On the Species Identification of Korean Geoduck Clam (Panopea sp. 1) Based on the Morphological and Molecular Evidence
by
and
Jeonghoon Han
1,
Jong Guk Kim
2,
O-Nam Kwon
3,
Jordan Jun Chul Park
4,
Kyun-Woo Lee
1 and
Young-Ung Choi
1,* 1
Marine Bio-Resources Research Unit, Korea Institute of Ocean Science & Technology (KIOST), Busan 49111, Republic of Korea
2
Division of Zoology, Honam National Institute of Biological Resources, Mokpo 58762, Republic of Korea
3
GABI Co., Ltd., Gangneung 25440, Republic of Korea
4
Département des Sciences, Université Sainte-Anne, Church Point, NS B0W 1M0, Canada
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(11), 2115; https://doi.org/10.3390/jmse11112115
Submission received: 21 September 2023
/
Revised: 9 October 2023
/
Accepted: 2 November 2023
/
Published: 6 November 2023
(This article belongs to the Special Issue Recent Advances in Marine Mollusca: Evolutionary Biology and Molecular Phylogeny)
Abstract
:The geoduck clam is a high-value species in South Korea. However, the molecular and morphological characteristics of geoduck clams from the southern coast of South Korea remain unexamined. The accurate identification of native geoduck clams is crucial for their conservation and management. Therefore, this study used a combination of molecular and morphological analyses to characterize native geoduck clams from the southern coast of South Korea. Based on complete mitochondrial genome and morphological analyses, the native species of geoduck clam from this study area was identified as Panopea sp. 1. The complete mitochondrial genome sequencing of Panopea sp. 1 revealed a total of 16,225 bp in length with 37 genes (13 protein-coding genes, 22 tRNA genes, and 2 rRNA genes). It was also shown that Panopea sp. 1 belongs to the family Hiatellidae based on a phylogenetic analysis tree with 11 bivalve species. In particular, Panopea sp. 1 is closely related to three other Panopea species (Panopea sp., Panopea abrupta, and Panopea japonica). The phylogenetic analysis correlated with the morphological analysis. Overall, this is the first reliable record of Panopea sp. 1 in South Korea. These findings provide a basis for accurate species identification based on morphological characteristics and complete mitochondrial genome sequencing.
1. Introduction
The geoduck clams of the genus Panopea de la Groye, 1807, belonging to the family Hiatellidae (Mollusca, Bivalvia), are among the largest deep-burrowing bivalves [1,2]. They are widely distributed in subtidal substrates along shallow coastlines and are buried deeply in muddy sand sediments down to 30–100 cm [3]. To date, approximately 150 fossil species of the genus Panopea have been documented, but only 9 extant species have been described, spanning habitats covering from temperate to subtropical regions; 5 of these 9 species are distributed in the Northern Hemisphere [4]. In general, geoduck clams are well suited for aquaculture as a valuable commercial marine fishery resource because of their high protein content and edible proportions, comprising nearly 55% of their bodies [5,6]. Since the 1970s, geoduck clams have been collected and farmed overseas, and their annual production has been reported to be approximately 6000 metric tons; subsequently, their product value is rising owing to increased consumption [7]. The increase in geoduck clam collection has led to the identification and documentation of various species worldwide. Specifically, the Pacific geoduck, Panopea generosa A. Gould, 1850, is farmed and collected in the United States (USA) and Canada [8], the New Zealand geoduck, Panopea zelandica Quoy & Gaimard, 1835, is collected in New Zealand, Panopea abrupta (Conrad, 1849), is collected on a limited basis in Alaska, USA, and P. generosa and Panopea globose Dall, 1898, are collected in Mexico [9,10,11]. Therefore, these newly identified species highlight the importance of the conservation of geoduck clams worldwide and the identification of each region-specific species.
