Gene Expression Profiles of Long-Chain Acyl-Coenzyme A Dehydrogenase, Nuclear Distribution C-Containing Protein 3, and Receptor Tyrosine Kinase Tie-1 in Swimming Larva of Sea Cucumber Apostichopus japonicus

Sehwan Kim1,2, Seungheon Lee1, Gil Jung Kim1, Young Chang Sohn1,
Author Information & Copyright
1Department of Marine Bioscience, Gangneung-Wonju National University, Gangneung 25457, Korea
2Samcheok Fisheries Resource Center, Samcheok 25932, Korea
Corresponding author Young Chang Sohn, Department of Marine Bioscience, Gangneung-Wonju National University, Gangneung 25457, Korea, Tel: +82-33-640-2348, E-mail:

© Copyright 2020 The Korean Society of Developmental Biology. This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received: Apr 05, 2023 ; Revised: May 13, 2023 ; Accepted: Jun 09, 2023

Published Online: Jun 30, 2023


The sea cucumber, Apostichopus japonicus, is one of the most valuable aquatic species. The color of body wall and appearance are important for the value of sea cucumbers. To examine expression pattern of long-chain acyl-coenzyme A dehydrogenase (LCAD), nuclear distribution C-containing protein 3 (NUDCD3), and receptor tyrosine kinase Tie-1 (TIE1), previously reported as differently expressed genes during the pigmentation of sea cucumber, we analyzed the temporal profiles of LCAD, NUDCD3, and TIE1 mRNAs in LED-exposed and light-shielded A. japonicus. Real-time quantitative PCR revealed that the LCAD, NUDCD3, and TIE1 mRNAs from the juveniles at 40–60 days post-fertilization (dpf) exhibited increasing patterns as compared to those of an early developmental larva (6-dpf). At 60-dpf juveniles, the LCAD and TIE1 mRNA levels of LED-exposed individuals were higher than those of light-shielded ones, whereas at 40-dpf and 50-dpf juveniles, the NUDCD3 mRNA expression was higher in the light-shielded condition (p<0.05). In the pigmented juveniles (90-dpf), the LCAD and TIE1 mRNA levels tended to show higher levels in red individuals than those in green ones, but there was a conversely higher level of NUDCD3 mRNA in green larva. In situ examination of LCAD and NUDCD3 mRNAs in light-shielded 6-dpf larva revealed that both genes are mainly expressed in the internal organs compared to the body surface. Together, these results may provide insights into the differential gene expression of LCAD, NUDCD3, and TIE1 during pigmentation process of the sea cucumber.

Keywords: Swimming larva; Body color; Gene expression; Light emitting diode; Apostichopus japonicus


Sea cucumbers are valuable marine resources supporting coastal livelihoods around the world. Of these, the sea cucumber, Apostichopus japonicus (Echinodermata: Holothuroidea), is one of the most economically important species inhabiting the shallow shelf of coastal regions around the Korean Peninsula, China, Japan (main island), and the Russian Far East (Liu, 2015). Color variation is an important trait in the sea cucumber aquaculture industry, which affects the market price of holothurian products (Jiang et al., 2013; Ru et al., 2019). Environmental factors, such as food and habitat, were found to determine the body color of sea cucumbers (MOF, 2004; Jiang et al., 2013). Interestingly, the red type sea cucumber showed definite genetic differentiation from the green and black types (Kan-No & Kijima, 2003). A report also suggested that the body color is affected by genetic factors in the parental generation (Park, 2006), partially supported by significantly different single-nucleotide polymorphism genotypes in allele-specific HSP70 gene between color variants (Kang et al., 2011). However, several studies have shown that there is no reproductive isolation and significant species-specific nucleotide polymorphism between color variants (Hu & Li, 2009; Jo et al., 2017). As the genetic distance between color variants (red, black, and green) of A. japonicus was 0.76%, irrespective of their body color, sea cucumbers can be classified as the same species (Sun et al., 2010). Recently, several transcriptomic and metabolomic analyses provided information for the potential molecular mechanisms underlying pigmentation, and color-determining genes and metabolites (Xing et al., 2017, 2018, 2021).

