Single-molecule long-read (SMRT) transcriptome sequencing of Mercenaria mercenaria reveals a powerful anti-apoptotic system critical for air exposure endurance

Cannuel, R., Beninger, P.G., McCombie, H., Boudry, P., 2009. Gill development and its functional and evolutionary implications in the blue mussel Mytilus edulis (Bivalvia: Mytilidae). Biol. Bull. 217 (2), 173–188. Chwieralski, 2006, Cathepsin-regulated apoptosis, Apoptosis, 11, 143, 10.1007/s10495-006-3486-y Deveraux, 1999, IAP family proteins - suppressors of apoptosis, Genes Dev., 13, 239, 10.1101/gad.13.3.239 Ertl, 2016, Transcriptome analysis of the Sydney rock oyster, Saccostrea glomerata: insights into molluscan immunity, PLoS One, 11, 10.1371/journal.pone.0156649 Estevez-Calvar, 2013, Genes of the mitochondrial apoptotic pathway in Mytilus galloprovincialis, PLoS One, 8, 10.1371/journal.pone.0061502 Fabbri, 2008, HSP expression in bivalves, Invertebr. Surviv. J., 5 Feig, 2007, How apoptosis got the immune system in shape, Eur. J. Immunol., 37, S61, 10.1002/eji.200737462 Gaitanaki, 2004, Various stressors rapidly activate the p38-MAPK signaling pathway in Mytilus galloprovincialis (lam.), Mol. Cell. Biochem., 260, 119, 10.1023/B:MCBI.0000026064.73671.91 He, 2015, Transcriptome analysis reveals strong and complex antiviral response in a mollusc, Fish & Shellfish Immunology, 46, 131, 10.1016/j.fsi.2015.05.023 Huan, 2012, Transcriptomic analysis of the clam Meretrix meretrix on different larval stages, Mar. Biotechnol., 14, 69, 10.1007/s10126-011-9389-0 Jia, 2018, SMRT sequencing of full-length transcriptome of flea beetle Agasicles hygrophila (Selman and Vogt), Sci. Rep., 8, 10.1038/s41598-018-20181-y Kefaloyianni, E., Gourgou, E., Ferle, V., Kotsakis, E., Gaitanaki, C., Beis, I., 2005. Acute thermal stress and various heavy metals induce tissue-specific pro- or anti-apoptotic events via the p38-MAPK signal transduction pathway in Mytilus galloprovincialis (lam.). J. Exp. Biol. 208 (23), 4427–4436. Kiss, 2010, Apoptosis and its functional significance in molluscs, Apoptosis, 15, 313, 10.1007/s10495-009-0446-3 Kuchel, 2010, Immunosuppressive effects of environmental stressors on immunological function in Pinctada imbricata, Fish & Shellfish Immunology, 29, 930, 10.1016/j.fsi.2010.07.033 Kuchel, R.P., Nair, S., Raftos, D.A., 2012. Changes in the transcriptional expression of oxidative stress response genes in Akoya pearl oysters (Pinctada fucata) exposed to air and mechanical agitation. Aquaculture 362, 33–38. Kuida, 2000, Caspase-9, International Journal of Biochemistry & Cell Biology, 32, 121, 10.1016/S1357-2725(99)00024-2 Li, 2012, Acclimation-dependent expression of heat shock protein 70 in Pacific abalone (Haliotis discus hannai Ino) and its acute response to thermal exposure, Chin. J. Oceanol. Limnol., 30, 146, 10.1007/s00343-012-1026-x Li, 2014, PLEK: a tool for predicting long non-coding RNAs and messenger RNAs based on an improved k-mer scheme, Bmc Bioinformatics, 15, 311, 10.1186/1471-2105-15-311 Li, Y.X., Zhang, L.L., Qu, T., Tang, X.Y., Li, L., Zhang, G.F., 2017. Conservation and divergence of mitochondrial apoptosis pathway in the Pacific oyster, Crassostrea gigas. Cell Death Dis. 8. Liu, 2018, The genome of the golden apple snail Pomacea canaliculata provides insight into stress tolerance and invasive adaptation, Gigascience, 7, 10.1093/gigascience/giy101 Menzel, 2010, Quahog clams and their possible mariculture, J. World Aquacult. Soc., 2, 21 Miller, 1999, An exegesis of IAPs: salvation and surprises from BIR motifs, Trends Cell Biol., 9, 323, 10.1016/S0962-8924(99)01609-8 Qian, Z.-J., Kim, S.-A., Lee, J.S., Kim, H.-J., Choi, I.L.W., Jung, W.