Abstract
Nurudea zhengii Ren was identified by aphid morphological characteristics as well as the gall shape and host plant species, and placed in the tribe Fordini (Hemiptera, Aphididae, Eriosomatinae). Here, its whole genome was firstly sequenced by a genome-skimming method and its mitochondrial genome (mitogenome) was assembled to examine its genetic variation and phylogenetic position. The complete mitogenome of Nurudea zhengii is 15,392 bp in length, and consists of 13 protein-coding genes, 22 tRNAs, two rRNAs and one D-loop region. The gene order follows the mitogenomes of the other Rhus gall aphids, and similarly has an AT bias with the content of 83.9%. The majority strand is A-skewed and C-skewed, and shows opposite skewness for G-skewed in the minority strands. The ratios of nonsynonymous to synonymous substitution rates of protein-coding genes are lower than one except for ATP8, which indicated that ATP8 was undergoing positive selection. Phylogenetic analysis among the Rhus gall aphids based on 13 protein-coding genes and two rRNA genes showed that N. zhengii was sister to N. shiraii, and then clustered with N. yanoniella as a group with high support value. The two species, N. shiraii and N. yanoniella, share the same host plant Rhus chinensis, while the host of N. zhengii is R. hypoleuca. However, the phylogenetic relationship indicated that the taxa sharing the same host plant were not absolutely clustered as the closest taxa at least at species level.
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Data Availability
The mitogenome data has been submitted to GenBank with the accession No. OM084945. The genomic sequence data supporting the study’s findings are publicly available in NCBI’s GenBank https://www.ncbi.nlm.nih.gov/sra/SRX13762787. The associated BioProject, BioSample, and SRA numbers are PRJNA794879, SAMN24603883, SRP354794.
References
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021
Battaglia V, Gabrieli P, Brandini S, Capodiferro MR, Javier PA, Chen XG, Achilli A et al (2016) The worldwide spread of the tiger mosquito as revealed by mitogenome haplogroup diversity. Front Genet 7:208. https://doi.org/10.3389/fgene.2016.00208
Bell J (1851) Chinese galls. J Pharm Biomed Anal 10:128
Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J et al (2013) MITOS: improved De novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69:313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Blackman RL, Eastop VF (1984) Aphids on the world’s crops: an Identification and information guide. Oriental Insects 35(1):104. https://doi.org/10.1080/00305316.2001.10417292
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27(8):1767–1780. https://doi.org/10.1093/nar/27.8.1767
Cameron SL (2014a) Insect mitochondrial genomics: implications for evolution and phylogeny. Annu Rev Entomol 59:95–117. https://doi.org/10.1146/annurev-ento-011613-162007
Cameron SL (2014b) How to sequence and annotate insect mitochondrial genomes for systematic and comparative genomics research. Syst Entomol 39(3):400–411. https://doi.org/10.1111/syen.12071
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Phylogenet Evol 17(4):540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Chen J, Wang Y, Qin M, Jiang LY, Qiao GX (2019) The mitochondrial genome of Greenidea psidii van der Goot (Hemiptera: Aphididae: Greenideinae) and comparisons with other Aphididae aphids. Int J Biol Macromol 122:824–832. https://doi.org/10.1016/j.ijbiomac.2018.10.209
Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 17(4):1394–1403. https://doi.org/10.1101/gr.2289704
Darty K, Denise A, Ponty Y (2009) VARNA: interactive drawing and editing of the RNA secondary structure. Bioinformatics 25(15):1974–1975. https://doi.org/10.1093/bioinformatics/btp250
Eastop VF, Hille Ris Lambers D (1976) Survey of the world’s aphids. The Hague. pp 573
Favret C (2021) Aphid Species File. Version 5.0/5.0. http://Aphid.SpeciesFile.org. Accessed 3 Nov 2022
Greiner S, Lehwark P, Bock R (2019) OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res 47(W1):W59–W64. https://doi.org/10.1101/545509
Hurst LD (2002) The ka/ks ratio: diagnosing the form of sequence evolution. Trends Genet 18(9):486. https://doi.org/10.1016/S0168-9525(02)02722-1
Katoh K, Rozewicki J, Yamada KD (2017) Mafft online service:multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166. https://doi.org/10.1093/bib/bbx108
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Kuraku S, Zmasek CM, Nishimura O, Katoh K (2013) ALeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res 41(W1):W22–W28. https://doi.org/10.1093/nar/gkt389
