Abstract
Sepiella japonica is a worldwide marine cuttlefish species of high economic value. S. japonica routinely modifying behaviors in reproductive life, such as rapid aging until death after spawning, has been recognized in artificial breeding. However, reproductive behavior at the level of genes is rarely reported, thus, the research on the genetic basis of behavior, reproduction, and artificial breeding was limited. We applied RNA-seq in different stages of reproduction to investigate the reason of rapid aging after spawning, pre-maturity, pre-spawning after maturity, and post-spawning. The retinoid X receptor (RXR) gene family in S. japonica was identified, and 1 343–1 452 differentially expressed genes (DEGs) in all 3 stages of reproductive life were identified from pairwise mRNA comparisons. Furthermore, through the GO term and KEGG analysis, S. japonica could handle neuronal development and network formation before maturity and have a functional degradation of neural communication, signal transduction, vision, and gene expression after spawning. Eight SjRXRαs have been identified and they played different roles in growth development or reproduction. Therefore, the regulation of several channels and receptors is the intrinsic molecular mechanism of rapid aging after spawning in S. japonica. This study revealed the survival strategy and provided fundamental data on the level of genes for understanding the reproductive behavior and the reproduction of S. japonica.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
6 Data Availability Statement
All data that support the findings of this study are available from the corresponding author on reasonable request.
Change history
22 February 2024
An Erratum to this paper has been published: https://doi.org/10.1007/s00343-024-3299-2
References
Aanes H, Collas P, Aleström P. 2014. Transcriptome dynamics and diversity in the early zebrafish embryo. Briefings in Functional Genomics, 13(2): 95–105, https://doi.org/10.1093/bfgp/elt049.
Altschul S F, Madden T L, Schäffer A A et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic acids research, 25(17): 3389–3402, https://doi.org/10.1093/nar/25.17.3389.
Anderson R C, Wood J B, Byrne R A. 2002. Octopus senescence: the beginning of the end. Journal of Applied Animal Welfare Science, 5(4): 275–283, https://doi.org/10.1207/S15327604JAWS0504_02.
Armingol E, Officer A, Harismendy O et al. 2021. Deciphering cell-cell interactions and communication from gene expression. Nature Reviews Genetics, 22(2): 71–88, https://doi.org/10.1038/s41576-020-00292-x.
Basyuk E, Rage F, Bertrand E. 2021. RNA transport from transcription to localized translation: a single molecule perspective. RNA Biology, 18(9): 1221–1237, https://doi.org/10.1080/15476286.2020.1842631.
Benelli M, Pescucci C, Marseglia G et al. 2012. Discovering chimeric transcripts in paired-end RNA-seq data by using EricScript. Bioinformatics, 28(24): 3232–3239, https://doi.org/10.1093/bioinformatics/bts617.
Berson D M. 2007. Phototransduction in ganglion-cell photoreceptors. Pflügers Archiv: European Journal of Physiology, 454(5): 849–855, https://doi.org/10.1007/s00424-007-0242-2.
Bodnar A G, Coffman J A. 2016. Maintenance of somatic tissue regeneration with age in short- and long-lived species of sea urchins. Aging Cell, 15(4): 778–787, https://doi.org/10.1111/acel.12487.
Bohush A, Leśniak W, Weis S et al. 2021. Calmodulin and its binding proteins in Parkinson’s disease. International Journal of Molecular Sciences, 22(6): 3016, https://doi.org/10.3390/ijms22063016.
Bouton D, Escriva H, De Mendonça R L et al. 2005. A conserved retinoid X receptor (RXR) from the mollusk Biomphalaria glabrata transactivates transcription in the presence of retinoids. Journal of Molecular Endocrinology, 34(2): 567–582, https://doi.org/10.1677/jme.1.01766.
Bradley J, Bönigk W, Yau K W et al. 2004. Calmodulin permanently associates with rat olfactory CNG channels under native conditions. Nature Neuroscience, 7(7): 705–710, https://doi.org/10.1038/nn1266.
Brini M, Calì T, Ottolini D et al. 2014. Neuronal calcium signaling: function and dysfunction. Cellular and Molecular Life Sciences, 71(15): 2787–2814, https://doi.org/10.1007/s00018-013-1550-7.
Bu D C, Luo H T, Huo P P et al. 2021. KOBAS-i: intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Research, 49(W1): W317–W325, https://doi.org/10.1093/nar/gkab447.
Burgerhout E, Minegishi Y, Brittijn S A et al. 2016. Changes in ovarian gene expression profiles and plasma hormone levels in maturing European eel (Anguilla anguilla); Biomarkers for broodstock selection. General and Comparative Endocrinology, 225: 185–196, https://doi.org/10.1016/j.ygcen.2015.08.006.
