Multiomics provided insights into the molecular mechanisms underlying black-colored mantle in scallops

doi:10.21203/rs.3.rs-3302702/v1

Download PDF

Research Article

Multiomics provided insights into the molecular mechanisms underlying black-colored mantle in scallops

https://doi.org/10.21203/rs.3.rs-3302702/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Systematic development of genetic breeding should be based on a good understanding of good growth traits, e.g., color traits, which can greatly influence organismal function. Melanin greatly influences the physiological functions of organisms; however, such studies on scallops are scarce. In this study, we collected the black mantle tissues from Bohai Red scallops and sequenced the transcriptome and metabolome, with normal-colored (white) mantle tissues as control (three black and three normal). Our results revealed that the pigment component in the black mantle of scallops was indeed melanin. Based on the transcriptome data, 1314 differentially expressed genes were obtained and subjected to the Gene Ontology (GO) enrichment analysis. The upregulated genes in the black mantle were mainly enriched in transition metal ion binding, hydrolytic enzyme activity, and copper ion binding. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis revealed that the up- and downregulated genes were enriched in different pathways, suggesting that the pathways for the formation of the black mantle were unique. Several candidate genes associated with black mantle formation in scallops were identified. Among them, the downregulation of MAO and GST genes and upregulation of CYP3A and PKA genes may have a positive effect on the formation of black mantle in scallops. The differentially expressed metabolites were mainly enriched in metabolism-related biological pathways. This suggested that the formation of black mantle in scallops may affect physiological functions related to metabolism in scallops.

Therefore, this study revealed several candidate genes related to the formation of black mantle in scallops via multiomics and provided a theoretical basis for breeding scallops with black mantle with high economic value.

Bohai Red Scallop

melanin

transcriptome analysis

metabolomic analysis

enzyme-linked immunosorbent assays

In aquaculture, genetic breeding is aimed at selecting variants with superior traits that are economically important, including attractive appearance, disease resistance, and high survival rate. As the most intuitive phenotypic trait, beautiful and diverse surface color of scallop is one of the factors influencing the preference of consumers and price at seafood market(Alfnes et al., 2006). However, current studies on the pigmentation of scallops are mainly focused on the carotenoids in the soft body(Wenchao et al., 2017), which play roles in eliminating free radicals and supporting the immune system(Maiani et al., 2010). Melanin is one of the most widely distributed biopigments and is generally black or brown in color(Lin and Fisher, 2007). Tyrosinase acts as a phenoloxidase in melanogenesis, regulating the melanin biosynthetic pathway(Simon et al., 2009). A previous study on natural melanin demonstrated that it can regulate a wide spectrum of molecular interactions and metabolic processes, and similar to carotenoids, it functions as an antioxidant and plays a critical role in immune regulation(Chan et al., 2014). Therefore, melanin has applications in cosmetics, functional foods, and other fields(Ahmed et al., 2015).

Bivalve scallops are widely distributed globally and are economically important because of their delicious taste. Much of the pigment-based coloration in Mollusca results from the products of the synthesis pathways of melanin, carotenoid, and tetrapyrrole(Williams, 2017). However, besides some studies on Pacific Oyster (Crassostrea gigas)(Wenchao et al., 2017, Shixin et al., 2015, Zhu et al., 2021), the studies on melanin in scallops are scarce. Better understanding of the molecular mechanisms underlying melanin deposition on the surface of scallops has potential economic value in terms of scallop breeding and evolutionary perspectives

Therefore, in this study, we identified the genes responsible for the coloration of scallop mantle with melanin using multiomic approach and performed their annotation, which would help in the development of genetic breeding of scallops.

Animals

This study was performed on “Bohai Red” scallop, which is a new bay scallop strain selected from the hybrids between the bay scallop and Peruvian scallop. It is widely cultured in northern China(C et al., 2017). The scallops were conditioned to breed and mature in the scallop hatchery of Yantai Spring-Sea AquaSeed Co., Ltd in Laizhou, Shandong, and were cultured in Yangma Island, Mouping, Shandong.

