Abstract
The white-spotted bamboo shark (Chiloscyllium plagiosum) is of great commercial, ecological and ornamental value and has been listed as a near-threatened species in the IUCN Red List. Characterizing the mitochondrial genome (mitogenome) should be useful for biodiversity and conservation investigations. In this study, the characteristics of the mitogenome of C. plagiosum were reported. The mitogenome of C. plagiosum was 16,726 bp in length, comprising 13 protein-coding genes, 2 ribosomal RNAs, 22 transfer RNAs and one control region, which was similar to most fish species. In the control region, some conserved motifs were identified, except for motifs in the central conserved domain. In addition, phylogenetic analysis revealed C. griseum was at the basal position among investigated bamboo shark species, suggesting the third codon positions in the mitochondrial protein-coding genes should be involved in bamboo shark phylogeny. Further studies with more powerful genetic markers are needed to resolve the phylogenetic conflicts in genus Chiloscyllium. These findings may have important evolutionary and conservation implications for sound management of C. plagiosum.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The mitochondrial genome sequence presented in this study have been deposited in NCBI GenBank database under accession numbers OP018327.
References
Bernt M, Donath A, Jühling F 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
Boore JL, Macey JR, Medina M (2005) Sequencing and comparing whole mitochondrial genomes of animals. Methods Enzymol 395:311–348. https://doi.org/10.1016/S0076-6879(05)95019-2
Brown TA, Clayton DA (2002) Release of replication termination controls mitochondrial DNA copy number after depletion with 2’3’-dideoxycytidine. Nucleic Acids Res 30:2004–2010. https://doi.org/10.1093/nar/30.9.2004
Cai S, Xu S, Song N, Gao T, Zhang Z (2014) Mitochondrial DNA control region structure and length polymorphism analysis of Setipinna tenuifilis. Acta Hydrobiol Sin 38:980–986. https://doi.org/10.7541/2014.145(In Chinese with English abstract)
Chen X, Ai W, Ye L, Wang X, Lin C, Yang S (2013) The complete mitochondrial genome of the grey bamboo shark (Chiloscyllium griseum) (Orectolobiformes: Hemiscylliidae): genomic characterization and phylogenetic application. Acta Oceanol Sin 32:59–65. https://doi.org/10.1007/s13131-013-0298-0
Chen X, Yang S, Pan C (2008) Genetic polymorphism of mitochondrial control region in Chiloscyllium plagiosum from coastal waters of southern China. Acta Oceanol Sin 30:115–121. https://doi.org/10.3321/j.issn:0253-4193.2008.06.014 (In Chinese with English abstract)
Chen X, Zhou Z, Pichai S, Huang X, Zhang H (2014) Complete mitochondrial genome of the brown-banded bamboo shark Chiloscyllium punctatum. Mitochondr DNA 25:113–114. https://doi.org/10.3109/19401736.2013.786710
Chen SF, Zhou YQ, Chen Y, Gu J (2018) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Cheng Y, Wang R, Sun Y, Xu TJ (2012) The complete mitochondrial genome of the small yellow croaker and partitioned Bayesian analysis of Sciaenidae fish phylogeny. Genet Mol Biol 35:191–199. https://doi.org/10.1590/S1415-47572012005000006
Compagno LJ (1984) Sharks of the world. United Nations Development Program, Rome. https://doi.org/10.1515/9780691210872
Da Cunha DB, da Silva Rodrigues-Filho LF, de Luna Sales JB (2017) A review of the mitogenomic phylogeny of the Chondrichthyes. In: da Silva Rodrigues-Filho LF, de Luna Sales JB, editors. Chondrichthyes-Multidisciplinary Approach. IntechOpen p113-126. https://doi.org/10.5772/intechopen.70028
Dierckxsens N, Mardulyn P, Smits G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45:e18–e18. https://doi.org/10.1093/nar/gkw955
