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Articles

Transcriptome analysis of mantle and pearl sac of freshwater pearl mussel Lamellidens marginalis to identify biomineralisation-associated genes

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Pages 107-117 | Received 13 Jul 2023, Published online: 06 Mar 2024

References

  • Andrews, S. (2010). FastQC: a quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. [Accessed 18 February 2024].
  • Bahn, S.Y., Jo, B.H., Choi, Y.S. & Cha, H.J. (2017) Control of nacre biomineralization by Pif80 in pearl oyster. Science Advances 3, e1700765.
  • Bai, Z., Zheng, H., Lin, J., Wang, G. & Li, J. (2013) Comparative analysis of the transcriptome in tissues secreting purple and white nacre in the pearl mussel Hyriopsis cumingii. PLoS One 8, e53617.
  • Barclay, A.N. (2003) Membrane proteins with immunoglobulin-like domains—a master superfamily of interaction molecules. Seminars in Immunology 15, 215–223. doi:10.1016/S1044-5323(03)00047-2.
  • Blank, S., Arnoldi, M., Khoshnavaz, S., Treccani, L., Kuntz, M., Mann, K. et al. (2003) The nacre protein perlucin nucleates growth of calcium carbonate crystals. Journal of Microscopy 212, 280–291.
  • Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. doi:10.1093/bioinformatics/btu170.
  • Carroll, J., Ding, S., Fearnley, I.M. & Walker, J.E. (2013) Post-translational modifications near the quinone binding site of mammalian complex I*. Journal of Biological Chemistry 288, 24799–24808. doi:10.1074/jbc.M113.488106.
  • Cheung, W.Y. (1980) Calmodulin plays a pivotal role in cellular regulation. Science 207, 19–27.
  • Chinkers, M. & Garbers, D.L. (1989) The protein kinase domain of the ANP receptor is required for signaling. Science 245, 1392–1394. doi:10.1126/science.2571188.
  • Fan, W., Hu, Y., Li, C., Xie, L. & Zhang, R. (2008) Cloning, characterization, and expression analysis of calreticulin from pearl oyster Pinctada fucata. Tsinghua Science and Technology 13, 466–473. doi:10.1016/S1007-0214(08)70075-0.
  • Fang, Z., Yan, Z., Li, S., Wang, Q., Cao, W., Xu, G. et al. (2008) Localization of calmodulin and calmodulin-like protein and their functions in biomineralization in P. fucata. Progress in Natural Science 18, 405–412. doi:10.1016/j.pnsc.2007.11.011.
  • Freer, A., S. Bridgett, J. Jiang, and M. Cusack (2014) Biomineral proteins from Mytilus edulis mantle tissue transcriptome. Marine Biotechnology 16, 34–45.
  • Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152. doi:10.1093/bioinformatics/bts565.
  • Funabara, D., Ohmori, F., Kinoshita, S., Koyama, H., Mizutani, S., Ota, A. et al. (2014) Novel genes participating in the formation of prismatic and nacreous layers in the pearl oyster as revealed by their tissue distribution and RNA interference knockdown. PLoS One 9, e84706. doi:10.1371/journal.pone.0084706.
  • Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I. et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644–652. doi:10.1038/nbt.1883.
  • Hanks, S.K. (2003) Genomic analysis of the eukaryotic protein kinase superfamily: a perspective. Genome Biology 4, 111. doi:10.1186/gb-2003-4-5-111.
  • Janakiram, K. (2003) Freshwater pearl culture technology development in India. Journal of Applied Aquaculture 13, 341–349.
  • Jin, C. & Li, J. (2017) The molecular mechanism of pearl biomineralization. Annals of Aquaculture and Research 4, 1032.
  • Joubert, C., Piquemal, D., Marie, B., Manchon, L., Pierrat, F., Zanella-Cléon, I. et al. (2010) Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics 11, 613.
  • Kinoshita, S., Wang, N., Inoue, H., Maeyama, K., Okamoto, K., Nagai, K. et al. (2011) Deep sequencing of ESTs from nacreous and prismatic layer producing tissues and a screen for novel shell formation-related genes in the pearl oyster. PLoS One 6, e21238. doi:10.1371/journal.pone.0021238.