Light is an environmental factor that affects the feeding behavior, growth, and survival of aquatic animals directly or indirectly (Zhou et al., 1999). In addition, appropriate light intensities induced better growth and development of larval and juvenile sea cucumbers, and the photoperiod has diverse effects on sea cucumbers, for example, emerging at night and finding shelter during day-time (Zhang et al., 2006; Dong et al., 2010, 2011; Li et al., 2019). A comparison of juvenile sea cucumbers at different photoperiods showed the highest growth level at 12 h light and 12 h dark condition (Chen et al., 2007). However, further elucidation of the environmental and endogenous factors is required to fully understand the mechanism underlying pigmentation of juvenile sea cucumber. Recently, long-chain acyl-coenzyme A dehydrogenase (LCAD), nuclear distribution C-containing protein 3 (NUDCD3), and receptor tyrosine kinase Tie-1 (TIE1), whose expression levels increase at each pigmentation stage, were suggested to be involved in body color related proteins (Xing et al., 2017). In this study, we investigated the transcript levels of LCAD, NUDCD3, and TIE1 genes in swimming larva and juveniles of A. japonicus to obtain basic information for the relationship between expression of the body color related genes and pigmentation.


1. Sea cucumber larva, light exposure, maintenance, and sampling

In June 2021, the larva and juvenile sea cucumbers used in the experiments were produced by 4 h heat-shock stimulation (24°C from 20°C) of mature female and male sea cucumbers (n=200, mean body weight 200 g) that were separated by body colors (brown and black; Wondeok Fishermen’s Union, Samcheok, Korea). The fertilized eggs, developing embryos, larva, and juveniles were maintained at 21°C with filtered seawater and air supplied using an air blower. Commercial feed of spirulina powder (Shandong, China) and bakers’ yeast (AngelYeast, Hubei, China) was supplied once a day to the swimming larva (until 20 days post-fertilization, dpf) and increased to twice a day (90-dpf) after the juveniles attached. Seawater was changed twice a day using a siphon and overflow during the experimental period.

To examine effect of light on the body color, the larval sea cucumbers were divided into two groups (LED-exposed/ light-shielded) and further reared at 200 L plastic tanks from 30-dpf to 90-dpf. One group was exposed to LED lights (3,000 lx; MB-600S, Mobydick, China) for 10 h in a day (LED-exposed condition, light phase (L): dark phase (D)=10/14 h), and the other group was covered with a PVC board during the experimental period, except for feeding time (light-shielded condition, L:D=0/24 h) (Table 1). The light exposure time was based on the average sunrise/sunset time at Samcheok, Gangwon-do, Korea, June 2021. This study did not require approval by the institution and ethics committee because there are no vertebrate participants.

Table 1. Sampling schedule, sampled larva and juvenile numbers of sea cucumber, Apostichopus japonicus
Sampled date Sampled larva and juvenile number Cumulative LED-exposed days
10L:14D 0L:24D
6-dpf >10,000 NA NA
40-dpf 100-300 10 days NA
50-dpf 100-300 20 days NA
60-dpf 100-300 30 days NA
90-dpf 10-20 60 days NA

dpf, days post-fertilization; NA, not applicable.

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2. cDNA cloning and sequence analysis

