Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-22T11:16:44.128Z Has data issue: false hasContentIssue false

First complete mitochondrial genome of Rhodinia species (Lepidoptera: Saturniidae): genome description and phylogenetic implication

Published online by Cambridge University Press:  03 September 2021

Dong-Bin Chen
Affiliation:
Department of Sericulture, College of Bioscience and Biotechnology, Shenyang Agricultural University, 120 Dongling Road, Shenyang110866, China
Ru-Song Zhang
Affiliation:
Department of Sericulture, College of Bioscience and Biotechnology, Shenyang Agricultural University, 120 Dongling Road, Shenyang110866, China
Xiang-Dong Jin
Affiliation:
Oak Silkmoth Group, Sericultural Institute of Jilin Province, 399 South Songjiang Road, Jilin132200, China
Jian Yang
Affiliation:
Department of Sericulture, College of Bioscience and Biotechnology, Shenyang Agricultural University, 120 Dongling Road, Shenyang110866, China
Peng Li
Affiliation:
Department of Sericulture, College of Bioscience and Biotechnology, Shenyang Agricultural University, 120 Dongling Road, Shenyang110866, China
Yan-Qun Liu*
Affiliation:
Department of Sericulture, College of Bioscience and Biotechnology, Shenyang Agricultural University, 120 Dongling Road, Shenyang110866, China
*
Author for correspondence: Yan-Qun Liu, Email: [email protected]