Ding SX, Pan Y, Zeng HS, Wang J (2009) Characterization of 12 polymorphic microsatellite loci for the whitespotted bamboo shark (Chiloscyllium plagiosum Bennett). Mol Ecol Resour 9:1398–1400. https://doi.org/10.1111/j.1755-0998.2009.02676.x
Dulvy NK, Pacoureau N, Rigby CL et al (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Curr Biol 31:4773–4787. https://doi.org/10.1016/j.cub.2021.08.062
Ebert DA, Hsuan-Ching HO, White WT et al (2013) Introduction to the systematics and biodiversity of sharks, rays, and chimaeras (Chondrichthyes) of Taiwan. Zootaxa 3752(1):15–19. https://doi.org/10.11646/zootaxa.3752.1.3
Formenti G, Theissinger K, Fernandes C et al (2022) The era of reference genomes in conservation genomics. Trends Ecol Evol 37:197–202. https://doi.org/10.1016/j.tree.2021.11.008
Fu MN, Wang J, Ding SX, Du JY, Su SQ (2010) Studies on the genetic structure and genetic subdivision of white spotted bamboo shark, Chiloscyllium plagiosum, by analyzing mitochondrial Cyt b genes. J Trop Oceanogr 29:86–91. https://doi.org/10.3969/j.issn.1009-5470.2010.06.013 (In Chinese with English abstract)
Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK (2014) Sizing up the ecological role of sharks as predators. Mar Ecol Prog Ser 495:291–298. https://doi.org/10.3354/meps10597
Hohenlohe PA, Funk WC, Rajora OP (2021) Population genomics for wildlife conservation and management. Mol Ecol 30:62–82. https://doi.org/10.1111/mec.15720
Inoue G, Miya M, Lam K, Tay BH, Danks JA, Bell J, Venkatesh B (2010) Evolutionary origin and phylogeny of the modern Holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol Biol Evol 27:2576–2586. https://doi.org/10.1093/molbev/msq147
IUCN (2021) The IUCN Red List of Threatened Species C. plagiosum. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T124554059A124453319.en. Accessed April 11 2022
Iwasaki W, Fukunaga T, Isagozawa R et al (2013) MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Mol Biol Evol 30:2531–2540. https://doi.org/10.1093/molbev/mst141
Kousteni V, Mazzoleni S, Vasileiadou K, Rovatsos M (2021) Complete mitochondrial DNA genome of nine species of sharks and rays and their phylogenetic placement among modern. Elasmobranchs Genes 12:324. https://doi.org/10.3390/genes12030324
Larizza A, Pesole G, Reyes A, Sbisà E, Saccone C (2002) Lineage specificity of the evolutionary dynamics of the mtDNA D-loop region in rodents. J Mol Evol 54:145–155. https://doi.org/10.1007/s00239-001-0063-4
Lee WJ, Kocher TD (1995) Complete sequence of a sea lamprey (Petromyzon marinus) mitochondrial genome: early establishment of the vertebrate genome organization. Gene 139(2):873. https://doi.org/10.1101/gad.9.3.370
Liu TX, Jin XX, Wang RX, Xu TJ (2013) Complete sequence of the mitochondrial genome of Odontamblyopus rubicundus (Perciformes: Gobiidae): genome characterization and phylogenetic analysis. J Genet 92:423–432. https://doi.org/10.1007/s12041-013-0283-6
Lowe TM, Chan PP (2016) tRNAscan-SE on-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 44:W54–W57. https://doi.org/10.1093/nar/gkw413
Martin A, Naylor G, Palumbi S (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155. https://doi.org/10.1038/357153a0
Masstor NH, Samat A, Nor SM, Md-Zain BM (2014) Molecular phylogeny of the Bamboo Sharks (Chiloscyllium spp). BioMed Res Int 2014:213896. https://doi.org/10.1155/2014/213896
Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305. https://doi.org/10.1111/j.1365-2656.2010.01753.x
Naylor GJP, Caira J, Jensen K et al (2012) Elasmobranch phylogeny: a mitochondrial estimate based on 595 species. In: Carrier J, Musick J, Heithaus M (eds) Biology of sharks and their relatives, 2nd edn. CRC Press, Boca Raton FL, pp 31–56
Ojala D, Montoya J, Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470–474. https://doi.org/10.1038/290470a0
