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Complete Mitochondrial DNA Sequence of the Japanese Sardine Sardinops Melanostictus†

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Complete Mitochondrial DNA Sequence of the Japanese Sardine Sardinops Melanostictus† FISHERIES SCIENCE 2000; 66: 924–932 Original Article Complete mitochondrial DNA sequence of the Japanese sardine Sardinops melanostictus† Jun G INOUE,1,* Masaki MIYA,2 Katsumi TSUKAMOTO1 AND Mutsumi NISHIDA1 1Ocean Research Institute, University of Tokyo, Nakano-ku, Tokyo 164-8639 and 2Department of Zoology, Natural History Museum & Institute, Chiba, Chuo, Chiba 260-8682, Japan SUMMARY: We determined the complete nucleotide sequence of the mitochondrial genome for a Japanese sardine, Sardinops melanostictus (Teleostei: Clupeiformes). The entire genome was purified by gene amplification using long polymerase chain reactions (PCR), and the products were subsequently used as templates for PCR with 30 sets of fish-versatile primers (including three species-specific primers) that amplify contiguous, overlapping segments of the entire genome. Direct sequencing of the PCR products demonstrated that the genome [16 881 base pairs (bp)] contained the same 37 mitochondrial structural genes (two ribosomal RNA, 22 transfer RNA, and 13 protein- coding genes) as found in other vertebrates, with the gene order identical to that in typical verte- brates. A major non-coding region between the tRNAPro and tRNAPhe genes (1200 bp) was considered as the control (D-loop) region, as it has several conservative blocks characteristic to this region. KEY WORDS: complete mitochondrial DNA sequence, Japanese sardine, long-PCR, mitogenomics, Sardinops melanostictus. INTRODUCTION In such studies, a short segment of the mtDNA [notably those from the control (D-loop) region of Animal mitochondrial DNA (mtDNA) is a closed 300–1000 base pairs (bp)] were commonly amplified circular molecule, typically 16–20 kilobases (kb) in using the polymerase chain reactions (PCR), the length, comprising 37 genes encoding 22 transfer RNA products subsequently digested by various restriction (tRNA), two ribosomal RNA (rRNA), and 13 proteins, endonucleases [restriction fragment length polymor- plus a control region that initiates replication and tran- phism (RFLP) analyses] or directly sequenced. In some scription.1–3 Because of its compactness, maternal in- cases, however, analyses of genetic variations have heritance, fast evolutionary rate compared to that of the revealed ambiguous geographic structures of the local nuclear DNA, and the resulting short coalescence time, populations, partly because the segment was too short to mtDNA is a useful marker for population genetic stu- contain sufficient genetic variations or the evolutionary dies, such as analyses of gene flow, hybridization, and rate of the segment was not suitable for a specific purpose introgression.4,5 Consequently, its usefulness as a genetic of the study. Unfortunately, our knowledge on the com- marker has received much attention from applied bio- plete mitochondrial genomes in fisheries resources is logical sciences, such as fisheries biology.6 Numerous restricted to several fishes, such as loach,16 carp,17 trout,18 studies have employed mtDNA as a genetic marker cod,19 ginbuna,20 deep-sea fish Gonostoma gracile,21 and to investigate the geographic population structures of Atlantic salmon.22 Also the genetic analyses have fisheries resources in Japanese waters, including ayu,7,8 heavily depended upon the early availability of ‘univer- Japanese flounder,9–11 red sea bream,12,13 diamond-shaped sal’ PCR primers for several short, partial segments of the squid Thysanoteuthis rhombus,14 and abalone Haliotis mitochondrial genome, such as those of the control diversicolor.15 region, two rRNA, and cytochrome b genes.23 For more effective uses of the mtDNA as a genetic marker in fisheries biology, it appears that more mito- chondrial genomic (mitogenomic) information is needed *Corresponding author: Tel: 81-3-5351-6520. Fax: 81-3-5351-6514. Email: [email protected] from various fisheries resources. With limited time and †Mitogenomics of the commercially important fishes in Japan—I. resources, however, it has been technically difficult to Received 13 December 1999. Accepted 22 May 2000. obtain such longer mtDNA sequences from a wide variety Japanese sardine mitochondrial genome FISHERIES SCIENCE 925 of animals. Miya and Nishida21 have overcome this diffi- Long PCR was done in a Model 9700 thermal cycler culty by developing a PCR-based approach for sequenc- (Perkin-Elmer, Foster City, CA, USA), and reactions ing the complete mitochondrial genome of fishes that were carried out with 30 cycles of a 25 mL reaction employs a long PCR technique and a number of fish- volume containing 15.25 mL of sterile distilled H2O, versatile primers. In this approach, the entire mitochon- 2.5 mL of 10 ¥ LA PCR buffer II (TaKaRa, Otsu, Shiga, drial genome was purified by gene amplification using Japan), 4.0 mL dNTP (4 mM), 1.0 mL each primer long PCR