Transcriptome sequencing and analysis

In total, six scallops at the same stage of development were dissected(three black mantle and three white mantle), and their mantle was collected, with using normal-colouredcolored (white) mantle tissuesscallop samples as controls, the transcriptome of black(treated group) and white(control group) mantle tissues was compared. Total RNA was extracted from the tissue(TIANGEN, Beijing, China) and quantified using Nanodrop 2000. The RNA integrity was confirmed using 1% agarose gel electrophoresis. Library construction and high-throughput sequencing were performed using Mouse Genome Informatics (MGI).

Raw data obtained from the sequencing were filtered by removing adapters, unknown nucleotides (> 10%), and low-quality reads (Q-value ≤ 20) and bases (> 50%) using SOAPnuke(Chen et al., 2018). Raw reads were mapped to the scallop genome (BioSample accessions: SAMN08322131(Liu et al., 2020)) using HISAT2(Kim et al., 2015) and Bowtie2(Langmead, 2010). The results obtained from Bowtie2 were statically analyzed using RSEM(Dewey and Bo, 2011), and the gene expression was determined using fragments per kilobase per million bases(Trapnell et al., 2010).

Differentially expressed genes (DEGs) were identified using DESeq2(Love et al., 2014) with |log₂fold change (FC)| > 1 and false discovery rate (FDR) < 0.05. Further, the DEGs were subjected to Gene Ontology (GO)(Ashburner et al., 2000) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses(Kanehisa et al., 2004, Kanehisa, 2002, Chen et al., 2011).

Metabolomic sequencing and analysis

To explore the differentially expressed metabolites, six scallops at the same stage of development were dissected(three black mantle and three white mantle) to collect their mantle which will divided into two groups(black and white). The mantle sample put into a centrifuge tube. To this, 400 µL methanol and some steel beads were added and vortexed for 3 min. If the sample was not completely broken, more steel beads were added and vortexed for 3 min. Further, the sample was sonicated for 10 min on an ice-water bath, followed by incubation at − 20°C for 30 min. Further, the sample was centrifuged at 12,000 rpm and 4°C for 10 min. The supernatants were harvested for subsequent analysis.

Data transformation raw files were converted into mzML format using Proteowizard. Peak extraction, alignment, and retention time correction were performed using the XCMS program. Subsequently, the identified metabolite information was obtained by searching the laboratory’s self-built database, the public database (Metlin), and metDNA. Statistical analysis was performed using R statistical program. Based on OPLS-DA analysis, differentially expressed metabolites were initially screened. Further screening was performed based on p-value < 0.05 and FC ≥ 2 and ≤ 0.5. The differentially expressed metabolites were functionally annotated using KEGG pathway enrichment analysis(Kanehisa et al., 2004).

Estimation of melanin

The black component and its amount in the mantle of scallops were assessed using Shellfish Melanin ELISA Test Kit (Shanghai Yuanjie Biotechnology Centre, Shanghai, China). The mantle obtained from scallops was divided into two groups: black mantle and white mantle, each comprising three replicates. The mantle tissue was homogenized with a high speed tissue grinder(OSE-Y30,TIANGEN,Beijing) in an appropriate volume of physiological saline solution and centrifuged at 3000 rpm for 10 min. The supernatant was collected for subsequent experiments.

ELISA was performed using standard melanin samples at 0, 3, 6, 12, 24, and 48 mg/mL, along with samples and blank wells(0 mg/mL standard melanin samples) as controls, using a 96-well plate. In each standard and sample well, 100 µL of horseradish peroxidase (HRP)-labeled detection antibody was added, and the wells were sealed with sealing membranes and incubated at 37°C for 60 min. After removing the liquid from the wells, the plates were tapped on absorbent paper. To each well, wash buffer was added, incubated for 1 min, and removed by flicking. The plates were tapped dry on an absorbent paper. This washing process was repeated five times. Subsequently, in each well, 50 µL of substrates A and B were added and incubated at 37°C for 15 min in dark. Finally, 50 µL of stop solution was added to each well, and the OD values were determined at 450 nm within 15 min. A standard calibration curve was plotted with the concentrations of the standard samples as the abscissa and their corresponding OD values as the ordinate. Linear regression analysis was performed, and the concentrations of the respective samples were calculated based on the equation derived from the calibration curve.