The geoduck clam Panopea japonica A. Adams, 1850 is an important bivalve resource and is mainly found in the coastal subtidal regions of Korea, Japan, northern China, and Russia [12]. In South Korea, despite its high commercial value, research on P. japonica has been mainly focused on its habitat ecology, growth, reproductive biology, seed production, feeding activity, and environmental tolerance [13,14,15]. However, specific species identity parameters based on the molecular and morphological characteristics of P. japonica remain unclear. Recently, Panopea sp. are a newly identified species which are distributed along the east coast of South Korea [16], whereas the geoduck clams inhabiting southern region of South Korea have yet to be examined and characterized. Therefore, it is important to emphasize that species identification is the preliminary step in the appropriate conservation and sustainable management of geoduck clam resources.
To date, mitochondrial DNA markers have been extensively applied in taxonomy and phylogenetics. Furthermore, mitochondrial DNA markers have previously been used for the identification of bivalve species, such as the flat Oyster, Ostrea denselamellosa [17], and Geoduck clam, Panopea sp. [16], indicating that mitochondrial DNA markers can be successfully used to identify bivalve species, including clams. Therefore, mitochondrial DNA markers were utilized in this study for the accurate species identification of geoduck clams collected from the southern coast of South Korea. Overall, here, we provide the complete mitochondrial genome of the native geoduck clam species from the southern coast of South Korea and compare their mitochondrial DNA genes to those of bivalve species using phylogenetic relationships. Overall, this study contributes to the population stock, conservation, and management of native geoduck clam species, while broadening the knowledge and evolutionary ecology of clams worldwide.
2. Materials and Methods
2.1. Sample Collection
Adult specimens of harvested native geoduck clams were provided by a local fish market on Geoje Island, South Korea, on 17 February 2023. The collection area is shown in Figure 1. All the protocols used for animal experimentation followed the Guidelines of the Institutional Animal Care and Experimental Committee, approved by the Korea Institute of Ocean Science & Technology (KIOST).
2.2. DNA Extraction, PCR Amplification, and DNA Sequencing
To extract genomic DNA, muscle tissue was retrieved from the samples and the DNeasy Blood and Tissue Kit (Qiagen, Valencia, CA, USA) was used. The quantity and quality of the isolated DNA were analyzed and measured at 230, 260, and 280 nm using a Victor3 multilabel plate reader (PerkinElmer, Waltham, MA, USA). To construct a genomic library, the TruSeq Nano DNA Kit was used (Macrogen, Seoul, South Korea) and the manufacturer’s instructions were followed (Illumina, San Diego, CA, USA). The assembly and annotation of the complete mitochondrial genomes of the geoduck clam species were performed using MITOS [18]. After the completion of the experiment, the voucher material was deposited at the National Marine Biodiversity Institute of Korea (MABIK).
2.3. Sequence Alignment and Phylogenetic Analysis
To construct a phylogenetic tree using previously identified species, the complete mitochondrial genomes of 12 bivalve species (five families: Arcticidae, Cardiidae, Hiatellidae, Myidae, and Lucinidae) were collected from the GenBank database (Table 1). The alignment of the concatenated set of 13 protein-coding genes (PCGs) for each mitochondrial genome was performed using the ClustalW algorithm in the MEGA software (ver. 10.0.1; Centre for Evolutionary Medicine and Informatics, Tempe, AZ, USA). To establish the best-fit substitution model for the phylogenetic analysis, the model with the lowest Bayesian and Akaike information criterion scores was estimated using a maximum likelihood (ML) analysis. Based on the results of the model test, the LG + G + I model was used with 1000 bootstrap replicates.
2.4. Morphological Characteristics
For the morphological identification of the geoduck clam specimen from the southern coast of South Korea, the morphology of its shell was analyzed. Live geoduck clam specimens were fixed in 95% ethanol and their valves were dissected for hinge structure and shell surface sculpture observations. Photographs of the geoduck clams (Figure 2) were taken with a Copy Stand system equipped camera (CS-920, Nikon, Shimadzu, Japan). The voucher material was deposited at the Honam National Institute of Biological Resources (HNIBR). The morphological description was established by referring to Signorelli and Alfaya [19], who carried out a taxonomic revision of Panopea abbreviata.