  • Le Luyer, J., Auffret, P., Quillien, V., Leclerc, N., Reisser, C., Vidal-Dupiol, J., & Ky, C.L (2019) Whole transcriptome sequencing and biomineralization gene architecture associated with cultured pearl quality traits in the pearl oyster, Pinctada margaritifera. BMC Genomics 20, 111. doi:10.1186/s12864-019-5443-5.
  • Levi-Kalisman, Y., Falini, G., Addadi, L. & Weiner, S. (2001) Structure of the nacreous organic matrix of a bivalve mollusk shell examined in the hydrated state using cryo-TEM. Journal of Structural Biology 135, 8–17.
  • Lewit-Bentley, A. & Réty, S. (2000) EF-hand calcium-binding proteins. Current Opinion in Structural Biology 10, 637–643. doi:10.1016/S0959-440X(00)00142-1.
  • Li, H., Wang, D., Deng, Z., Huang, G., Fan, S., Zhou, D., Liu, B., Zhang, B. & Yu, D. (2017) Molecular characterization and expression analysis of chitinase from the pearl oyster Pinctada fucata. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 203, 141–148. doi:10.1016/j.cbpb.2016.10.007.
  • Li, S., Xie, L., Zhang, C., Zhang, Y., Gu, M. & Zhang, R. (2004) Cloning and expression of a pivotal calcium metabolism regulator: calmodulin involved in shell formation from pearl oyster (Pinctada fucata). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 138, 235–243. doi:10.1016/j.cbpc.2004.03.012.
  • Liao, Q., Qin, Y., Zhou, Y., Shi, G., Li, X., Li, J., Mo, R., Zhang, Y. & Yu, Z. (2021) Characterization and functional analysis of a chitinase gene: Evidence of Ch-chit participates in the regulation of biomineralization in Crassostrea hongkongensis. Aquaculture Reports 21, 100852. doi:10.1016/j.aqrep.2021.100852.
  • Lin, J.Y., Ma, K.Y., Bai, Z.Y. & Li, J.L. (2013) Molecular cloning and characterization of perlucin from the freshwater pearl mussel, Hyriopsis cumingii. Gene 526, 210–216.
  • Liu, X., W. Guo, C. Jin, Z. Bai, and J. Li (2019) A novel shell matrix protein hic9 from Hyriopsis cumingii involved in the pearl biomineralization. Hyriopsis cumingii. Journal of Fisheries of China 43, 782–789.
  • Liu, X., Yin Jr, Z., Ma Sr, Z., Liang Sr, J., Yao Jr, L. & Zhang Sr, R. (2022) More than 90% of nacre matrix proteins are composed of silk-like proteins. bioRxiv, 2022-09. doi:10.1101/2022.09.07.507049.
  • Marie, B., N. Le Roy, I. Zanella-Cléon, M. Becchi, and F. Marin (2011) Molecular evolution of mollusc shell proteins: insights from proteomic analysis of the edible mussel Mytilus. Journal of Molecular Evolution 72, 531–546.
  • Marie, B., Luquet, G., Bédouet, L., Milet, C., Guichard, N., Medakovic, D. & Marin, F. (2008) Nacre calcification in the freshwater mussel Unio pictorum: Carbonic anhydrase activity and purification of a 95 kDa calcium-binding glycoprotein. ChemBioChem 9, 2515–2523.
  • McDougall, C., Aguilera, F., Moase, P., Lucas, J.S. & Degnan, B.M. (2013) Pearls. Current Biology 23, R671–R673. doi:10.1016/j.cub.2013.05.042.
  • McDougall, C., Aguilera, F., Shokoohmand, A., Moase, P. & Degnan, B.M. (2021) Pearl sac gene expression profiles associated with pearl attributes in the silver-lip pearl oyster, Pinctada maxima. Frontiers in Genetics 11, 597459. doi:10.3389/fgene.2020.597459.