Estimation of melanin

Melanin content in the mantle of Bohai red scallop, The OD values at 450 nm were determined according to different standard concentrations (Table 1), and the regression curve was plotted as y = 0.032417x + 0.044 (Fig. 1).

The OD values of each of the six coat membrane samples were substituted into the regression curve to obtain the melanin concentration, and the mean value was calculated (Table 2), which proved that the melanin content in the black coat membrane was higher than that in the white coat membrane (Fig. 2).

In this set of data, an independent samples t-test was performed on the melanin concentration in the different coloured coat membranes, and the test for chi-square showed significance = 0.391 > 0.05, indicating chi-square, and the t-test result looked at the first line, significance (two-tailed) = 0.011 < 0.05. The result showed that the difference between the melanin content in the black and the white coat membranes was significant (t = 4.523,p < 0.05 ), the melanin content of the black coat membrane was significantly higher than the melanin content of the white coat membrane (Table 3).

Table 1

OD values of melanin standard at 450 nm
Concentration of melanin standard (mg/mL)	0	3	6	12	24	48
OD value of the standard	0.044	0.123	0.261	0.31	0.921	1.585

Table 2

Melanin concentration in the scallop mantle
	Black mantle		White mantle
Melanin content	OD value	concentration	OD value	concentration
	0.483	67.711386	0.382	52.13314002
	0.528	74.65218867	0.39	53.36706049
	0.469	65.55202517	0.42	57.99426227
Average concentration	69.30519995		54.49815426

Table 3

Comparison of differences in melanin concentration in black and white mantles
Melanin content		Number	Mean	Standard Deviation	t-value
	black	3	69.30519995	4.754831886	4.523^**
	white	3	54.49815426	3.089938258
note: **p < 0.05

Transcriptome sequencing and analysis of DEGs

Transcriptome analysis of the six scallop mantle samples yielded a total of 56.45 Gb of clean data. The mean Q30 value was 90.82%, indicating high sequencing quality. The DEGs were screened using the threshold of |log₂(FC)| > 1 and FDR < 0.05. In total, 1314 DEGs were obtained after filtering, including 461 up- and 853 downregulated genes in black mantle tissue(Fig. 3).

The 461 upregulated genes in the black mantle were subjected to GO enrichment analysis (Fig. 4a). Most genes enriched in biological process were related to cellular and metabolic process; those enriched in cellular component were largely related to cellular anatomical entity, and most genes enriched in molecular function were related to binding and catalytic activity. The 853 downregulated genes were subjected to GO enrichment analysis; however, the genes enriched in cellular component were largely related to cellular anatomical entity (Fig. 4b). Subsequently, we selected 20 most significantly enriched GO terms from the upregulated and downregulated genes and visualized using a bubble chart. It was revealed that the upregulated genes were largely enriched in transition metal ion binding, hydrolase activity, and copper ion binding, whereas the downregulated genes were largely enriched in RNA-directed DNA polymerase activity.

To investigate the relevant pathway in which the DEGs were involved, KEGG pathway enrichment analysis was performed. In total, 20 KEGG pathways with the most significant enrichment were selected (Fig. 5a and b). It was observed that the up- and downregulated genes were enriched in completely different pathways.

Metabolomic sequencing and analysis

Overall, 338 differentially expressed metabolites were identified between the black and white mantles, including 287 metabolites in positive pattern and 51 metabolites in negative pattern. These metabolites were subjected to KEGG pathway enrichment analysis (Fig. 6a and b), which revealed that the changed mantle color (to black) primarily affects the metabolic-related physiological activities of scallops.

In this study, several candidate genes associated with the melanin formation in the black mantle of scallop were identified using a multiomic approach, providing a strong reference for scallop breeding with high economic value.

Previous studies have indicated that melanin synthesis involves multiple pathways(Rzepka et al., 2016). It can be divided into two phases. The first phase is a two-step reaction involving tyrosinases, which catalyze the conversion of tyrosine to L-DOPA and further the oxidation of L-DOPA to DOPA-quinone. The two-step reaction is catalyzed by tyrosinas, here tyrosinases exhibit a unique dual catalytic function. The second phase involves DOPA-quinone as a starting material from two different pathways, the process of eumelanin and melatonin were generated individually. The vast majority of responses in this phase are spontaneous. Therefore, tyrosinase is the key rate-limiting enzyme in melanogenic reaction(Zhao et al., 2019). ws, a tyrosinase-related gene, was highly expressed in Mercenaria mercenaria L. with deep shell color(Hu et al., 2020), indicating that this gene exhibits a certain promotional effect on the deep shell color trait in this organism.