Abstract

To explore the characteristics of the mitochondrial genome (mitogenome) of the squeaking silkmoths Rhodinia, a genus of wild silkmoths in the family Saturniidae of Lepidoptera, and reveal phylogenetic relationships, the mitogenome of Rhodinia fugax Butler was determined. This wild silkmoth spins a green cocoon that has potential significance in sericulture, and exhibits a unique feature that its larvae can squeak loudly when touched. The mitogenome of R. fugax is a circular molecule of 15,334 bp long and comprises 13 protein-coding genes, two ribosomal RNA genes, 22 transfer RNA genes, and an A + T-rich region, consistent with previous observations of Saturniidae species. The 370-bp A + T-rich region of R. fugax contains no tandem repeat elements and harbors several features common to the Bombycidea insects, but microsatellite AT repeat sequence preceded by the ATTTA motif is not present. Mitogenome-based phylogenetic analysis shows that R. fugax belongs to Attacini, instead of Saturniini. This study presents the first mitogenome for Rhodinia genus.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Arunkumar, KP, Metta, M and Nagaraju, J (2006) Molecular phylogeny of silkmoths reveals the origin of domesticated silkmoth, Bombyx mori from Chinese Bombyx mandarina and paternal inheritance of Antheraea proylei mitochondrial DNA. Molecular Phylogenetics and Evolution 40, 419427.CrossRefGoogle ScholarPubMed
Benson, G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research 27, 573580.CrossRefGoogle ScholarPubMed
Bernt, M, Donath, A, Jühling, F, Externbrink, F, Florentz, C, Fritzsch, G, Pütz, J, Middendorf, M and Stadler, PF (2013) MIandOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69, 313319.CrossRefGoogle Scholar
Bouvier, EL (1936) Étude des Saturnioïdes normaux. Familie des Hémileucidés. Trosième et dernière partie. Annales de Sciences Naturelles et de Zoologie 10, 267529.Google Scholar
Cameron, SL (2014) Insect mitochondrial genomics: implications for evolution and phylogeny. Annual Review of Entomology 59, 95117.CrossRefGoogle ScholarPubMed
Cameron, SL and Whiting, MF (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, 112123.CrossRefGoogle Scholar
Castresana, J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540552.CrossRefGoogle ScholarPubMed
Chen, MM, Li, Y, Chen, M, Wang, H, Li, Q, Xia, RX, Zeng, CY, Li, YP, Liu, YQ and Qin, L (2014) Complete mitochondrial genome of the atlas moth, Attacus atlas (Lepidoptera: Saturniidae) and the phylogenetic relationship of Saturniidae species. Gene 545, 95101.CrossRefGoogle ScholarPubMed
Coppens, B (2020) Rhodinia Verecunda – ‘Taiwanese squeaking silkmoth’. Available at https://breedingbutterflies.com/rhodinia-verecunda-taiwanese-squeaking-silkmoth/ (Accessed 13 August 2020).Google Scholar
de Bruijn, MH (1983) Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature 304, 234241.CrossRefGoogle ScholarPubMed
Greiner, S, Lehwark, P and Bock, R (2019) OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research 47, W59W64.CrossRefGoogle ScholarPubMed
He, YY, Wang, X and Chen, LS (2017) The complete mitochondrial genome of Neoris haraldi Schawerda (Lepidoptera: Saturniidae). Mitochondrial DNA Part B: Resources 2, 625626.CrossRefGoogle Scholar
Hong, MY, Lee, EM, Jo, YH, Park, HC, Kim, SR, Hwang, JS, Jin, BR, Kang, PD, Kim, KG, Han, YS and 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, 4957.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17, 754755.CrossRefGoogle ScholarPubMed
Jalili, V, Afgan, E, Gu, Q, Clements, D, Blankenberg, D, Goecks, J, Taylor, J and Nekrutenko, A (2020) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2020 update. Nucleic Acids Research 48, W395W402.CrossRefGoogle ScholarPubMed
Jiang, ST, Hong, GY, Yu, M, Li, N, Yang, Y, Liu, YQ and Wei, ZJ (2009) Characterization of the complete mitochondrial genome of the giant silkworm moth, Eriogyna pyretorum (Lepidoptera: Saturniidae). International Journal of Biological Sciences 5, 351365.CrossRefGoogle Scholar
Kim, SR, Kim, MI, Hong, MY, Kim, KY, Kang, PD, Hwang, JS, Han, YS, Jin, BR and Kim, I (2009) The complete mitogenome sequence of the Japanese oak silkmoth, Antheraea yamamai (Lepidoptera: Saturniidae). Molecular Biology Reports 36, 18711880.CrossRefGoogle Scholar
Kim, MJ, Kang, AR, Jeong, HC, Kim, KG and Kim, I (2011) Reconstructing intraordinal relationships in Lepidoptera using mitochondrial genome data with the description of two newly sequenced lycaenids, Spindasis takanonis and Protantigius superans (Lepidoptera: Lycaenidae). Molecular Phylogenetics and Evolution 61, 436445.CrossRefGoogle Scholar
Kim, JS, Park, JS, Kim, MJ, Kang, PD, Kim, SG, Jin, BR, Han, YS and Kim, I (2012) Complete nucleotide sequence and organization of the mitochondrial genome of Eri-silkworm, Samia cynthia ricini (Lepidoptera: Saturniidae). Journal of Asia-Pacific Entomology 15, 162173.CrossRefGoogle Scholar
Kim, MJ, Choi, SW and Kim, I (2013) Complete mitochondrial genome of the larch hawk moth, Sphinx morio (Lepidoptera: Sphingidae). Mitochondrial DNA 24, 622624.CrossRefGoogle Scholar
Kim, JS, Kim, MJ, Jeong, JS and Kim, I (2018) Complete mitochondrial genome of Saturnia jonasii (Lepidoptera: Saturniidae): genomic comparisons and phylogenetic inference among Bombycoidea. Genomics 110, 274282.CrossRefGoogle ScholarPubMed
Kitching, IJ, Rougerie, R, Zwick, A, Hamilton, CA, St Laurent, RA, Naumann, S, Ballesteros, ML and Kawahara, AY (2018) A global checklist of the Bombycoidea (Insecta: Lepidoptera). Biodiversity Data Journal 6, e22236.CrossRefGoogle Scholar
Kong, WQ and Yang, JH (2015) The complete mitochondrial genome of Rondotia menciana (Lepidoptera: Bombycidae). Journal of Insect Science 15, 48.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549.CrossRefGoogle ScholarPubMed
Langley, J, van der Westhuizen, S, Morland, G and van Asch, B (2020) Mitochondrial genomes and polymorphic regions of Gonimbrasia belina and Gynanisa maja (Lepidoptera: Saturniidae), two important edible caterpillars of Southern Africa. International Journal of Biological Macromolecules 144, 632642.CrossRefGoogle Scholar
