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

Caihui WANG; Fukai WANG; Peican ZHU; Junlin SONG; Min CHEN; Junhao NING; Xia LU; Chunde WANG; Bo LIU

doi:10.1007/s00343-024-3248-0

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

Biology | Updated：2025-08-07

- Multiomics provided insights into the molecular mechanisms underlying black-colored mantle in scallops
- Journal of Oceanology and Limnology Vol. 43, Issue 4, Pages: 1255-1266(2025)
- Affiliations：
  
  1.Qingdao Agricultural University, Qingdao 266109, China
  2.Chinese Academy of Fishery Sciences, Yantai 264003, China
- Author bio：
  
  chundewang2007@163.com
  liubomusic@126.com
- Funds：
- DOI：10.1007/s00343-024-3248-0
  CLC：
- Received：30 May 2024，
  
  Published：01 July 2025
- Accepted：
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WANG Caihui,WANG Fukai,ZHU Peican,et al.Multiomics provided insights into the molecular mechanisms underlying black-colored mantle in scallops[J].Journal of Oceanology and Limnology,2025,43(04):1255-1266.
DOI：

WANG Caihui,WANG Fukai,ZHU Peican,et al.Multiomics provided insights into the molecular mechanisms underlying black-colored mantle in scallops[J].Journal of Oceanology and Limnology,2025,43(04):1255-1266. DOI： 10.1007/s00343-024-3248-0.

摘要

Abstract

In our previous studies

we obtained scallops with black mantles by treating fertilized eggs with EMS (ethylmethane sulfonate) in the

Argopecten

scallop variety “Bohai”. While scallops that are potentially rich in melanin may have higher market values

the mechanisms underlying the occurrence of these black-mantled are largely unknown. We sequenced and compared the transcriptomes and metabolomes of the mantles from the black-mantled “Bohai Red” scallops and those from the scallops with normal-colored (white) mantles. Results reveal that the pigment component in the black mantle of scallops was melanin indeed. Based on the transcriptome data

1 314 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. Several candidate genes associ

ated with black mantle formation in scallops were identified. Among them

the downregulation of monoamine oxidase (

MAO

) and glutathione S-transferases (

GST

) genes and upregulation of cytochrome P450 family 3 subfamily A (

CYP3A

) and protein kinase A (

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

suggesting that the formation of black mantle in scallops may affect physiological functions related to metabolism in scallops. This study provided new evidence for understanding the mechanisms of coloration in scallop tissues

which eventually benefit the selection of new scallop strain with high melanin content.

关键词

Keywords

references

Ahmed B , De Boeck C , Dumont A et al . 2017 . First experimental evidence for the transmission of Chlamydia psittaci in poultry through eggshell penetration . Transboundary and Emerging Diseases , 64 ( 1 ): 167 - 170 , https://doi.org/10.1111/tbed.12358 https://doi.org/10.1111/tbed.12358 .

Alfnes F , Guttormsen A G , Steine G et al . 2006 . Consumers' willingness to pay for the color of salmon: a choice experiment with real economic incentives . American Journal of Agricultural Economics , 88 ( 4 ): 1050 - 1061 , https://doi.‍org/10.1111/j.‍1467-8276.2006.00915.x https://doi.‍org/10.1111/j.‍1467-8276.2006.00915.x . https://do 10.1111/j.1467-8276.2006.00915.x http://dx.doi.org/10.1111/j.1467-8276.2006.00915.x

Ashburner M , Ball C A , Blake J A et al . 2000 . Gene ontology: tool for the unification of biology . Nature Genetics , 25 ( 1 ): 25 - 29 , https://doi.‍org/10.1038/75556 https://doi.‍org/10.1038/75556 . https://do 10.1038/75556 http://dx.doi.org/10.1038/75556

Azam M S , Kwon M , Choi J et al . 2018 . Sargaquinoic acid ameliorates hyperpigmentation through cAMP and ERK-mediated downregulation of MITF in α-MSH-stimulated B 16 F 10 cells. Biomedicine & Pharmacotherapy , 104 : 582 - 589 , https://doi.org/10.1016/j.biopha.2018.05.083 https://doi.org/10.1016/j.biopha.2018.05.083 .

Chan C F , Huang C C , Lee M Y et al . 2014 . Fermented broth in tyrosinase- and melanogenesis inhibition . Molecules , 19 ( 9 ): 13122 - 13135 , https://doi.org/10.3390/molecules190913122 https://doi.org/10.3390/molecules190913122 .

Chen Y X , Chen Y S , Shi C M et al . 2018 . SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data . GigaScience , 7 ( 1 ): gix 120 , https://doi.org/10.1093/gigascience/gix120 https://doi.org/10.1093/gigascience/gix120 .

