJ, et al. 2011 Order Lepidoptera Linnaeus, 1758. Zootaxa Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148 212–221
Wang X, Zhang H, Kitching I, et al. 2021 First mitogenome of subfamily Langiinae (Lepidoptera: Sphingidae) with its phylogenetic implications. Gene 789 145667
Wilson AC, Cann RL, Carr SM, et al. 1985 Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26 375–400
Wolstenholme DR 1992 Animal mitochondrial DNA: structure and evolution. Int. Rev. Cytol. 141 173–216
Wu QL, Cui WX, Du BZ, et al. 2014 The complete mitogenome of the turnip moth Agrotis segetum (Lepidoptera: Noctuidae). Mitochondrial DNA 25 345–347
Wu QL, Cui WX and Wei SJ 2015 Characterization of the complete mitochondrial genome of the black cutworm Agrotis ipsilon (Lepidoptera: Noctuidae). Mitochondrial DNA 26 139–140
Xiao-Hui G, Ming-Yang C, Ya-Feng H, et al. 2017 The complete mitochondrial genome of the monophagous moth Protegira songi (Lepidoptera: Noctuidae). Conserv. Genet. Resour. 9 277–279
Xin ZZ, Liu Y, Zhang DZ, et al. 2018 Comparative mitochondrial genome analysis of Spilarctia subcarnea and other noctuid insects. Int. J. Biol. Macromol. 107 121–128
Xu XD, Jia YY, Cao SS, et al. 2020 Six complete mitochondrial genomes of mayflies from three genera of Ephemerellidae (Insecta: Ephemeroptera) with inversion and translocation of trnI rearrangement and their phylogenetic relationships. PeerJ 8 e9740
Xue S, Zhang Y, Gao S, et al. 2019 Characterization and phylogenetic analysis of the complete mitochondrial genome of Ctenoplusia albostriata (Lepidoptera: Noctuidae: Plusiinae). Mitochondrial DNA B Resour. 4 3509–3510
Yang X, Cameron SL, Lees DC, et al. 2015 A mitochondrial genome phylogeny of owlet moths (Lepidoptera: Noctuoidea), and examination of the utility of mitochondrial genomes for lepidopteran phylogenetics. Mol. Phylogenet. Evol. 85 230–237
Yang M, Song L, Shi Y, et al. 2019 The complete mitochondrial genome of a medicinal insect, Hydrillodes repugnalis (Lepidoptera: Noctuoidea: Erebidae), and related phylogenetic analysis. Int. J. Biol. Macromol. 123 485–493
Ye F, Shi Y, Xing L, et al. 2013 The complete mitochondrial genome of Paracymoriza prodigalis (Leech, 1889) (Lepidoptera), with a preliminary phylogenetic analysis of Pyraloidea. Aquat. Insects 3571–88
Yin J, Hong GY, Wang AM, et al. 2010 Mitochondrial genome of the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) and comparison with other Lepidopterans. Mitochondrial DNA 21 160–169
Yuan ML and Zhang QL 2013 The complete mitochondrial genome of Gynaephora menyuanensis (Lepidoptera: Lymantriidae) from the Qinghai-Tibetan Plateau. Mitochondrial DNA 24 328–330
Zahiri R, Kitching IJ, Lafontaine JD, et al. 2011 A new molecular phylogeny offers hope for a stable family level classification of the Noctuoidea (Lepidoptera). Zool. Scr. 40 158–173
Zahiri R, Holloway JD, Kitching IJ, et al. 2012 Molecular phylogenetics of Erebidae (Lepidoptera, Noctuoidea). Syst. Entomol. 37 102–124
Zhang DX and Hewitt GM 1997 Insect mitochondrial control region: a review of its structure, evolution and usefulness in evolutionary studies. Biochem. Syst. Ecol. 25 99–120
Zhang DX, Szymura JM and Hewitt GM 1995 Evolution and structural conservation of the control region of insect mitochondrial DNA. J. Mol. Evol. 40 382–391
Zhang LL, Hao JS, Huang DY, et al. 2013 Complete mitochondrial genomes of the bright sunbean Curetis bulis and the small copper Lycaena phlaeas (Lepidoptera: Lycaenidae) and their phylogenetic implications. Genet Mol. Res. 12 4434–4445
Zhang D, Gao F, Jakovlić I, et al. 2020 PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol. Ecol. Resour. 20 348–355
Zhu XY, Xin ZZ, Liu Y, et al. 2018 The complete mitochondrial genome of Clostera anastomosis (Lepidoptera: Notodontidae) and implication for the phylogenetic relationships of Noctuoidea species. Int. J. Biol. Macromol. 118 1574–1583
Acknowledgements
This study was funded by the Department of Science and Technology (DST) – Science and Engineering Research Board (SERB) [grant number: EMR/2017/000566]. The authors are grateful to the Director, Entomology Research Institute, Loyola College, Chennai, India, for providing the facilities for this study.
Funding
The funding agency had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Contributions
MR: Conception and design data. RAS: Conception and design data. SI: Revising and editing the intellectual content. KS: Acquisition of data, analysis and interpretation of data and drafting the article. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no conflict of interest.
Additional information
Corresponding editor: Uma Ramakrishnan
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Riyaz, M., Shah, R.A., Savarimuthu, I. et al. Characterization of complete mitochondrial genomes of five noctuoid moths (Lepidoptera: Noctuoidea) and their phylogenetic implications. J Biosci 48, 48 (2023). https://doi.org/10.1007/s12038-023-00357-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12038-023-00357-z