Pearce J, Fraser MW, Sequeira AM, Kaur P (2021) State of shark and ray genomics in an era of extinction. Front Mar Sci 8:744986. https://doi.org/10.3389/fmars.2021.744986
Sambrook J, Fritsch FE, Maniatis T (1982) Molecular Cloning: a Laboratory Manual. Biochem Educ 11:82. https://doi.org/10.1016/0307-4412-8390-068-7
Stein RW, Mull CG, Kuhn TS et al (2018) Global priorities for conserving the evolutionary history of sharks rays and chimaeras. Nat Ecol Evol 2:288–298. https://doi.org/10.1038/s41559-017-0448-4
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Uno Y, Nozu R, Kiyatake I et al (2020) Cell culture-based karyotyping of orectolobiform sharks for chromosome-scale genome analysis. Commun Biol 3:36–52. https://doi.org/10.1038/s42003-020-01373-7
Vélez-Zuazo X, Agnarsson I (2011) Shark tales: a molecular species-level phylogeny of sharks (Selachimorpha, Chondrichthyes). Mol Phylogenet Evol 58:207–217. https://doi.org/10.1016/j.ympev.2010.11.018
Waterhouse RM, Seppey M, Simão FA et al (2018) BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol 35:543–548. https://doi.org/10.1093/molbev/msx319
Xu SY, Sun DR, Song NG et al (2017) Local adaptation shapes pattern of mitochondrial population structure in Sebastiscus marmoratus. Environ biol fish 100:763–774. https://doi.org/10.1007/s10641-017-0602-5
Xu SY, Zhang H, Gao TX (2020) Comprehensive whole genome survey analyses of male and female brown-spotted flathead fish Platycephalus sp.1. Genomics 112:4742–4748. https://doi.org/10.1016/j.ygeno.2020.08.030
Xu SY, Zhao RR, Cai SS et al (2023) Application of genomic markers generated for ray-finned fishes in chondrichthyan phylogenomics. Org Divers Evol. https://doi.org/10.1007/s13127-023-00607-w
Zhang J, Liu Y, Zhang X et al (2013) The identification of microRNAs in the whitespotted bamboo shark (Chiloscyllium plagiosum) liver by Illumina sequencing. Gene 527:259–265. https://doi.org/10.1016/j.gene.2013.06.012
Zhang YL, Gao HY, Li HB et al (2020) The white-spotted bamboo shark genome reveals chromosome rearrangements and fastevolving immune genes of cartilaginous fish. iScience 23:101754. https://doi.org/10.1016/j.isci.2020.101754
Zhao RR, Lu Z, Cai SS et al (2021) Whole genome survey and genetic markers development of crocodile flathead Cociella Crocodilus. Anim Genet 52(1):891–895. https://doi.org/10.1111/age.13136
Zhao RR, Cai SS, Lu DF et al (2022) Genomic comparison and genetic marker identification of the white-spotted bamboo shark Chiloscyllium plagiosum. Front Mar Sci 9:936681. https://doi.org/10.3389/fmars.2022.936681
Zhong L, Wang M, Li D, Tang S, Chen X (2021) Mitochondrial genome of Eleutheronema rhadinum with an additional non-coding region and novel insights into the phylogenetics. Front Mar Sci 8:746598. https://doi.org/10.3389/fmars.2021.746598
Acknowledgements
We thank Mr. Qingjie Zhou from Haichang Ocean Park for sample collection.
Funding
This study was supported by the National Natural Science Foundation of China (grant number 32200413).
Author information
Authors and Affiliations
Contributions
Shanshan Cai conceived and designed the study. Dingfang Lu, Xiaowen Huang, Ruirui Zhao and Xiaoyan Xie processed and analyzed the data. All authors contributed to the preparation of the manuscript.
Corresponding author
Ethics declarations
Competing Interest
The authors declare no conflicts of interest.
Ethics Statement
Ethical review and approval was not required for the animal study because the sample was naturally dead when collecting.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lu, D., Huang, X., Zhao, R. et al. Characterization and Phylogenetic Analysis of the Complete Mitochondrial Genome of white-spotted Bamboo Shark (Chiloscyllium plagiosum). Thalassas 40, 125–132 (2024). https://doi.org/10.1007/s41208-023-00638-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41208-023-00638-2