In our study, the MAO gene from tyrosine metabolism pathway was downregulated in black mantle tissue. During melanin synthesis, under the catalytic action of monoamine oxidase (MAO), hydrogen peroxide (H₂O₂) and dopamine (DA) are produced. DA may induce oxidative stress in melanocytes to promote apoptosis(Park et al., 2007). In the skin lesions of vitiligo with decreased pigment content in melanocytes, the activity of DA oxidative enzymes noticeably increased(Iyengar and R.S.Misra, 1988). Therefore, the decreased activity of MOA protects the cell against oxidative injury. In our study, the MAO gene, which has a similar to expressed relationship with DA, exhibited reduced expression in tissues with high melanin content. This is consistent with the previous studies reporting that melanin production is inversely proportional to the DA expression.

Cytochrome P450s (CYP450) is a critical monooxygenase. According to nucleotides in different permutations, CYP450 can be categorized into various enzyme families(Wang, 1998). In this study, DEGs in the black and white mantle tissues were assessed. CYP3A gene was upregulated in the black mantle tissues. A study reported that retinol, via decolonization, exhibits an inhibitory effect on the production of melanin in the murine B16 cells (representative of malignant melanoma)(Sato et al., 2008). In a study on human diabetes, CYP3A gene mediated retinol metabolism in the liver(Xinqiang et al., 1992). Meanwhile, the KEGG database also shows that CYP3A enzyme participates in retinol metabolism. Previous studies have reported that different cytochrome P450 family members of Pacific oyster are upregulated in the black mantle and black muscle. Moreover, these enzymes participate in melanin synthesis as they catalyze the conversion of retinoic acid to retinol. In addition, retinol dehydrogenase can convert retinoic to retinoic acid, and retinoic acid can be done by the increased activities of tyrosinase induced by and promoted melanin production. Therefore, it was proposed that retinol dehydrogenase and cytochrome P450 affect retinoic acid production; more retinoid acid increases the activity of tyrosinase, thus producing more melanin(Hao et al., 2009). It has been demonstrated that upregulation of the retinaldehyde dehydrogenase gene promotes the production of retinoic acid and can upregulate the tyrosinase gene, producing more melanin(Cheng, 2019). This indicates that retinol metabolism plays an important role in the melanogenesis process. Thus, integrating this information, we speculated that environmental stimuli and other factors elevated CYP3A expression, which repressed the synthesis of retinol in scallops promoting melanin synthesis.

Glutathione-S-transferase (GSH) is widely present in organisms, with the highest levels in the liver. This enzyme detoxifies various compounds by binding to reduced GSH. GSH with strong radical scavenging(Mengyue et al., 2014). GSH activated by GST isozymes effectively scavenges free radicals(Yu et al., 2017). Moreover, GSH can inhibit tyrosinase activity through reduction(Ji and Jie, 2014). When the GST gene is downregulated, the inhibitory effect of GSH on tyrosinase is decreased, and the catalytic activity of tyrosinase is significantly enhanced. In this study, the GST gene, which plays a role in the xenobiotic metabolism by cytochrome P450 via various pathways, was downregulated. This was combined with the increased melanin content in the mantle. Therefore, we speculated that downregulation of the GST gene may also have facilitated melanin production, which is consistent with previous studies(Shaofeng, 2018).

In this study, the PKA genes were observed to participate in several different signaling pathways of melanogenesis. In yeast, three genes encoding the catalytic subunit of PKA were identified by Toda et al(Toda et al., 1987). The function of the PKA gene is still debated. For instance, in the wild-type strain of Aspergillus fumigatus, PKA gene induction plays a role in melanin synthesis(Grosse et al., 2008). In Mycosphaerella graminicola, the PKA gene plays a role in melanin formation and osmotic stress tolerance(Mehrabi and Kema, 2006).

