Abstract
Oysters face a complex and changeable environment in the intertidal zone. Heat stress is the main cause of their mass summer deaths. Several important genes are identified to be associated with heat response for oysters. However, regulation of these heat response genes in oysters remains largely unknown. In this study, 27 RNA-seq datasets are used to give a relatively comprehensive of long noncoding RNA (lncRNA) sets for C. gigas. Then, the differential expressed genes and lncRNAs are identified under heat stress. Among all the heat shock proteins (HSPs) and inhibitor of apoptosis proteins (IAPs) in the C. gigas genome, 25 heat shock proteins and 14 IAPs are differential expressed. The Gene Ontology analysis reveals that differential expressed genes (DEGs) are enriched in 6, 7, and 7 GO terms in cellular components, molecular function, and biological process, respectively. Within these terms, cellular response to stimulus is the most abundant term. Furthermore, the potential cis target of the differential expressed lncRNAs (DELs) are predicted to investigate their functions. Of the 394 DELs, there are 80 DELs being found to be corresponded to 113 protein-coding genes. Of them, eight HSPs are found to be regulated by their lncRNA regulators under heat stress. This work provides valuable resource of lncRNA and their regulatory roles under heat stress in C. gigas and gives new insights into adaptive evolution in marine mollusks.
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References
Azlan A, Obeidat SM, Yunus MA, Azzam G (2019) Systematic identification and characterization of Aedes aegypti long noncoding RNAs (lncRNAs). Sci Rep-Uk 9:1–9
Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927
Chapman RW, Mancia A, Beal M, Veloso A, Rathburn C, Blair A, Holland A, Warr G, Didinato G, Sokolova IM (2011) The transcriptomic responses of the eastern oyster, Crassostrea virginica, to environmental conditions. Mol Ecol 20:1431–1449
Cheney D, Elston R, Macdonald B, Kinnan K, Suhrbier A (2001) The roles of environmental stressors and culture methods on the summer mortality of the Pacific oyster Crassostrea gigas. J Shellfish Res 20:1195
Cheng L, Abraham J, Trenberth KE, Fasullo J, Boyer T, Locarnini R, Zhang B, Yu F, Wan L, Chen X (2021) Upper ocean temperatures hit record high in 2020. Springer
Coen LD, Bishop MJ (2015) The ecology, evolution, impacts and management of host–parasite interactions of marine molluscs. J Invertebr Pathol 131:177–211
Farcy VC, Lebel J.-M, Fiévet B (2009) Transcriptional expression levels of cell stress marker genes in the Pacific oyster Crassostrea gigas exposed to acute thermal stress. Cell Stress Chaperones 14:371–380
Feng D, Li Q, Yu H, Kong L, Du S (2018) Transcriptional profiling of long non-coding RNAs in mantle of Crassostrea gigas and their association with shell pigmentation. Sci Rep-Uk 8:1436
Fu H, Jiao Z, Li Y, Tian J, Ren L, Zhang F, Li Q, Liu S (2021) Transient receptor potential (TRP) channels in the Pacific oyster (Crassostrea gigas): genome-wide identification and expression profiling after heat stress between C. gigas and C. angulata. Int J Mole Sci 22:3222
Gagnaire P-A, Lamy J-B, Cornette F, Heurtebise S, Dégremont L, Flahauw E, Boudry P, Bierne N, Lapegue S (2018) Analysis of genome-wide differentiation between native and introduced populations of the cupped oysters Crassostrea gigas and Crassostrea angulata. Genome Biol Evol 10:2518–2534
Guo X, He Y, Zhang L, Lelong C, Jouaux A (2015) Immune and stress responses in oysters with insights on adaptation. Fish Shellfish Immunol 46:107–119
Guo X, Li C, Wang H, Xu Z (2018) Diversity and evolution of living oysters. J Shellfish Res 37:755–772
Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–300
Huang X-D, Dai J-G, Lin K-T, Liu M, Ruan H-T, Zhang H, Liu W-G, He M-X, Zhao M (2018) Regulation of IL-17 by lncRNA of IRF-2 in the pearl oyster. Fish Shellfish Immunol 81:108–112
Hung T, Chang HY (2010) Long noncoding RNA in genome regulation: prospects and mechanisms. RNA Biol 7:582–585
Kapranov P, St Laurent G, Raz T, Ozsolak F, Reynolds CP, Sorensen PH, Reaman G, Milos P, Arceci RJ, Thompson JF (2010) The majority of total nuclear-encoded non-ribosomal RNA in a human cell is ‘dark matter’ un-annotated RNA. BMC Biol 8:1–15
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37:907–915