-K., 2012. The antioxidant and anti-inflammatory effects of abalone intestine digest, Haliotis discus hannai in RAW 264.7 macrophages. Biotechnol. Bioprocess Eng. 17 (3), 475–484. Roberts, 2013, The advantages of SMRT sequencing, Genome Biol., 14, 10.1186/gb-2013-14-6-405 Romero, 2015, The complexity of apoptotic cell death in mollusks: an update, Fish & Shellfish Immunology, 46, 79, 10.1016/j.fsi.2015.03.038 Saleem, 2013, Inhibitors of apoptotic proteins: new targets for anticancer therapy, Chem. Biol. Drug Des., 82, 243, 10.1111/cbdd.12176 Tilgner, 2014, Defining a personal, allele-specific, and single-molecule long-read transcriptome, Proc. Natl. Acad. Sci. U. S. A., 111, 9869, 10.1073/pnas.1400447111 Venier, 2006, Development of mussel mRNA profiling: can gene expression trends reveal coastal water pollution?, Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 602, 121, 10.1016/j.mrfmmm.2006.08.007 Wang, 2001, The expanding role of mitochondria in apoptosis, Genes Dev., 15, 2922 Wang, K.L., Espinosa, E.P., Tanguy, A., Allam, B., 2016. Alterations of the immune transcriptome in resistant and susceptible hard clams (Mercenaria mercenaria) in response to Quahog Parasite Unknown (QPX) and temperature. Fish & Shellfish Immunology 49, 163–176. Xing, Q., Yu, Q., Dou, H.Q., Wang, J., Li, R.J., Ning, X.H., Wang, R.J., Wang, S., Zhang, L.L., Hu, X.L., Sao, Z.M., 2016. Genome-wide identification, characterization and expression analyses of two TNFRs in yesso scallop (Patinopecten yessoensis) provide insight into the disparity of responses to bacterial infections and heat stress in bivalves. Fish & Shellfish Immunology 52, 44–56. Xu, 2015, Histological, ultrastructural and heat shock protein 70 (HSP70) responses to heat stress in the sea cucumber Apostichopus japonicus, Fish & Shellfish Immunology, 45, 321, 10.1016/j.fsi.2015.04.015 Yang, 2000, The IAP family: endogenous caspase inhibitors with multiple biological activities, Cell Res., 10, 169, 10.1038/sj.cr.7290046 Zhang, 2012, Molecular cloning, characterization and expression of heat shock protein 70 gene from the oyster Crassostrea hongkongensis responding to thermal stress and exposure of Cu2+ and malachite green, Gene, 497, 172, 10.1016/j.gene.2012.01.058 Zhang, 2011, Gene discovery, comparative analysis and expression profile reveal the complexity of the Crassostrea gigas apoptosis system, Dev. Comp. Immunol., 35, 603, 10.1016/j.dci.2011.01.005 Zhang, 2012, The oyster genome reveals stress adaptation and complexity of shell formation, Nature, 490, 49, 10.1038/nature11413 Zhang, L.L., Hou, R., Su, H.L., Hu, X.L., Wang, S., Bao, Z.M., 2012b. Network analysis of oyster transcriptome revealed a cascade of cellular responses during recovery after heat shock. PLoS One 7 (4). Zhang, 2014, Transcriptome analysis reveals a rich gene set related to innate immunity in the eastern oyster (Crassostrea virginica), Mar. Biotechnol., 16, 17, 10.1007/s10126-013-9526-z Zhang, G., Li, L., Meng, J., Qi, H., Qu, T., Xu, F., Zhang, L., 2016. Molecular basis for adaptation of oysters to stressful marine intertidal environments, in: H.A. Lewin, R.M. Roberts (Eds.), Annual Review of Animal Biosciences vol. 4 (1), 357–381. Zhao, X.L., Yu, H., Kong, L.F., Li, Q., 2012. Transcriptomic responses to salinity stress in the Pacific oyster Crassostrea gigas. PLoS One 7 (9). Zhou, 2019, Oxidative stress, apoptosis activation and symbiosis disruption in giant clam Tridacna crocea under high temperature, Fish & Shellfish Immunology, 84, 451, 10.1016/j.fsi.2018.10.033 Zhu, 2016, Expression characterization of stress genes under high and low temperature stresses in the Pacific oyster, Crassostrea gigas, Mar. Biotechnol., 18, 176, 10.1007/s10126-015-9678-0