3. Results and Discussion
The species identification of geoduck clams in this study was described based on the significant morphological characteristics of the shell, such as shell thick to thin; externally white in color; external surface sculptured by irregular commarginal folds and widely spaced growth lines; outline elongated and subquadrate, with wide gaps at both ends; a length of 10 cm and height of up to 6.4 cm, a length-to-height ratio of 1.56, inequilateral, and slightly longer posteriorly; anterior end rounded, posterior end truncated to slightly produced ventrally, and ventral margin slightly convex; umbo weakly prominent and subcentral anteriorly (length from umbo to anterior end occupying 48% of the total length); a hinge with a dorsally recurved cardinal tooth; nymphal ridge short and covered by a ligament layer; the posterior ligament layer prominent, bilobed, dark brown in color, and with thin periostracum (tan in color); internal surface shear and white in color; pallial line continuous, separated from a ventral margin of approximately 0.9 cm; pallial sinus U-shaped, slightly deeper than high (length-to-height ratio 1.04); adductors positioned dorsally; posterior adductor scar reinforcement; and siphonal extension of 13.2 cm long in preserved specimens (in ethanol).
Based on the identified morphological features, the geoduck clam specimens from the southern coast of South Korea can be placed in the genus Panopea: an enlarged siphonal extension that fits into the mantle, elongated and subquadrate shells, a continuous pallial line, a short nymph, and one cardinal tooth in the hinge. Previously, the geoduck clam specimens collected from this region have been identified as P. japonica, originally reported from Japan. However, we found significant differences in the shell morphology of the geoduck clam specimens collected in this study and P. japonica (cf. Figure 3): (1) the length-to-height ratio of the clam shell was much larger in the study specimens (1.56) compared to that of P. japonica (1.39); (2) the postero-dorsal edge was relatively smooth in the study specimens, whereas as it is produced in P. japonica; the postero-ventral edge was slightly angular in the studied specimens, whereas it is rounded in P. japonica; and (3) the pallial sinus was much deeper in the studied specimens (the length-to-height ratio: 1.04) compared to that of P. japonica (1.59). These significant morphological differences made the geoduck clam specimens analyzed in this study readily distinguishable from P. japonica.
Recently, Han et al. [16] reported a novel Panopea sp. from the eastern coast of South Korea, including its shell morphology, complete mitochondrial genome sequence, and reproductive information. The native geoduck clam collected for this study from the southern coasts of South Korea was very similar to the eastern Panopea sp., however, we found several differences in the conchological features between both species: (1) growth lines on external surface were more widely spaced in the southern population examined in the present study; (2) the umbo was located more anteriorly in the eastern populations (length from umbo to anterior margin occupying 42% in eastern populations, contrary to 48% in the southern population); and (3) the internal surface of the eastern populations had an additional line parallel to the posterior outline that has not been reported from other congeners (Han et al. [16]; Figure 2c). Although the species identification of the genus Panopea based on morphological taxonomy is possible, it is difficult to accurately distinguish and identify similar species using morphological data alone due to morphological ambiguity and diversity [20].