Nucleotide sequences for LCAD, NUDCD3, and TIE1 were retrieved using the Chinese Sea Cucumber Database ( According to the sequence information in the database, the primers were designed using the ApE program (A plasmid Editor Version 2.0.36. by M. Wayne Davis) and synthesized by Bioneer (Daejeon, Korea; Table 2). Total RNAs were extracted from the intestines and the respiratory trees of mature sea cucumbers as previously described (Maeng et al., 2019). The LCAD, NUDCD3, and TIE1 cDNAs were amplified by PCR methods using primer sets (Table 2) and LA Taq (Takara, Osaka, Japan) and inserted into pGEM-T Easy vector (Promega, Madison, WI, USA). The PCR cycling conditions for LCAD and TIE1 were as follows: 1 min at 94°C; 35 cycles of 30 s at 94°C, 30 s at 55°C, and 35 s at 72°C; 10 min at 72°C. For NUDCD3, the PCR conditions were as follows: 1 min at 94°C; 32 cycles of 10 s at 98°C and 30 s at 68°C; 10 min at 72°C. PCR products were purified using PCR and/or Gel Purification Kit (Bioneer) and ligated with pGEM-T Easy vector for 24 h at 16°C using T4 DNA ligase (Promega). The pGEM-T Easy vectors containing LCAD, NUDCD3, and TIE1 cDNAs were transformed into DH5 α competent cells and cultured in Luria-Bertani ampicillin medium for 24 h at 37°C. The pGEM-T easy vectors were extracted using a plasmid mini extraction kit (Qiagen, Valencia, CA, USA) and the inserted cDNAs were sequenced by Sanger method (Solgent, Daejeon, Korea). The nucleotide sequences were analyzed using the MultAlin multiple sequence alignment site ( and the ApE program.

Table 2. Oligo primer sequences for PCR and real-time qPCR
Target Direction Sequence (5’-3’) Application

LCAD, long-chain acyl-coenzyme A dehydrogenase; NUDCD3, nuclear distribution C-containing protein 3; TIE1, tyrosine kinase Tie-1.

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3. Real-time qPCR

Total RNAs were extracted from juvenile sea cucumbers sampled at 40-, 50-, and 60-dpf (10, 20, and 30 days after LED exposure) using the RNeasy Mini Kit (Invitrogen, Waltham, MA, USA). To synthesize cDNAs, PrimeScript RT reagent Kit (Takara) was used along with total RNA (1 μg each), 5× gDNA Eraser Buffer, 2 μL of gDNA Eraser (1 μL), and the PCR mixtures including 5× PrimeScript Buffer II, 4 μL PrimeScript RT Enzyme Mix I, 1 μL RT Primer Mix, 1 μL RNase-Free distilled water were reacted for 2 min at 42°C. Reverse transcription was performed for 15 min at 37°C and incubated at 85°C for 5 s to inactivate reverse transcriptase to synthesize cDNAs. qPCR was performed using the QuantStudio™ 7 Flex Real-Time PCR system (Applied Biosystems, Foster City, CA, USA). The primers used in qPCR were designed using Primer Express v3.0 software (Applied Biosystems) and synthesized by Bioneer (Table 2). Using 10 ng of the synthesized cDNA as a template, primers (10 μ M), TB GreenTM Premix EX Taq II (Takara), and ROX Reference Dye II (Takara) were used, and the final qPCR mixture was a two-step qPCR with a volume of 20 μL. qPCR conditions were 95°C for 30 s; 40 cycles of 95°C for 5 s and 60°C for 34 s; 95°C for 15 min and 60°C for 1 min.

4. Whole-mount in situ hybridization (WMISH)

Larval specimens (1.5–9 dpf) were hybridized in situ using a digoxigenin-labeled LCAD and NUDCD3 antisense probes. Detection of mRNA was carried out essentially according to the protocol of Arenas-Mena et al. (2000) and Maeng et al. (2012).

5. Statistical analysis

Statistical significance was evaluated by one-way ANOVA using SPSS software (version 23.0; IBM, Armonk, NY, USA) and Tukey’s post hoc test. In addition, the Student’s t tests were used to compare the expression levels data between the LED-exposed and light-shielded conditions. Differences between the groups were considered significant at p<0.05.


1. Spatial distribution of LCAD and NUDCD3 transcripts in swimming larva

WMISH shows that sea cucumber LCAD and NUDCD3 transcripts are mainly localized to a population of cells in the internal organs of the auricularia larva, such as intestine, although the mRNAs could not be observed clearly (Fig. 1B and C). In addition, the gene expression levels showed increasing tendencies during each development stages of the auricularia larva (Fig. 1D and E).