Lavrov, DV, Brown, WM and Boore, JL (2000) A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proceedings of the National Academy of Sciences of the USA 97, 1373813742.CrossRefGoogle ScholarPubMed
Liu, YQ, Li, YP, Pan, MH, Dai, FY, Zhu, XW, Lu, C and Xiang, ZH (2008) The complete mitochondrial genome of the Chinese oak silkmoth, Antheraea pernyi (Lepidoptera: Saturniidae). Acta Biochimica et Biophysica Sinica (Shanghai) 40, 693703.CrossRefGoogle Scholar
Liu, QN, Zhu, BJ, Dai, LS, Wei, GQ and Liu, CL (2012) The complete mitochondrial genome of the wild silkworm moth, Actias selene. Gene 505, 291299.CrossRefGoogle ScholarPubMed
Lowe, TM and Eddy, SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25, 955964.CrossRefGoogle ScholarPubMed
Michener, CD (1952) The Saturniidae (Lepidoptera) of the Western Hemisphere: morphology, phylogeny and classification. Bulletin of the American Museum of Natural History 98, 335502.Google Scholar
Mitamura, T (1998) Rearing of Rhodinia fugax Butler (Lepidoptera: Saturniidae) on a species of willow and on the artificial diet containing its left powder. Journal of Sericultural Science of Japan 67, 503506.Google Scholar
Nguyen, LT, Schmidt, HA, von Haeseler, A and Minh, BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268274.CrossRefGoogle ScholarPubMed
Pan, MH, Yu, QY, Xia, YL, Dai, FY, Liu, YQ, Lu, C, Zhang, Z and Xiang, ZH (2008) Characterization of mitochondrial genome of Chinese wild mulberry silkworm, Bomyx mandarina (Lepidoptera: Bombycidae). Science in China Series C: Life Science 51, 693701.Google Scholar
Park, JS, Kim, MJ and Kim, I (2016) The complete mitochondrial genome of the moon moth, Actias aliena (Lepidoptera: Saturniidae). Mitochondrial DNA 27, 149150.CrossRefGoogle Scholar
Perna, NT and Kocher, TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution 41, 353358.CrossRefGoogle ScholarPubMed
Ratnasingham, S and Hebert, PDN (2020) Barcode of life data system v4. Available at http://www.boldsystems.org/index.php/Taxbrowser_Taxonpage?taxid=94178 (Accessed 13 August 2020).Google Scholar
Regier, JC, Grant, MC, Mitter, C, Cook, CP, Peigler, RS and Rougerie, R (2008) Phylogenetic relationships of wild silkmoths (Lepidoptera: Saturniidae) inferred from four protein-coding nuclear genes. Systematics Entomology 33, 219228.CrossRefGoogle Scholar
Rubin, JJ, Hamilton, CA, McClure, CJW, Chadwell, BA, Kawahara, AY and Barber, JR (2018) The evolution of anti-bat sensory illusions in moths. Science Advances 4, eaar7428.CrossRefGoogle ScholarPubMed
Saito, S, Tamura, K and Aotsuka, T (2005) Replication origin of mitochondrial DNA in insects. Genetics 171, 16951705.CrossRefGoogle ScholarPubMed
Shantibala, T, Victor, T, Luikham, R, Arunkumar, KP, Sharma, HD, Lokeshwari, RK and Kim, I (2016) Complete mitochondrial genome of the wild Eri silkworm, Samia canningi (Lepidoptera: Saturniidae). Mitochondrial DNA 27, 844845.CrossRefGoogle Scholar
Shantibala, T, Devi, KM, Lokeshwari, RK, Anju, S and Luikham, R (2018) Complete mitochondrial genome of a latent wild oak Tasar silkworm, Antheraea frithi (Lepidoptera: Saturniidae). Mitochondrial DNA Part B: Resources 3, 1516.CrossRefGoogle Scholar
Sima, YH, Chen, M, Yao, R, Li, YP, Liu, T, Jin, X, Wang, LP, Su, JF, Li, XS and Liu, YQ (2013) The complete mitochondrial genome of the Ailanthus silkmoth, Samia cynthia cynthia (Lepidoptera: Saturniidae). Gene 526, 309317.CrossRefGoogle Scholar
Simon, C, Buckley, TR, Frati, F, Stewart, JB and Beckenbach, AT (2006) Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Annual Review of Ecology Evolution and Systematics 37, 545579.CrossRefGoogle Scholar
Singh, D, Kabiraj, D, Sharma, P, Chetia, H, Mosahari, PV, Neog, K and Bora, U (2017) The mitochondrial genome of Muga silkworm (Antheraea assamensis) and its comparative analysis with other lepidopteran insects. PLoS ONE 12, e0188077.CrossRefGoogle ScholarPubMed
Taanman, JW (1999) The mitochondrial genome: structure, transcription, translation and replication. Biochimica and Biophisica Acta 1410, 103123.CrossRefGoogle ScholarPubMed
Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F and Higgins, DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.CrossRefGoogle ScholarPubMed
Wang, X, Chen, ZM, Gu, XS, Wang, M and Zwick, A (2019) Phylogenetic relationships among Bombycidae s.l. (Lepidoptera) based on analyses of complete mitochondrial genomes. Systematics Entomology 44, 490498.CrossRefGoogle Scholar
Wernersson, R and Pedersen, AG (2003) RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Research 31, 35373539.CrossRefGoogle ScholarPubMed
Yang, L, Wei, ZJ, Hong, GY, Jiang, ST and Wen, LP (2009) The complete nucleotide sequence of the mitochondrial genome of Phthonandria atrilineata (Lepidoptera: Geometridae). Molecular Biology Reports 36, 14411449.CrossRefGoogle Scholar
Yang, XS, Xue, DY and Han, HX (2013) The complete mitochondrial genome of Biston panterinaria (Lepidoptera: Geometridae), with phylogenetic utility of mitochondrial genome in the Lepidoptera. Gene 515, 349358.CrossRefGoogle Scholar
Yang, J, Zhang, RS, Chen, DB, Chen, MM, Li, YP and Liu, YQ (2019) The complete mitochondrial genome of Antheraea proylei strain In981 (Lepidoptera: Saturniidae). Mitochondrial DNA Part B: Resources 4, 22642265.CrossRefGoogle Scholar
Yukuhiro, K, Sezutsu, H, Itoh, M, Shimizu, K and Banno, Y (2002) Significant levels of sequence divergence and gene rearrangements have occurred between the mitochondrial genomes of the wild mulberry silkmoth, Bombyx mandarina, and its close relative, the domesticated silkmoth, Bombyx mori. Molecular Biology and Evolution 19, 13851389.CrossRefGoogle ScholarPubMed
Zardoya, R (2020) Recent advances in understanding mitochondrial genome diversity. F1000Research 9, 270.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Chen et al. supplementary material

Chen et al. supplementary material

Download Chen et al. supplementary material(PDF)
PDF 1.3 MB