In this study, the complete mitochondrial genome of the novel Panopea sp. 1 was sequenced and deposited in GenBank (GenBank accession number: OQ469488). The complete mitochondrial genome length of Panopea sp. 1 was 15,910 bp. This length is shorter than that of Panopea sp. (16,006 bp), but longer than those of Panopea abrupta (15,381 bp), Panopea globosa (15,469 bp), and Panopea generosa (15,585 bp) [16,21]. Furthermore, the mitochondrial genome of Panopea sp. 1 encodes a complete set of 37 genes (13 PCGs, 22 transfer RNA genes, and 2 ribosomal RNA genes) and a control region (D-loop) (Table 2 and Figure 4). The nucleotide composition of its mitochondrial genome is: 25.3% A, 39.4% T, 10.6% C, and 24.8% G. This composition is similar, but slightly different from that of other species in the genus Panopea, such as Panopea sp. (25.8% A, 38.4% T, 11.4% C, and 24.4% G), P. abrupta (25.6% A, 38.8% T, 11.3% C, and 24.3% G), P. generosa (25.0% A, 38.7% T, 11.2% C, and 25.0% G), and P. globosa (23.3% A, 40.4% T, 10.1% C, and 26.1% G). The A + T and G + C contents of the 13 PCGs in the mitochondrial genome of Panopea sp. 1 were 64.2% and 35.8%, respectively, whereas those in all sequences of the mitochondrial genome were 64.7% and 35.3%, respectively. In particular, the A + T content in the mitochondrial genome of Panopea sp. 1 was the same as that of Panopea sp. (64.2%) and similar to that of P. abrupta (64.4%), whereas it was higher than that of P. generosa (63.7%) and P. globosa (63.7%). Additionally, in Panopea sp. 1, all 13 PCGs used ATG as the start codon and TAA/TAG as stop codons. Twelve PCGs in Panopea sp. used ATG/GTG as the start codon, whereas nad4 started with the ATA codon in Panopea sp. Collectively, the comparative analysis of the complete mitochondrial genome of Panopea sp. 1 revealed intraspecific variations in the mitochondrial genomes of the genus Panopea.
The molecular phylogenetic analysis revealed that the phylogenetic placement of Panopea sp. 1 was in parallel with previous results [4,16,21]. The molecular phylogenetic tree of the complete mitogenome showed that the Panopea sp. 1 identified in this study clustered with the genus Panopea (Figure 5). However, within the genus Panopea, Panopea sp. 1 formed a separate clade from the genus Panopea. In particular, Panopea sp. 1 constituted three Panopea species (Panopea sp., P. abrupta, and P. japonica), which were placed together as sister groups, indicating that they are independent Panopea species. Based on these findings, in addition to the molecular and morphological results of this study, the native geoduck clam collected from the southern coast of South Korea was identified as Panopea species compiles, thus Panopea sp. 1. These results corroborate that the complete mitochondrial genome sequence is useful for the accurate species identification in the genera Panopea species.
In summary, based on its mitochondrial DNA sequence and morphological features, Panopea sp. 1 is the first-reported species from the southern coast of South Korea. The complete mitochondrial genome sequence was sufficient to identify the Panopea species collected from the southern coast of South Korea, supporting the usefulness of mitochondrial DNA-based markers in bivalve species identification. These findings will be useful for substantiating the precise molecular phylogeny for species identification and evolutionary studies in relation to the conservation and management of clam resources.
Author Contributions
Data curation, formal analysis, writing—original draft, J.H.; investigation, J.G.K., J.J.C.P. and K.-W.L.; conceptualization, formal analysis, project administration, funding acquisition, O.-N.K. and Y.-U.C. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by supported by the Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (2018-0377) and by the KIOST project (PEA0122).
Institutional Review Board Statement
All experiments were conducted in compliance with the guidelines of the Institutional Animal Care and Experimental Committee of the Korea Institute of Ocean Science and Technology (KIOST) which approved the experimental protocol.
Informed Consent Statement
Not applicable.
Data Availability Statement
All data generated or analyzed during this study are available from the KIOST data repository. Materials are available upon request by the corresponding author.
Acknowledgments
The authors acknowledge the support of the Korea Institute of Marine Science & Technology Promotion (KIMST), funded by the Ministry of Oceans and Fisheries (2018-0377) and the KIOST project (PEA0122). We are also thankful to Moongeun Yoon of the National Marine Biodiversity Institute of Korea for his help and friendly attitude during this study. Finally, we thank the editor and anonymous reviewers, whose comments have greatly improved the manuscript.