Fig. 1. Whole-mount in situ hybridization of LCAD and NUDCD3 transcripts in larval sea cucumber, Apostichopus japonicus. (A) Anatomy of auricularia larva (6 days post-fertilization, dpf). (B, D) Expression of the LCAD and (C, E) NUDCD3 mRNAs. Bcc, buccal ciliated cavity; Hs, hyaline sphere; Int, intestine; Oes, Oesophagus; I, 1.5–3 dpf larvae; II, 4–6 dpf larvae; III, 7–9 dpf larvae. LCAD, long-chain acyl-coenzyme A dehydrogenase; NUDCD3, nuclear distribution C-containing protein 3.
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2. Effect of LED-exposure on LCAD, NUDCD3, and TIE1 expression during larval development

In general, the examined LCAD, NUDCD3, and TIE1 transcript levels showed increasing tendencies during larval development stages (6-dpf to 60-dpf) of sea cucumbers. In light-shielded individuals, however, the LCAD, NUDCD3, and TIE1 mRNA were not significantly changed during 40-dpf and 60-dpf stages. At 60-dpf juveniles, the LCAD and TIE1 mRNA levels of LED-exposed individuals were significantly higher than those of light-shielded individuals (p<0.05; Fig. 2A and C). At 40-dpf and 50-dpf juveniles, however, the NUDCD3 mRNA expression levels were significantly higher in light-shielded condition than LED-exposed condition (p<0.05; Fig. 2B).

Fig. 2. Effect of LED-exposure on body color related gene transcripts in sea cucumber, Apostichopus japonicas, larva and juveniles. (A) LCAD, (B) NUDCD3, and (C) TIE1 transcript levels during 6–60 days post-fertilization (dpf) larval stages. (D) LCAD, NUDCD3, and TIE1 transcript levels at 90-dpf juvenile stage which were separated by body colors (G, green; R, red). The LCAD, NUDCD3, and TIE1 transcript levels were analyzed by qPCR as described in Materials and Methods. Different lowercase letters on the bars indicate significantly different values among the groups (p<0.05). Asterisks mean significantly different values between LED-exposed and light-shielded individuals (*p<0.05, **p<0.01, ***p<0.001). L:D=10:14 and L:D=0:24 mean LED-exposed and light-shielded conditions, respectively. LCAD, long-chain acyl-coenzyme a dehydrogenase; NUDCD3, nuclear distribution C-containing protein 3.
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3. Effect of LED-exposure on body color and relationship with LCAD, NUDCD3, and TIE1 expression

In the pigmented juveniles (90-dpf), the LCAD and TIE1 mRNA levels showed higher tendencies in the red individuals than those in green ones, whereas the NUDCD3 mRNA was higher level in the green juveniles (Fig. 2D). In addition, the LCAD mRNA levels were significantly higher in the LED-exposed red individuals compared to the light-shielded ones and the NUDCD3 mRNA level was slightly but significantly higher in the LED-exposed red juveniles (p<0.05).


More than 50 years ago, the body color of sea cucumbers was known to be determined by pigment cells in the dermis layer of the body wall in granule forms (Menton & Eisen, 1970). Among the different color morphs, red, black, and albino are rare and have great appeal to consumers as high-quality traits (Ru et al., 2019). In this study, we examined spatiotemporal expression profiles of the body color related mRNAs, LCAD, NUDCD3, and TIE1 at several developmental and pigmented stages of A. japonicus. In addition, LED-exposed and light-shielded juveniles were applied to the qPCR analysis to better understand the relationships among body color, LED-exposure, and the gene expression levels LCAD, NUDCD3, and TIE1.

In various mammalian melanocytes, tyrosine kinase receptors (RTKs), such as growth factor receptors and TIEs, produce a variety of signals associated with stimulation of proliferation, differentiation, migration, and survival (Zhou et al., 2019). In fact, activation of RTKs by a ligand induced transcription of tyrosinase and melanin synthesis in differentiated melanocytes, and expression of a mutant RTK was associated with lesser pigmentation of melanocytes, suggesting the downregulation of tyrosinases (Luo et al., 1995; Alexeev & Yoon, 2006). In accordance with the mammalian RTKs, we showed that the sea cucumber TIE1 transcript levels were gradually increased at juvenile stage nearby pigmentation period compared to those of the earlier developmental stages, irrespective of LED-exposed condition. Interestingly, the TIE1 gene expression level of LED-exposed sea cucumber juveniles was significantly higher than that of light-shielded juveniles, implying the possible involvement of light in TIE1-meditated pigmentation process.