Butler-Struben H M, Brophy S M, Johnson N A et al. 2018. In vivo recording of neural and behavioral correlates of anesthesia induction, reversal, and euthanasia in cephalopod molluscs. Frontiers in Physiology, 9: 109, https://doi.org/10.3389/fphys.2018.00109.
Chen C J, Chen H, Zhang Y et al. 2020. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13(8): 1194–1202, https://doi.org/10.1016/j.molp.2020.06.009.
Cole C N, Scarcelli J J. 2006. Transport of messenger RNA from the nucleus to the cytoplasm. Current Opinion in Cell Biology, 18(3): 299–306, https://doi.org/10.1016/j.ceb.2006.04.006.
Corrales P, Vidal-Puig A, Medina-Gómez G. 2018. PPARs and metabolic disorders associated with challenged adipose tissue plasticity. International Journal of Molecular Sciences, 19(7): 2124, https://doi.org/10.3390/ijms19072124.
Dawson M I, Xia Z B. 2012. The retinoid X receptors and their ligands. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 1821(1): 21–56, https://doi.org/10.1016/j.bbalip.2011.09.014.
DeLamater J, Friedrich W N. 2002. Human sexual development. Journal of Sex Research, 39(1): 10–14, https://doi.org/10.1080/00224490209552113.
Deryckere A, Styfhals R, Vidal E A G et al. 2020. A practical staging atlas to study embryonic development of Octopus vulgaris under controlled laboratory conditions. BMC Developmental Biology, 20(1): 7, https://doi.org/10.1186/s12861-020-00212-6.
Dong Z Y, Yang H, Guo B Y et al. 2022. Cloning of the sjRXR gene and analysis of its distribution in developmental stages of Sepiella japonica. Journal of Fishery Sciences of China, 29(6): 814–824, https://doi.org/10.12264/JFSC2021-0239. (in Chinese with English abstract)
Du C, Anderson A, Lortie M et al. 2013. Oxidative damage and cellular defense mechanisms in sea urchin models of aging. Free Radical Biology and Medicine, 63: 254–263, https://doi.org/10.1016/j.freeradbiomed.2013.05.023.
Dupont S, Mamidi A, Cordenonsi M et al. 2009. FAM/USP9x, a deubiquitinating enzyme essential for TGFβ signaling, controls Smad4 monoubiquitination. Cell, 136(1): 123–135, https://doi.org/10.1016/j.cell.2008.10.051.
Fesenko E E, Kolesnikov S S, Lyubarsky A L. 1985. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature, 313(6000): 310–313, https://doi.org/10.1038/313310a0.
Finn R D, Clements J, Eddy S R. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research, 39(Web Server issue): W29–W37, https://doi.org/10.1093/nar/gkr367.
Froud R J, Ragan C I. 1984. Cytochrome c-mediated electron transfer between ubiquinol-cytochrome c reductase and cytochrome c oxidase. Kinetic evidence for a mobile cytochrome c pool. The Biochemical Journal, 217(2): 551–560, https://doi.org/10.1042/bj2170551.
Fryxell K J. 1996. The coevolution of gene family trees. Trends in Genetics, 12(9): 364–369, https://doi.org/10.1016/s0168-9525(96)80020-5.
Gleadall I G. 2013. The effects of prospective anaesthetic substances on cephalopods: summary of original data and a brief review of studies over the last two decades. Journal of Experimental Marine Biology and Ecology, 447: 23–30, https://doi.org/10.1016/j.jembe.2013.02.008.
Grasmann G, Smolle E, Olschewski H et al. 2019. Gluconeogenesis in cancer cells—repurposing of a starvation-induced metabolic pathway?. Biochimica et Biophysica Acta (BBA) —Reviews on Cancer, 1872(1): 24–36, https://doi.org/10.1016/j.bbcan.2019.05.006.
Haas B J, Papanicolaou A, Yassour M et al. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols, 8(8): 1494–1512, https://doi.org/10.1038/nprot.2013.084.
Hiraoka S, Ando H, Ban M et al. 1997. Changes in expression of neurohypophysial hormone genes during spawning migration in chum salmon, Oncorhynchus keta. Journal of Molecular Endocrinology, 18(1): 49–55, https://doi.org/10.1677/jme.0.0180049.
Hogg R C, Raggenbass M, Bertrand D. 2003. Nicotinic acetylcholine receptors: from structure to brain function. In: Reviews of Physiology, Biochemistry and Pharmacology 147. Springer, Berlin, Heidelberg. p.1–46, https://doi.org/10.1007/s10254-003-0005-1.