Conflicts of Interest
The authors declare no conflict of interest.
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Figure 1.
Sampling site of the Geoduck clam, Panopea sp. 1, on southern coast of South Korea.
Figure 2.
Photographs of Panopea sp. 1 examined in the present study. (a) Habitus, right side; (b) habitus, dorsal; (c) interior view of left valve; and (d) detail of hinge structure in left valve.
Figure 2.
Photographs of Panopea sp. 1 examined in the present study. (a) Habitus, right side; (b) habitus, dorsal; (c) interior view of left valve; and (d) detail of hinge structure in left valve.
Figure 3.
Photographic images of Panopea japonica after Okutano (2000) with no scale (a) exterior view of left valve; and (b) interior view of right valve.
Figure 3.
Photographic images of Panopea japonica after Okutano (2000) with no scale (a) exterior view of left valve; and (b) interior view of right valve.
Figure 4.
The mitochondrial genome map of Panopea sp. 1.
Figure 5.
Maximum-likelihood phylogeny of the complete mitogenomes. The red triangle indicates the Panopea sp. 1 analyzed in this study.
Figure 5.
Maximum-likelihood phylogeny of the complete mitogenomes. The red triangle indicates the Panopea sp. 1 analyzed in this study.
Table 1.
List of complete mitochondrial genomes used in this study.
| Family | Species | Size (bp) | Accession No. |
|---|---|---|---|
| Arcticidae | Arctica islandica | 18,289 | NC_022709 |
| Cardiidae | Acanthocardia tuberculata | 16,104 | NC_008452 |
| Cardiidae | Fulvia mutica | 19,110 | NC_022194 |
| Cardiidae | Tridacna squamosa | 20,930 | NC_026558 |
| Hiatellidae | Panopea abrupt | 15,381 | KX494111 |
| Hiatellidae | Panopea generosa | 15,585 | NC_025635 |
| Hiatellidae | Panopea globosa | 15,469 | NC_025636 |
| Hiatellidae | Panopea sp. | 16,006 | OQ469487 |
| Lucinidae | Loripes lacteus | 17,321 | NC_013271 |
| Lucinidae | Lucinella divaricata | 18,940 | NC_013275 |
| Myidae | Mya arenaria | 17,947 | NC_024738 |
Table 2.
Summary of Panopea sp. 1 mitogenome.
| Full Gene Name | Location | Size (bp) | Start Codon | Stop Codon | Intergenic Region * |
|---|---|---|---|---|---|
| Cytochrome c oxidase subunit I (cox1) | 1–1563 | 1563 | GTG | TAG | 0 |
| D-lopp (DR) | 1564–2308 | 745 | - | - | 0 |
| Cytochrome c oxidase subunit II (cox2) | 2309–3046 | 738 | ATG | TAA | 10 |
| tRNA-Val (trnV) | 3057–3121 | 65 | - | - | 2 |
| tRNA-Thr (trnT) | 3124–3189 | 66 | - | - | 68 |
| tRNA-Tyr (trnY) | 3258–3319 | 72 | - | - | 11 |
| NADH dehydrogenase subunit 4L (nad4l) | 3331–3621 | 291 | ATG | TAG | 52 |
| ATP synthase F0 subunit 8 (atp8) | 3674–3787 | 114 | ATG | TAA | 163 |
| NADH dehydrogenase subunit 4 (nad4) | 3951–5138 | 1188 | ATG | TAG | 0 |
| tRNA-His (trnH) | 5139–5202 | 64 | - | - | 0 |