In the melanogenesis pathway, PKA binds to cyclic adenosine monophosphate (cAMP) and plays a regulatory role in melanin synthesis(Azam et al., 2018). For instance, diethylstilbestrol can promote the activity of tyrosine kinase through cAMP-PKA pathway in melanogenesis pathway to modulate melanogenesis in B16 cells(Jian et al., 2011). In maize, a decrease in PKA expression was accompanied by decreased expression of melanin transcription factors(Qian, 2011). In addition, when the PKA gene expression is decreased in Apostichous japonicus, melanin synthesis is decreased(Deyou, 2013). In our study, the PKA gene was upregulated in black mantle tissue. This is consistent with the positive correlation of the PKA gene and melanogenesis in the tissues. Therefore, we speculated that the PKA gene is the main factor underlying the black mantle trait in scallops.

Author Contribution

Caihui Wang and Fukai Wang: responsible for implementation of experiments and wrote the articles. Peican Zhu: responsible for writing assistance. Junlin Song: responsible for writing assistance. Min Chen: responsible for providing language help. Junhao Ning: responsible for providing language help. Xia Lu: responsible for writing assistance. Bo Liu and Chunde Wang: designed the experiments and revised the manuscript.

Funding

The study is supported by the Natural Science Foundation of Shandong Province (ZR2020MC192), Agricultural Industrial Technology System in Shandong Province (SDIT-14), Fund for Agriculture Seed Improvement Project of Shandong Province (No. 2020LZGC016), the Scientific and Technological Project of Yantai, Shandong Province (No. 2022XCZX083), and the Science and Technology Innovation Capacity Improvement Project of Shandong Province (2021TSGC1229)

Data availability

The data that has been used is confidential.