and the products were subsequently used as (5 mM), 0.25 mL of 1.25 unit LA Taq (TaKaRa), and 1.0 templates for PCR with a number of newly designed, fish- mL of template containing approximately 5 ng DNA. versatile primers that amplify contiguous overlapping The thermal cycle profile was that of ‘shuttle PCR’: segments of the entire genome.21 The complete mtDNA denaturation at 98°C for 10 s, and annealing and exten- sequence is obtained by the direct sequencing of these sion combined at the same temperature (68°C) for 16 contiguous PCR products and preliminary experiments min. Long-PCR products were electrophoresed on a have revealed that this PCR-based approach for sequenc- 1.0% L 03 agarose (TaKaRa) gel and later stained with ing the complete mitochondrial genome is applicable to ethidium bromide for band characterization via ultravi- a wide variety of fishes (Miya M & Nishida M, unpubl. olet transillumination. The long-PCR products were data).21 It should be noted that this approach not only diluted with TE buffer (1:20) for subsequent use as PCR greatly reduces the possibility of amplification of mito- templates. chondrial pseudogenes in the nuclear genome, but also allows an accurate determination of the complete PCR and sequencing mtDNA sequences that is faster than sequencing cloned mtDNA.21,24–26 Also, it should be useful for small, rare, or We used 30 sets of primers that amplify contiguous, over- endangered species.21 lapping segments of the entire genome. These primers This paper, the first in a series of papers entitled include 57 fish-versatile primers that were designed with ‘Mitogenomics of the commercially important fishes in reference to the aligned, complete nucleotide sequences Japan,’ describes the mitochondrial genome and its gene from the mitochondrial genome of six species of bony organization of a clupeid, Sardinops melanostictus, one of fishes (loach,16 carp,17 trout,18 cod,19 bichir,31 and lung- the five Sardinops species that have been recognized on fish32). Three species-specific primers were supplemented the basis of geographic separation of the populations.27–29 in regions where no appropriate fish-versatile primers were available. MATERIALS AND METHODS The PCR was done in a Model 9700 thermal cycler (Perkin-Elmer), and reactions were carried out with Fish sample and DNA extraction 30 cycles of a 25 mL reaction volume containing 14.4 mL of sterile, distilled H2O, 2.5 mL of 10 ¥ PCR buffer II A Japanese sardine specimen was obtained from a com- (Perkin-Elmer), 2.0 mL of dNTP (4 mM), 2.5 mL of each mercial source and tissues for DNA extraction were primer (5 mM), 0.1 mL of 0.5 unit Ex Taq (TaKaRa), and immediately preserved in 99.5% ethanol. Total genomic 1.0 mL of template. The thermal cycle profile was as DNA was extracted from the muscle tissue using a follows: denaturation at 94°C for 15 s, annealing at 50°C QIAamp tissue kit (QIAGEN Hilden, Germany) fol- for 15 s, and extension at 72°C for 30 s. The PCR prod- lowing the manufacturer’s protocol. A voucher specimen ucts were electrophoresed on a 1.0% L 03 agarose gel and was deposited in the Fish Collection, National Science stained with ethidium bromide for band characterization Museum, Tokyo (NSMT-P 58444). via ultraviolet transillumination. Double-stranded PCR products were purified by fil- tration through a Microcon-100 (Amicon Inc., Bedford, Mitochondrial DNA purification by long PCR MA, USA), which were subsequently used for direct cycle sequencing with dye-labeled terminators (Perkin- We previously determined partial sequences for the 16S Elmer). Primers used were the same as those for PCR. All rRNA and cyt b genes from the S. melanostictus specimen sequencing reactions were performed according to the (Inoue JG, Miya M, Tsukamoto K, Nishida M, unpubl. manufacturer’s instructions. Labeled fragments were ana- data) using primer pairs 4 (L2510-16S H3058-16S) and + lyzed on a Model 310 DNA sequencer (Perkin-Elmer). 27 (L14734-Glu + H15557-CYB) designated in Table 1. On the basis of these two sequences, a set of species-spe- cific primers (Same-16S-L + Same-CYB-H; Table 1) were Sequence analyses designed so as to amplify the 16S–cyt b region (Fig. 1). The cyt b–16S region, a remaining portion of the whole The DNA sequences were analyzed using the computer mitochondrial genome, was amplified using another set software package program DNASIS version 3.2 (Hitachi of fish-versatile primers (L15285-CYB + H2582-16S; Software Engineering Co. Ltd, Yokohama, Japan). The Table 1). location of the 13 protein-coding genes was determined 926 FISHERIES SCIENCE JG Inoue et al. Table1 PCR and sequencing primers in the analysis of Japanese sardine mitochondrial genome Primers Sequence (5¢Æ3¢) Long PCR primers Same-16S-L1 CAA CCA CGA AAA GCG GCC CTA ATT GGA GCC Same-CYB-H1 GGC AGA TAG GAG GTT AGT AAT GAC AGT GGC L15285-CYB CCC TAA CCC GVT TCT TYG C H2582-16S ATT GCG CTA CCT TTG CAC GGT PCR and sequencing primers 1. L709-12S TAC ACA TGC AAG TCT CCG CA H1552-12S ACT TAC CGT GTT ACG ACT TGC CTC 2.
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