| tRNA-Glu (trnE) | 5203–5266 | 64 | - | - | −5 |
| tRNA-Ser2 (trnS2) | 5262–5324 | 63 | - | - | 3 |
| NADH dehydrogenase subunit 3 (nad3) | 5328–5693 | 366 | ATG | TAG | 2 |
| tRNA-Ile (trnI) | 5696–5762 | 67 | - | - | 6 |
| tRNA-Asp (trnD) | 5769–5832 | 64 | - | - | 4 |
| tRNA-Lys (trnK) | 5837–5899 | 63 | - | - | 2 |
| tRNA-Leu2 (TrnL2) | 5902–5966 | 65 | - | - | 0 |
| NADH dehydrogenase subunit 1 (nad1) | 5967–6890 | 924 | ATG | TAA | 1 |
| tRNA-Leu1 (TrnL1) | 6892–6956 | 65 | - | - | 33 |
| tRNA-Asn (TrnN) | 6990–7056 | 67 | - | - | 1 |
| NADH dehydrogenase subunit 5 (nad5) | 7058–8782 | 1725 | ATG | TAA | −1 |
| NADH dehydrogenase subunit 6 (nad6) | 8782–9303 | 522 | ATG | TAG | 3 |
| tRNA-Arg (trnR) | 9307–9370 | 64 | 2 | ||
| Cytochrome b (cob) | 9373–10,530 | 1158 | GTG | TAA | 8 |
| tRNA-Trp (trnW) | 10,539–10,605 | 68 | - | - | −52 |
| 16S ribosomal RNA(trnL) | 10,554–11,838 | 1285 | - | - | 0 |
| ATP synthase F0 subunit 6 (atp6) | 11,839–12,546 | 708 | ATG | TAA | 7 |
| tRNA-Met (trnM) | 12,554–12,617 | 64 | - | - | 1 |
| 12S ribosomal RNA (rrnS) | 12,619–13,481 | 863 | - | - | 0 |
| Cytochrome c oxidase subunit III (cox3) | 13,482–14,267 | 786 | ATG | TAG | 4 |
| tRNA-Ser1 (trnS1) | 14,272–14,338 | 67 | - | - | 0 |
| NADH dehydrogenase subunit 2 (nad2) | 14,339–15,385 | 1047 | ATG | TAA | 11 |
| tRNA-Gln (trnQ) | 15,397–15,462 | 66 | - | - | 8 |
| tRNA-Phe (trnF) | 15,471–15,533 | 63 | - | - | 14 |
| tRNA-Cys (trnC) | 15,548–15,612 | 65 | - | - | 22 |
| tRNA-Pro (trnP) | 15,635–15,701 | 67 | - | - | 10 |
| tRNA-Gly (trnG) | 15,712–15,777 | 66 | - | - | 14 |
| tRNA-Ala (trnA) | 15,792–15,856 | 65 | - | - | - |
* Negative numbers indicate overlapping nucleotides between adjacent genes.
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MDPI and ACS Style
Han, J.; Kim, J.G.; Kwon, O.-N.; Park, J.J.C.; Lee, K.-W.; Choi, Y.-U. On the Species Identification of Korean Geoduck Clam (Panopea sp. 1) Based on the Morphological and Molecular Evidence. J. Mar. Sci. Eng. 2023, 11, 2115. https://doi.org/10.3390/jmse11112115
AMA Style
Han J, Kim JG, Kwon O-N, Park JJC, Lee K-W, Choi Y-U. On the Species Identification of Korean Geoduck Clam (Panopea sp. 1) Based on the Morphological and Molecular Evidence. Journal of Marine Science and Engineering. 2023; 11(11):2115. https://doi.org/10.3390/jmse11112115
Chicago/Turabian StyleHan, Jeonghoon, Jong Guk Kim, O-Nam Kwon, Jordan Jun Chul Park, Kyun-Woo Lee, and Young-Ung Choi. 2023. "On the Species Identification of Korean Geoduck Clam (Panopea sp. 1) Based on the Morphological and Molecular Evidence" Journal of Marine Science and Engineering 11, no. 11: 2115. https://doi.org/10.3390/jmse11112115
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