Declaration of Competing Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ahmed, B., De Boeck, C., Dumont, A., Cox, E., De Reu, K. & Vanrompay, D. (2015). First Experimental Evidence for the Transmission of Chlamydia psittaci in Poultry through Eggshell Penetration. Transboundary & Emerging Diseases: 3-11.
Alfnes, F., Guttormsen, A.G., Steine, G. & Kolstad, K. (2006). Consumers' Willingness to Pay for the Color of Salmon: A Choice Experiment with Real Economic Incentives. Social Science Electronic Publishing.
Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D. & Cherry, J.M. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics, 25: 25-9.
Azam, M.S., Kwon, M., Choi, J. & Kim, H.R. (2018). Sargaquinoic acid ameliorates hyperpigmentation through cAMP and ERK-mediated downregulation of MITF in alpha-MSH-stimulated B16F10 cells. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie, 104: 582-589. DOI 10.1016/j.biopha.2018.05.083
C, C.W.A., A, B.L., B, X.L., C, B.M.A., A, Y.Z., C, X.Z., A, F.L. & A, G.L. (2017). Selection of a new scallop strain, the Bohai Red, from the hybrid between the bay scallop and the Peruvian scallop. Aquaculture, 479: 250-255.
Chan, C.F., Huang, C.C., Lee, M.Y. & Lin, Y.S. (2014). Fermented broth in tyrosinase- and melanogenesis inhibition. Molecules, 19: 13122-35. DOI 10.3390/molecules190913122
Chen, X., Xizeng, M., Jiaju, H., Yang, D., Jianmin, W., Shan, D., Lei, K., Ge, G., Chuan-Yun, L. & Liping, W. (2011). KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic acids research, 39: 316-22.
Chen, Y., Chen, Y., Shi, C., Huang, Z., Zhang, Y., Li, S., Li, Y., Ye, J., Yu, C., Li, Z., Zhang, X., Wang, J., Yang, H., Fang, L. & Chen, Q. (2018). SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. Gigascience, 7: 1-6. DOI 10.1093/gigascience/gix120
Cheng, H. (2019). The study of retinoic acid regulating tyrosinase expression in Crassostrea gigas.: Ludong University.
Dewey, C.N. & Bo, L. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12: 323-323.
Deyou, M. (2013). Mechanism of albinism in sea cucumber Apostichous japonicus and characterization of body color separation albino offspring based on high throughput sequencing. University of Chinese Academy of Sciences.
Grosse, C., Heinekamp, T., Kniemeyer, O., Gehrke, A. & Brakhage, A.A. (2008). Protein kinase A regulates growth, sporulation, and pigment formation in Aspergillus fumigatus. Applied and environmental microbiology, 74: 4923-33. DOI 10.1128/aem.00470-08
Hao, H., Zhouxiu-Ling & Lumei-Yun (2009). Inhibition of reduced glutathione and antiscorbutic acid on tyrosinase activity. Chinese Journal of Biochemical Pharmaceutics.
Hu, Z., Song, H., Zhou, C., Yu, Z.L., Yang, M.J. & Zhang, T. (2020). De novo assembly transcriptome analysis reveals the preliminary molecular mechanism of pigmentation in juveniles of the hard clam Mercenaria mercenaria. Genomics, 112: 3636-3647. DOI 10.1016/j.ygeno.2020.04.020
Iyengar, B. & R.S.Misra (1988). NeuraI D ifferentiation of MeIanocytes in VitiIiginous Skin. Cells Tissues Organs. DOI https://doi.org/10.1159/000146616
Ji, Y. & Jie, T. (2014). The Study of the Relationship Between GSTM1 Gene Deletion and the Onset of Senile Cataract. China &Foreign Medical Treatment. DOI 10.16662/j.cnki.1674-0742.2014.27.085
Jian, D., Jiang, D., Su, J., Chen, W., Hu, X., Kuang, Y., Xie, H., Li, J. & Chen, X. (2011). Diethylstilbestrol enhances melanogenesis via cAMP-PKA-mediating up-regulation of tyrosinase and MITF in mouse B16 melanoma cells. Steroids, 76: 1297-304. DOI 10.1016/j.steroids.2011.06.008
Kanehisa, M. (2002). The KEGG database. Novartis Foundation symposium, 247: 91-101; discussion 101-3, 119-28, 244-52.
Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y. & Hattori, M. (2004). The KEGG resource for deciphering the genome. Nucleic acids research, 32: D277-80. DOI 10.1093/nar/gkh063
Kim, D., Langmead, B. & Salzberg, S.L. (2015). HISAT: a fast spliced aligner with low memory requirements. 12: 357-60. DOI 10.1038/nmeth.3317
Langmead, B. (2010). Aligning short sequencing reads with Bowtie. Current protocols in bioinformatics, Chapter 11: Unit 11.7. DOI 10.1002/0471250953.bi1107s32
Lin, J. & Fisher, D. (2007). Melanocyte biology and skin pigmentation. Nature, 445: 843-50.
Liu, X., Li, C., Chen, M., Liu, B. & Wang, C. (2020). Draft genomes of two Atlantic bay scallop subspecies Argopecten irradians irradians and A. i. concentricus. Scientific Data, 7.
Love, M.I., Huber, W. & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15: 550.