Cordero R J B , Casadevall A . 2020 . Melanin . Current Biology , 30 ( 4 ): R142 - R143 , https://doi.org/10.1016/j.cub.2019.12.042 https://doi.org/10.1016/j.cub.2019.12.042 .

Grosse C , Heinekamp T , Kniemeyer O et al . 2008 . Protein kinase A regulates growth, sporulation, and pigment formation in Aspergillus fumigatus . Applied and Environmental Microbiology , 74 ( 15 ): 4923 - 4933 , https://doi.org/10.1128/AEM.00470-08 https://doi.org/10.1128/AEM.00470-08 .

Hao S X , Hou X , Wei L et al . 2015 . Extraction and identification of the pigment in the adductor muscle scar of Pacific oyster Crassostrea gigas . PLoS One , 10 ( 11 ): e 0142439 , https://doi.org/10.1371/journal.pone.0142439 https://doi.org/10.1371/journal.pone.0142439 .

He C . 2019 . The Study of Retinoic Acid Regulating Tyrosinase Expression in Crassostrea Gigas . MA thesis. Ludong University, Yantai, China . (in Chinese with English abstract)

Hu M , Liu C , Zhang M et al . 2014 . Alteration of cytochrome P450s activity under diabetic conditions and its impact on the development of diabetes mellitus . Journal of China Pharmaceutical University , 45 ( 2 ): 153 - 160 , https://jcpu.‍cpu.‍edu.‍cn/en/article/doi/10.‍11665/j.‍issn.‍1000-5048.20140204. https://jcpu.‍cpu.‍edu.‍cn/en/article/doi/10.‍11665/j.‍issn.‍1000-5048.20140204. (in Chinese with English abstract)

Hu Z , Song H , Zhou C et al . 2020 . De novo assembly transcriptome analysis reveals the preliminary molecular mechanism of pigmentation in juveniles of the hard clam Mercenaria mercenaria . Genomics , 112 ( 5 ): 3636 - 3647 , https://doi.org/10.1016/j.ygeno.2020.04.020 https://doi.org/10.1016/j.ygeno.2020.04.020 .

Iyengar B , Misra R S . 1988 . Neural differentiation of melanocytes in vitiliginous skin . Acta Anat (Basel) , 133 ( 1 ): 62 - 5 , https://doi.org/10.1159/000146616 https://doi.org/10.1159/000146616 .

Jian D , Jiang D J , Su J et al . 2011 . Diethylstilbestrol enhances melanogenesis via cAMP-PKA-mediating up-regulation of tyrosinase and MITF in mouse B16 melanoma cells . Steroids , 76 ( 12 ): 1297 - 1304 , https://doi.org/10.1016/j.steroids.2011.06.008 https://doi.org/10.1016/j.steroids.2011.06.008 .

Jiang S F . 2018 . Studies on the Influencing Factors and Related Genes of Melanin Formation in Rhizoctonia solani AG-1 IA. PhD dissertation. South China Agricultural University, Guangzhou, China . (in Chinese with English abstract)

Kanehisa M . 2002 . The KEGG database . In: Bock G, Goode J A eds. 'In Silico' Simulation of Biological Processes: Novartis Foundation Symposium . John Wiley & Sons , England . 247 : 91 - 101 . https://do 10.1002/0470857897.ch8 http://dx.doi.org/10.1002/0470857897.ch8

Kanehisa M , Goto S , Kawashima S et al . 2004 . The KEGG resource for deciphering the genome . Nucleic Acids Research , 32 ( S1 ): D277 - D280 , https://doi.org/10.1093/nar/gkh063 https://doi.org/10.1093/nar/gkh063 .

Kim D , Langmead B , Salzberg S L . 2015 . HISAT: a fast spliced aligner with low memory requirements . Nature Methods , 12 ( 4 ): 357 - 360 , https://doi.‍org/10.1038/nmeth.3317 https://doi.‍org/10.1038/nmeth.3317 . https://do 10.1038/nmeth.3317 http://dx.doi.org/10.1038/nmeth.3317

Langmead B . 2010 . Aligning short sequencing reads with Bowtie . Current Protocols in Bioinformatics , 11 ( 7 ): 1 - 14 , https://doi.org/10.1002/0471250953.bi1107s32 https://doi.org/10.1002/0471250953.bi1107s32 .

Li B , Dewey C N . 2011 . RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome . BMC Bioinformatics , 12 ( 1 ): 323 , https://doi.org/10.1186/1471-2105-12-323 https://doi.org/10.1186/1471-2105-12-323 .