Ma C, Yang PC, Jiang F, Chapuis MP, Shali Y, Sword GA, Kang L (2012) Mitochondrial genomes reveal the global phylogeography and dispersal routes of the migratory locust. Mol Ecol 21:4344–4358. https://doi.org/10.1111/j.1365-294X.2012.05684.x
Matsumura S (1917) A collection of essays for Mr. Yasushi Nawa, written in commemoration of his sixtieth Birthday. In: Nagano K (ed) Gifu Japan, pp 75–85
Perna NT, Koche TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41(3):353–358. https://doi.org/10.1007/BF00186547
Ren ZM, Harris AJ, Dikow RB, Ma EB, Zhong Y, Wen J (2017) Another look at the phylogenetic relationships and intercontinental biogeography of eastern Asian–North American Rhus gall aphids (Hemiptera: Aphididae: Eriosomatinae): evidence from mitogenome sequences via genome skimming. Mol Phylogenet Evol 117:102–110. https://doi.org/10.1016/j.ympev.2017.05.017
Ren ZM, Su X, von Dohlen CD, Wen J (2018) Nurudea zhengii Ren, a new species of the Rhus Gall Aphids (Aphididae: Eriosomatinae: Fordini) from eastern China. Pakistan J Zool 50(6):2087–2092. https://doi.org/10.17582/journal.pjz/2018.50.6.2087.2092
Ren ZM, von Dohlen CD, Harris AJ, Dikow RB, Su X, Wen J (2019) Congruent phylogenetic relationships of Melaphidina aphids (Aphididae: Eriosomatinae: Fordini) according to nuclear and mitochondrial DNA data with taxonomic implications on generic limits. PLoS ONE 14(2):e0213181. https://doi.org/10.1371/journal.pone.0213181
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302. https://doi.org/10.1093/molbev/msx248
Shao R, Dowton M, Murrell A, Barker SC (2003) Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. Mol Biol Evol 20(10):1612–1619. https://doi.org/10.1093/molbev/msg176
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56(4):564–577. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Tsai PH, Tang C (1964) The classification of the Chinese gall aphids with descriptions of three new genera and six new species from Meitan. Kweichow Ecol Entomol 97(16):405–418
Wei DD, Lang N, Tao Y, He W, Tu YQ, Miao ZQ, Yang L, Wang JJ (2019) The mitochondrial genome of the brown citrus aphid Aphis (Toxoptera) citricidus: insights into the repeat regions in aphids and phylogenetic implications. Int J Biol Macromol 136:531–539. https://doi.org/10.1016/j.ijbiomac.2019.06.101
Yang ZX, Chen XM, Havill NP, Feng Y, Chen H (2010) Phylogeny of Rhus gall aphids (Hemiptera: Pemphigidae) based on combined molecular analysis of nuclear EF-1α and mitochondrial COII genes. Entomol Sci 13:351–357. https://doi.org/10.1111/j.1479-8298.2010.00391.x
Yang M, Song L, Shi Y, Li J, Zhang Y, Song N (2019) The first mitochondrial genome of the family Epicopeiidae and higher-level phylogeny of Macroheterocera (Lepidoptera: Ditrysia). Int J Biol Macromol 136:123–132. https://doi.org/10.1016/j.ijbiomac.2019.06.051
Zhang GX, Qiao GX, Zhong TS, Zhang WY (1999) Fauna sinica insecta. Homoptera: mindaridae and pemphigidae, vol 14. Science Press, Beijing
Acknowledgements
The research was funded by The National Natural Science Foundation of China with Grant number 31870366, Shanxi International Science and Technology Cooperation Project with no. 201803D421051, Research Project Supported by Shanxi Scholarship Council of China with no. 2020-018, and the National High Technology Research and Development “863” Program with no. 2014AA021802
Funding
This work was funded by National Natural Science Foundation of China (Grant No. 31870366), International Science and Technology Cooperation Program of Shanxi Province (Grant No. 201803D421051), Shanxi Scholarship Council of China (Grant No. 2020-018) and National High-tech Research and Development Program (Grant No. 2014AA021802).
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Zhumei Ren: conceptualization, funding acquisition, investigation, project administration, resources, supervision, writing—review & editing. Yuzhen Song: formal analysis, investigation, methodology, data curation, writing—original draft, software. Yukang Liang: data curation, methodology. Wenli Ma: validation, writing—review & editing. M. James C. Crabbe: methodology, validation, writing—review & editing.
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Song, Y., Liang, Y., Ma, W. et al. Complete Mitochondrial Genome and Phylogenetic Position of Nurudea zhengii Ren (Insecta, Hemiptera, Aphididae). Biochem Genet (2024). https://doi.org/10.1007/s10528-024-10717-5
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DOI: https://doi.org/10.1007/s10528-024-10717-5