Maiani, G., Castón, M.J.P., Catasta, G., Toti, E. & Schlemmer, U. (2010). Carotenoids: Actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Molecular Nutrition & Food Research, 53: S194-S218.
Mehrabi, R. & Kema, G.H. (2006). Protein kinase A subunits of the ascomycete pathogen Mycosphaerella graminicola regulate asexual fructification, filamentation, melanization and osmosensing. Molecular plant pathology, 7: 565-77. DOI 10.1111/j.1364-3703.2006.00361.x
Mengyue, H., Can, L., Mian, Z., Nan, H., Li, L. & Xiaodong, L. (2014). Alteration of cytochrome P450s activity under diabetic conditions and its impact on the development of diabetes mellitus. Journal of China Pharmaceutical University. DOI doi: 10． 11665 /j． issn． 1000 － 5048． 20140204
Park, E.S., Kim, S.Y., Na, J.I., Ryu, H.S., Youn, S.W., Kim, D.S., Yun, H.Y. & Park, K.C. (2007). Glutathione prevented dopamine-induced apoptosis of melanocytes and its signaling. Journal of dermatological science, 47: 141-9. DOI 10.1016/j.jdermsci.2007.03.009
Qian, W. (2011). The mechanism of catalytic subunit of cAMP-dependent protein kinase A regulating pathogenicity of Setosphaeria turcica. Hebei Agricultural University.
Rzepka, Z., Buszman, E., Beberok, A. & Wrześniok, D. (2016). From tyrosine to melanin: Signaling pathways and factors regulating melanogenesis. Postepy higieny i medycyny doswiadczalnej (Online), 70: 695-708. DOI 10.5604/17322693.1208033
Sato, K., Morita, M., Ichikawa, C., Takahashi, H. & Toriyama, M. (2008). Depigmenting mechanisms of all-trans retinoic acid and retinol on B16 melanoma cells. Bioscience, biotechnology, and biochemistry, 72: 2589-97. DOI 10.1271/bbb.80279
Shaofeng, J. (2018). Studies on the Influencing Factors and Related Genes of Melanin Formation in Rhizoctonia solani AG-1 IA. South China Agricultural University.
Shixin, Hao, Xin, Hou, Lei, Wei, Jian, Li, Zhonghu & Xiaotong (2015). Extraction and Identification of the Pigment in the Adductor Muscle Scar of Pacific Oyster Crassostrea gigas. PloS one.
Simon, J.D., Peles, D., Wakamatsu, K. & Ito, S. (2009). Current challenges in understanding melanogenesis: bridging chemistry, biological control, morphology, and function. Pigment cell & melanoma research, 22: 563-79. DOI 10.1111/j.1755-148X.2009.00610.x
Toda, T., Cameron, S., Sass, P., Zoller, M. & Wigler, M. (1987). Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell, 50: 277-87. DOI 10.1016/0092-8674(87)90223-6
Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., Baren, M.J.V., Salzberg, S.L., Wold, B.J. & Pachter, L. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology.
Wang, J., S.Zhou,H,H (1998). Molecular mechanisms of CYP3A gene expression and regulation. Progress in Physiological Sciences, 29: 173-176.
Wenchao, Y., Cheng, H., Zhongqiang, C., Fei, X., Lei, W., Jun, C., Qiuyun, J., Na, W., Zhuang, L. & Wen, G. (2017). A Preliminary Study on the Pattern, the Physiological Bases and the Molecular Mechanism of the Adductor Muscle Scar Pigmentation in Pacific Oyster Crassostrea gigas. Frontiers in Physiology, 8: 699-.
Williams, S.T. (2017). Molluscan shell colour. Biological Reviews, 92.
Xinqiang, Z., Xingshu, H., Yifan, Z. & Min, N.Z. (1992). THE EFFECIS OF CAULIFLOWER JUICE ON GLUTATHIONE S-TRANSFERASE,GLUTATHIONE AND CYTOCHROME P450 IN THE LIVER OF RAT. CARCLNOGENESIS TERATOGENESIS & M UTAGENESIS.
Yu, W., He, C., Cai, Z., Xu, F., Wei, L., Chen, J., Jiang, Q., Wei, N., Li, Z., Guo, W. & Wang, X. (2017). A Preliminary Study on the Pattern, the Physiological Bases and the Molecular Mechanism of the Adductor Muscle Scar Pigmentation in Pacific Oyster Crassostrea gigas. Front Physiol, 8: 699. DOI 10.3389/fphys.2017.00699
Zhao, M., Hu, J., Ni, H., Jiang, Z. & Wang, L. (2019). Research progress in melanogenesis signaling pathway. Sheng wu gong cheng xue bao = Chinese journal of biotechnology, 35: 1633-1642. DOI 10.13345/j.cjb.190084
Zhu, Y., Li, Q., Yu, H., Liu, S. & Kong, L. (2021). Shell Biosynthesis and Pigmentation as Revealed by the Expression of Tyrosinase and Tyrosinase-like Protein Genes in Pacific Oyster (Crassostrea gigas) with Different Shell Colors. Marine Biotechnology, 23: 777-789.

No competing interests reported.

Download PDF

Version 1

posted

You are reading this latest preprint version

Multiomics provided insights into the molecular mechanisms underlying black-colored mantle in scallops

Status:

Version 1

Abstract

Figures

Inatroduction

Materials And Methods

RESULTS

Discussion

Declarations

References

Additional Declarations

Status:

Version 1