Li M , Tang J Y , Yuan M Q et al . 2023a . Outer fold is sole effective tissue among three mantle folds with regard to oyster shell colour. International Journal of Biological Macromolecules , 241 : 124655 , https://doi.org/10.1016/j.ijbiomac.2023.124655 https://doi.org/10.1016/j.ijbiomac.2023.124655

Li Z Z , Li Q , Xu C X et al . 2023b . Histological, elemental, and ultrastructural analysis of melanin in mantle of Pacific oyster ( Crassostrea gigas ) . Microscopy Research & Technique , 86 ( 3 ): 283 - 293 , https://doi.org/10.1002/jemt.24269 https://doi.org/10.1002/jemt.24269 .

Lin J Y , Fisher D E . 2007 . Melanocyte biology and skin pigmentation . Nature , 445 ( 7130 ): 843 - 850 , https://doi.org/10.1038/nature05660 https://doi.org/10.1038/nature05660 .

Liu X , Li C , Chen M et al . 2020 . Draft genomes of two Atlantic bay scallop subspecies Argopecten irradians irradians and A . i . concentricus . Scientific Data , 7 ( 1 ): 99 , https://doi.org/10.6084/m9.figshare.11961984 https://doi.org/10.6084/m9.figshare.11961984 .

Love M I , Huber W , Anders S . 2014 . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 . Genome Biology , 15 ( 12 ): 550 , https://doi.org/10.1186/s13059-014-0550-8 https://doi.org/10.1186/s13059-014-0550-8 .

Lu M Y . 2009 . Inhibition of reduced glutathione and antiscorbutic acid on tyrosinase activity . Chinese Journal of Biochemical Pharmaceutics . 30 ( 2 ): 95 - 98 , 102 , https://api.semanticscholar.org/CorpusID:87709246. https://api.semanticscholar.org/CorpusID:87709246. (in Chinese with English abstract)

Ma D Y . 2013 . Mechanism of Albinism in Sea Cucumber Apostichous Japonicus and Characterization of Body Color Separation Albino Offspring Based on High Throughput Sequencing. PhD dissertation. University of Chinese Academy of Sciences, Qingdao, China . (in Chinese with English abstract) . https://do 10.1007/s11802-014-2297-y http://dx.doi.org/10.1007/s11802-014-2297-y

Maiani G , Castón M J P , Catasta G et al . 2009 . Carotenoids: actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans . Molecular Nutrition & Food Research , 53 ( S2 ): S194 - S218 , https://doi.org/10.1002/mnfr.200800053 https://doi.org/10.1002/mnfr.200800053 .

Mehrabi R , Kema G H J . 2006 . Protein kinase A subunits of the ascomycete pathogen Mycosphaerella graminicola regulate asexual fructification, filamentation, melanization and osmosensing . Molecular Plant Pathology , 7 ( 6 ): 565 - 577 , https://doi.org/10.1111/j.1364-3703.2006.00361.x https://doi.org/10.1111/j.1364-3703.2006.00361.x .

Park E S , Kim S Y , Na J I et al . 2007 . Glutathione prevented dopamine-induced apoptosis of melanocytes and its signaling . Journal of Dermatological Science , 47 ( 2 ): 141 - 149 , https://doi.org/10.1016/j.jdermsci.2007.03.009 https://doi.org/10.1016/j.jdermsci.2007.03.009 .

Patil S , Sistla S , Bapat V et al . 2018 . Melanin-mediated synthesis of silver nanoparticles and their affinity towards tyrosinase . Applied Biochemistry and Microbiology , 54 ( 2 ): 163 - 172 , https://doi.org/10.1134/S0003683818020096 https://doi.org/10.1134/S0003683818020096 .

Rzepka Z , Buszman E , Beberok A et al . 2016 . From tyrosine to melanin: signaling pathways and factors regulating melanogenesis . Postepy Higieny I Medycyny Doswiadczalnej , 70 : 695 - 708 , https://doi.org/10.5604/17322693.1208033 https://doi.org/10.5604/17322693.1208033 .

Sato K , Morita M , Ichikawa C et al . 2008 . Depigmenting mechanisms of all-trans retinoic acid and retinol on B16 melanoma cells . Bioscience, Biotechnology, and Biochemistry , 72 ( 10 ): 2589 - 2597 , https://doi.org/10.1271/bbb.80279 https://doi.org/10.1271/bbb.80279 .

Simon J D , Peles D , Wakamatsu K et al . 2009 . Current challenges in understanding melanogenesis: bridging chemistry, biological control, morphology, and function . Pigment Cell & Melanoma Research , 22 ( 5 ): 563 - 579 , https://doi.org/10.1111/j.1755-148X.2009.00610.x https://doi.org/10.1111/j.1755-148X.2009.00610.x .

Tian S M , Pan L Q , Zhang H . 2014 . Identification of a CYP3A-like gene and CYPs mRNA expression modulation following exposure to benzo [a ] pyrene in the bivalve mollusk Chlamys farreri. Marine Environmental Research , 94 : 7 - 15 , https://doi.org/10.1016/j.marenvres.2013.11.001 https://doi.org/10.1016/j.marenvres.2013.11.001 .