Melanin is considered as the major pigment widely present in diverse animal phyla, and the variations in melanin formation result in a wide range of body colors including echinoderms (Calestani & Wessel, 2018). In the sea cucumber body, the concentration of melanin pigment was gradually increased with deepening color (Xing et al., 2021). In this study, LCAD expression increased at juvenile stage nearby pigmentation period, suggesting the potential role of LCAD in the synthesis and accumulation of melanin pigments. In 60-dpf juveniles, LED-exposure increased transcript level of LCAD than that of light-shielded sea cucumber, which are similar results for both protein and mRNA levels of LCAD during development of purple sea cucumber (Xing et al., 2017) and upregulation of LCAD protein level in human keratinocytes under radiation condition (Amar et al., 2019). In future studies, fine-tuned examination for diverse light sources and photoperiods are required to better understand the relationship between higher expression level of LCAD and body color of sea cucumber.

In differentially expressed proteins during pigmentation stages of purple sea cucumber, NUDCD3 was classified in two functional groups of melanogenesis and Wnt signaling pathway (Xing et al., 2017). Activation of the Wnt signaling pathway enhanced melanocyte specification at early stages of zebrafish development (Vibert et al., 2017), suggesting a pivotal role of Wnt signaling in regulation of melanocyte differentiation in vertebrates. Interestingly, we observed an increasing pattern of NUDCD3 expression levels in light-shielded 40- and 50-dpf juveniles compared to those of LED-exposed ones, whereas LED-exposure increased the NUDCD3 expression levels at later pigmentation stages. Considering the promoting effect of Wnt signaling in melanocyte development and pigmentation (Schepsky et al., 2006; Wang et al., 2017), it is noteworthy that the Wnt signaling pathway associated with melanin synthesis and regulation in sea cucumbers are likely dependent to light-exposure and developmental stages.

Spatial distribution of LCAD and NUDCD3 transcripts in swimming larva stage was expected to be high in the body surface. Unexpectedly, LCAD and NUDCD3 were shown to be highly expressed in internal organs such as intestine. The spatial gene expression related to the skeletonic mesenchyme lineage in sea cucumber larvae also showed similar patterns with the ingression of skeletogenic pigment cells in sea urchin embryos (McCauley et al., 2012). Thus, it is presumed that genes distributed in internal organs through various metamorphic processes, such as impregnation and rotation, migrate to the body surface and participate in the formation of the skeleton and body color. However, the detailed involvement of LCAD and NUDCD3 genes in pigmentation process of sea cucumbers remains to be further studied. To select and produce high-quality sea cucumbers, further studies are essentially required, such as evaluation of the body color related genes and characterization of pigmentation process in the melanocytes.

Conflict of interests

The authors declare no potential conflict of interest.


We are grateful to Dr. Young Guk Jin, National Institute of Fisheries Science, Korea, and Bangrae Kim, senior researcher, Samcheok Fisheries Resource Center, Korea, and Dr. Jae Ok Kim, Korea National Fishery Products Quality Management Service, Korea, and Hyun Jin Kim, Dept. of Aqualife Medicine, Chonnam National University, Korea, for their comments and critical reading of the manuscript.

Authors’ contributions

Con ceptualization: Kim S, Sohn YC.

Data curation: Kim S, Lee S, Kim GJ, Sohn YC.

Formal analysis: Kim S, Sohn YC.

Methodology: Kim S, Lee S.

Software: Lee S, Sohn YC.

Validation: Kim S, Sohn YC.

Investigation: Kim S, Lee S, Kim GJ, Sohn YC.

Writing-original draft: Kim S, Kim GJ, Sohn YC.

Wr iting-review & editing: Kim S, Lee S, Kim GJ, Sohn YC.

Ethics approval

This article does not require IRB/IACUC approval because there are no human and animal participants.



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