Lang RP, Bayne CJ, Camara MD, Cunningham C, Jenny MJ, Langdon CJ (2009) Transcriptome profiling of selectively bred Pacific oyster Crassostrea gigas families that differ in tolerance of heat shock. Mar Biotechnol 11:650–668
Laurent GS, Wahlestedt C, Kapranov P (2015) The Landscape of long noncoding RNA classification. Trends Genet 31:239–251
Li A, Li L, Zhang Z, Li S, Wang W, Guo X, Zhang G (2021a) Noncoding variation and transcriptional plasticity promote thermal adaptation in oysters by altering energy metabolism. Mol Biol Evol 38:5144–5155
Li L, Li A, Song K, Meng J, Guo X, Li S, Li C, De Wit P, Que H, Wu F (2018) Divergence and plasticity shape adaptive potential of the Pacific oyster. Nature Ecology & Evolution 2:1751
Li S, Yamada M, Han X, Ohler U, Benfey PN (2016) High-resolution expression map of the Arabidopsis root reveals alternative splicing and lincRNA regulation. Dev Cell 39:508–522
Li Z, Li Q, Liu S, Han Z, Kong L, Yu H (2021b) Integrated analysis of coding genes and non-coding RNAs associated with shell color in the Pacific oyster (Crassostrea gigas). Mar Biotechnol 23:417–429
Liu J, Jung C, Xu J, Wang H, Deng S, Bernad L, Arenas-Huertero C, Chua N-H (2012) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24:4333–4345
Meistertzheim AL, Tanguy A, Moraga D, Thébault MT (2007) Identification of differentially expressed genes of the Pacific oyster Crassostrea gigas exposed to prolonged thermal stress. FEBS J 274:6392–6402
Morris KV, Mattick JS (2014) The rise of regulatory RNA. Nat Rev Genet 15:423–437
Ørom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143:46–58
Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE 7:e30619
Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A (2012) Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22:577–591
Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290
Samain J-F, Degremont L, Soletchnik P, Haure J, Bédier E, Ropert M, Moal J, Huvet A, Bacca H, Van Wormhoudt A (2007) Genetically based resistance to summer mortality in the Pacific oyster (Crassostrea gigas) and its relationship with physiological, immunological characteristics and infection processes. Aquaculture 268:227–243
Song K (2021) Genome-wide patterns of codon usage in the Pacific oyster genome. Journal of Ocean University of China 20:1175–1182
Song K, Wen S, Zhang G (2019). Adaptive evolution patterns in the Pacific oyster Crassostrea gigas. Mar Biotechnol 1–9
Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138
Wilusz JE, Sunwoo H, Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23:1494–1504
Yamashita A, Shichino Y, Yamamoto M (2016) The long non-coding RNA world in yeasts. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms 1859:147–154
Yu H, Zhao X, Li Q (2016) Genome-wide identification and characterization of long intergenic noncoding RNAs and their potential association with larval development in the Pacific oyster. Sci Rep-Uk 6:1–8
Zhang GF, Fang XD, Guo XM, Li L, Luo RB, Xu F, Yang PC, Zhang LL, Wang XT, Qi HG, Xiong ZQ, Que HY, Xie YL, Holland PWH, Paps J, Zhu YB, Wu FC, Chen YX, Wang JF, Peng CF, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang ZY, Zhu QH, Feng Y, Mount A, Hedgecock D, Xu Z, Liu YJ, Domazet-Loso T, Du YS, Sun XQ, Zhang SD, Liu BH, Cheng PZ, Jiang XT, Li J, Fan DD, Wang W, Fu WJ, Wang T, Wang B, Zhang JB, Peng ZY, Li YX, Li N, Wang JP, Chen MS, He Y, Tan FJ, Song XR, Zheng QM, Huang RL, Yang HL, Du XD, Chen L, Yang M, Gaffney PM, Wang S, Luo LH, She ZC, Ming Y, Huang W, Zhang S, Huang BY, Zhang Y, Qu T, Ni PX, Miao GY, Wang JY, Wang Q, Steinberg CEW, Wang HY, Li N, Qian LM, Zhang GJ, Li YR, Yang HM, Liu X, Wang J, Yin Y, Wang J (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54
Zheng Z, Huang R, Tian R, Jiao Y, Du X (2016) Pm-miR-133 hosting in one potential lncRNA regulates RhoA expression in pearl oyster Pinctada martensii. Gene 591:484–489
Zhu X, Chen Y, Zhang Z, Zhao S, Xie L, Zhang R (2020) A species-specific miRNA participates in biomineralization by targeting CDS regions of Prisilkin-39 and ACCBP in Pinctada fucata. Sci Rep-Uk 10:1–12
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This work is supported by the National Natural Science Foundation of China (11701546).
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Song, K. Genome-Wide Identification of Long Non-coding RNAs in Crassostrea gigas and Their Association with Heat Stress. Mar Biotechnol 24, 744–752 (2022). https://doi.org/10.1007/s10126-022-10140-0
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DOI: https://doi.org/10.1007/s10126-022-10140-0