Toda T , Cameron S , Sass P et al . 1987 . Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase . Cell , 50 ( 2 ): 277 - 287 , https://doi.org/10.1016/0092-8674(87)90223-6 https://doi.org/10.1016/0092-8674(87)90223-6 .

Tran-Ly A N , Reyes C , Schwarze F W M R et al . 2020a . Microbial production of melanin and its various applications . World Journal of Microbiology and Biotechnology , 36 ( 11 ): 170 , https://doi.org/10.1007/s11274-020-02941-z https://doi.org/10.1007/s11274-020-02941-z .

Tran-Ly A N , Ribera J , Schwarze F W M R et al . 2020b . Fungal melanin-based electrospun membranes for heavy metal detoxification of water . Sustainable Materials and Technologies , 23 : e 00146 , https://doi.org/10.1016/j.susmat.2019.e00146 https://doi.org/10.1016/j.susmat.2019.e00146 .

Trapnell C , Williams B A , Pertea G et al . 2010 . Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation . Nature Biotechnology , 28 ( 5 ): 511 - 515 , https://doi.org/10.1038/nbt.1621 https://doi.org/10.1038/nbt.1621 .

Wang C D , Liu B , Liu X et al . 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 , https://doi.org/10.1016/j.aquaculture.2017.05.045 https://doi.org/10.1016/j.aquaculture.2017.05.045 .

Wang C H , Liu B , Chen M et al . 2022 Mutations in Growth-related genes induced by EMS treatment in scallops . Frontiers in Genetics , 13 : 879844 , https://doi.org/10.3389/fgene.2022.879844 https://doi.org/10.3389/fgene.2022.879844 .

Wang J S , Zhou H H . 1998 . Molecular mechanisms of CYP3A gene expression and regulation . Progress in Physiological Sciences , 29 ( 2 ): 173 - 176 . (in Chinese)

Wang Q . 2011 . The Mechanism of Catalytic Subunit of cAMP-Dependent Protein Kinase A Regulating Pathogenicity of Setosphaeria turcica . MA thesis. Agricultural University of Hebei . Baoding, China . p.‍ 26 - 30 . (in Chinese with English abstract)

Williams S T . 2017 . Molluscan shell colour . Biological Reviews , 92 ( 2 ): 1039 - 1058 , https://doi.org/10.1111/brv.12268 https://doi.org/10.1111/brv.12268 .

Xie C , Mao X Z , Huang J J et al . 2011 . KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases . Nucleic Acids Research , 39 ( S2 ): W316 - W322 , https://doi.org/10.1093/nar/gkr483 https://doi.org/10.1093/nar/gkr483 .

Yan J , Tian J . 2014 . The study of the relationship between GSTM1 gene deletion and the onset of senile cataract . China & Foreign Medical Treatment , 27 ): 53 - 54 , https://doi.org/10.3969/j.issn.1674-0742.2014.27.025. https://doi.org/10.3969/j.issn.1674-0742.2014.27.025. (in Chinese with English abstract

Yu W C , He C , Cai Z Q et al . 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 , https://doi.org/10.3389/fphys.2017.00699 https://doi.org/10.3389/fphys.2017.00699 .

Zhang L , Li X , Li N et al . 2018 . Correlation analysis of carotenoid concentration and the growth traits of 'Haida golden scallop' . Periodical of Ocean University of China , 48 ( 3 ): 41 - 47 , https://doi.org/10.16441/j.cnki.hdxb.20170188. https://doi.org/10.16441/j.cnki.hdxb.20170188. (in Chinese with English abstract)

Zhao M J , Hu J J , Ni H et al . 2019 . Research progress in melanogenesis signaling pathway . Chinese Journal of Biotechnology , 35 ( 9 ): 1633 - 1642 , https://doi.org/10.13345/j.cjb.190084. https://doi.org/10.13345/j.cjb.190084. (in Chinese with English abstract)

Zheng H P , Liu H L , Chen X Q et al . 2015 . The magnificent ctenophore scallop "Nan'ao Golden Scallop ". China Fisheries , 10 : 57 - 58 . (in Chinese)

Zhu X Q , Huang X S , Zheng Y F et al . 1992 . The effects of cauliflower juice on glutathione s-transferase, glutathione and cytochrome P450 in the liver of rat . Carcinogenesis, Teratogenesis & Mutagenesis , 4 ( 5 ): 26 - 29 , https://doi.org/10.3969/j.issn.1004-616x.1992.05.007. https://doi.org/10.3969/j.issn.1004-616x.1992.05.007. (in Chinese with English abstract)

Zhu Y J , Li Q , Yu H et al . 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 ( 5 ): 777 - 789 , https://doi.org/10.1007/s10126-021-10063-2 https://doi.org/10.1007/s10126-021-10063-2 .

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