  • Merzendorfer, H. (2011) The cellular basis of chitin synthesis in fungi and insects: common principles and differences. European Journal of Cell Biology 90, 759–769. doi:10.1016/j.ejcb.2011.04.014.
  • Michalak, M., Corbett, E.F., Mesaeli, N., Nakamura, K. & Opas, M. (1999) Calreticulin: one protein, one gene, many functions. Biochemical Journal 344, 281–292.
  • Narasimhulu, K. & Lakshmana Rao, J. (2000) EPR and IR spectral studies of the sea water mussel Mytilus conradinus shells. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 56, 1345–1353. doi:10.1016/S1386-1425(99)00259-0.
  • Nesemann, H., Sharma, S., Sharma, G., Khanal, S.N., Pradhan, B., Shah D.N. & Tachamo, R.D. (2007) Aquatic Invertebrates of the Ganga River System. Vol. 1, (Mollusca, Annelida, Crustacea (in part)). H. Nesemann, Kathmandu, Nepal.
  • Nie, H., Jiang, K., Jiang, L., Huo, Z., Ding, J. & Yan, X. (2020) Transcriptome analysis reveals the pigmentation related genes in four different shell color strains of the Manila clam Ruditapes philippinarum. Genomics 112, 2011–2020. doi:10.1016/j.ygeno.2019.11.013.
  • Patnaik, B.B., Wang, T.H., Kang, S.W., Hwang, H.J., Park, S.Y., Park, E.B. et al. (2016) Sequencing, de novo assembly, and annotation of the transcriptome of the endangered freshwater pearl bivalve, Cristaria plicata, provides novel insights into functional genes and marker discovery. PLoS One 11, e0148622. doi:10.1371/journal.pone.0148622.
  • Pavan-Kumar, A., Varshney, S., Suman, S., Das, R., Chaudhari, A. & Krishna, G. (2022) Complete mitochondrial genome of freshwater pearl mussel Lamellidens marginalis (Lamarck, 1819) and its phylogenetic relation within unionidae family. Molecular Biology Reports 49, 9593–9603. doi:10.1007/s11033-022-07857-5.
  • Pekkarinen, M. & Valovirta, I. (1997) Histochemical and X-ray studies on tissue concretions and shells of Margaritifera margaritifera (Linnaeus). Journal of Shellfish Research 16, 169–178.
  • Shen, W., Hu, Y., He, Z., Xu, S., Xu, X., Zhang, G. & Ren, G. (2020) Histological and comparative transcriptome analyses provide insights into the immune response in pearl sac formation of Hyriopsis cumingii. Frontiers in Marine Science 7, 256. doi:10.3389/fmars.2020.00256.
  • Shi, Y., M. Xu, J. Huang, H. Zhang, W. Liu, Z. Ou, and M. He (2019) Transcriptome analysis of mantle tissues reveals potential biomineralization-related genes in Tectus pyramis Born. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 29, 131–144.
  • Suzuki, M., Sakuda, S. & Nagasawa, H. (2007) Identification of chitin in the prismatic layer of the shell and a chitin synthase gene from the Japanese pearl oyster, Pinctada fucata. Bioscience, Biotechnology, and Biochemistry 71, 1735–1744.
  • Suzuki, M., Saruwatari, K., Kogure, T., Yamamoto, Y., Nishimura, T., Kato, T. & Nagasawa, H. (2009) An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science 325, 1388–1390.
  • Tallant, C., A. Marrero, and F. X. Gomis-Rüth (2010) Matrix metalloproteinases: fold and function of their catalytic domains. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research 1803, 20–28.
  • Taylor, J. & Strack, E. (2008) Pearl production. In: Southgate, P. & Lucas, J. (Eds) The Pearl Oyster. Elsevier, Amsterdam, pp. 273–302. doi:10.1016/B978-0-444-52976-3.00008-5.
  • Varshney, S., Sagwekar, M., Pavan-Kumar, A., Das, R., Gireesh-Babu, P., Chaudhari, A. & Krishna, G. (2020) Development and characterisation of novel polymorphic microsatellite loci in the freshwater mussel Lamellidens marginalis (Lamarck, 1819) using next generation sequencing. Molluscan Research 40, 308–312. doi:10.1080/13235818.2020.1799147.
  • Venkatesan, A., Satin, L.S. & Raghavan, M. (2021) Roles of calreticulin in protein folding, immunity, calcium signaling and cell transformation. In: Agellon, L.B. & Michalak, M. (Eds) Cellular Biology of the Endoplasmic Reticulum. Springer International Publishing, Cham, pp. 145–162. doi:10.1007/978-3-030-67696-4_7.
  • Wang, N. & Huo, Y.X. (2022) Using genome and transcriptome analysis to elucidate biosynthetic pathways. Current Opinion in Biotechnology 75, 102708. doi:10.1016/j.copbio.2022.102708.
  • Wang, X., Liu, Z. & Wu, W. (2017) Transcriptome analysis of the freshwater pearl mussel (Cristaria plicata) mantle unravels genes involved in the formation of shell and pearl. Molecular Genetics and Genomics 292, 343–352. doi:10.1007/s00438-016-1278-9.
  • Weiss, I. (2012) Species-specific shells: chitin synthases and cell mechanics in molluscs. Zeitschrift für Kristallographie-Crystalline Materials 227, 723–738.
  • Weiss, I. M., Kaufmann, S., Mann, K. & Fritz, M. (2000) Purification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc Haliotis laevigata. Biochemical and Biophysical Research Communications 267, 17–21.
  • Wouters, M.A., Rigoutsos, I., Chu, C.K., Feng, L.L., Sparrow, D.B. & Dunwoodie, S.L. (2005) Evolution of distinct EGF domains with specific functions. Protein Science 14, 1091–1103. doi:10.1110/ps.041207005.
  • Yadav, T. & Privman, E. (2019) A comparative analysis of methods for de novo assembly of hymenopteran genomes using either haploid or diploid samples. Scientific Reports 9, 6480. doi:10.1038/s41598-019-42795-6.
  • Yan, Z., Fang, Z., Ma, Z., Deng, J., Li, S., Xie, L. & Zhang, R. (2007) Biomineralization: functions of calmodulin-like protein in the shell formation of pearl oyster. Biochimica et Biophysica Acta (BBA) - General Subjects 1338–1344.
  • Zentz, F., Bédouet, L., Almeida, M., Milet, C., Lopez, E. & Giraud, M. (2001) Characterization and quantification of chitosan extracted from nacre of the abalone Haliotis tuberculata and the oyster Pinctada maxima. Marine Biotechnology 3, 36–44. doi:10.1007/s101260000042.
  • Zhang, G., Fang, X., Guo, X., Li, L., Luo, R., Xu, F. et al. (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490, 49–54. doi:10.1038/nature11413.
  • Zhang, A.J., Liu, S.L. & Zhu, J.Y. (2016) Transcriptome analysis of the freshwater pearl mussel, Hyriopsis cumingii (Lea) using Illumina paired-end sequencing to identify genes and markers. Iranian Journal of Fisheries Science 15, 479–496.
  • Zhang, Y., Meng, Q., Jiang, T., Wang, H., Xie, L. & Zhang, R. (2003) A novel ferritin subunit involved in shell formation from the pearl oyster (Pinctada fucata). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 135, 43–54.
  • Zhao, X., Wang, Q., Jiao, Y., Huang, R., Deng, Y., Wang, H. & Du, X. (2012) Identification of genes potentially related to biomineralization and immunity by transcriptome analysis of pearl sac in pearl oyster Pinctada martensii. Marine Biotechnology 14, 730–739. doi:10.1007/s10126-012-9438-3.
  • Zhu, C., Southgate, P.C. & Li, T. (2019) Production of pearls. In: Smaal, A., Ferreira, J., Grant, J., Petersen, J. & Strand, Ø. (Eds), Goods and Services of Marine Bivalves (pp 73–93). Cham: Springer. doi:10.1007/978-3-319-96776-9_5

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