Janesick A, Wu S C, Blumberg B. 2015. Retinoic acid signaling and neuronal differentiation. Annual Review of Physiology, 72(8): 1559–1576, https://doi.org/10.1007/s00018-014-1815-9.
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.
Li H F, Lin S R, Qi P Z et al. 2022a. Proteomic analysis of the spineless cuttlefish Sepiella japonica: exploratory analyses on the phenomenon of death after spawning. Frontiers in Marine Science, 9: 995691, https://doi.org/10.3389/fmars.2022.995691.
Li R Q, Li Y R, Kristiansen K et al. 2008. SOAP: short oligonucleotide alignment program. Bioinformatics, 24(5): 713–714, https://doi.org/10.1093/bioinformatics/btn025.
Li Y, Zeng H Q, Xu F Y et al. 2022b. H+-ATPases in plant growth and stress responses. Annual Review of Plant Biology, 73: 495–521, https://doi.org/10.1146/annurev-arplant-102820-114551.
Lo H F, Chen B E, Lin M G et al. 2016. Gene expression and molecular characterization of a chaperone protein HtpG from Bacillus licheniformis. International Journal of Biological Macromolecules, 85: 179–191, https://doi.org/10.1016/j.ijbiomac.2015.12.080.
Loram J, Bodnar A. 2012. Age-related changes in gene expression in tissues of the sea urchin Strongylocentrotus purpuratus. Mechanisms of Ageing and Development, 133(5): 338–347, https://doi.org/10.1016/jmad.2012.03.012.
Lü, Z M, Liu W, Liu L Q et al. 2016. De novo assembly and comparison of the ovarian transcriptomes of the common Chinese cuttlefish (Sepiella japonica) with different gonadal development. Genomics Data, 7: 155–158, https://doi.org/10.1016/j.gdata.2015.12.011.
Martyniuk C J, Mehinto A C, Colli-Dula R C et al. 2020. Transcriptome and physiological effects of toxaphene on the liver-gonad reproductive axis in male and female largemouth bass (Micropterus salmoides). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 36: 100746, https://doi.org/10.1016/j.cbd.2020.100746.
Mawa Z, Hossain M Y, Hasan M R et al. 2021. First record on size at sexual maturity and optimum catchable length of 10 marine fishes from the Bay of Bengal (Bangladesh) through multi-models approach: a key for sound fisheries management. Environmental Science and Pollution Research, 28(28): 38117–38127, https://doi.org/10.1007/s11356-021-13491-8.
Mengeling B J, Murk A J, Furlow J D. 2016. Trialkyltin rexinoid-X receptor agonists selectively potentiate thyroid hormone induced programs of Xenopus laevis metamorphosis. Endocrinology, 157(7): 2712–2723, https://doi.org/10.1210/en.2016-1062.
Mi H Y, Muruganujan A, Thomas P D. 2013. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Research, 41(Database issue): D377–D386, https://doi.org/10.1093/nar/gks1118.
Mortazavi A, Williams B A, McCue K et al. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods, 5(7): 621–628, https://doi.org/10.1038/nmeth.1226.
Nagaraj K, Mualla R, Hortsch M. 2014. The L1 family of cell adhesion molecules: a sickening number of mutations and protein functions. In: Berezin V, Walmod P S eds. Cell Adhesion Molecules. Springer, New York, NY. p.195–229, https://doi.org/10.1007/978-1-4614-8090-7_9.
Nishikawa J I, Mamiya S, Kanayama T et al. 2004. Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods. Environmental Science & Technology, 38(23): 6271–6276, https://doi.org/10.1021/es049593u.
Nolfi-Donegan D, Braganza A, Shiva S. 2020. Mitochondrial electron transport chain: oxidative phosphorylation, oxidant production, and methods of measurement. Redox Biology, 37: 101674, https://doi.org/10.1016/j.redox.2020.101674.
Pal M M. 2021. Glutamate: the master neurotransmitter and its implications in chronic stress and mood disorders. Frontiers in Human Neuroscience, 15: 722323, https://doi.org/10.3389/fnhum.2021.722323.
Park D C, Yeo S G. 2013. Aging. Korean journal of audiology, 17(2): 39–44, https://doi.org/10.7874/kja.2013.17.2.39.
Plachez C, Richards L J. 2005. Mechanisms of axon guidance in the developing nervous system. Current Topics in Developmental Biology, 69: 267–346, https://doi.org/10.1016/s0070-2153(05)69010-2.
Raghavan M, Wijeyesakere S J, Peters L R et al. 2013. Calreticulin in the immune system: ins and outs. Trends in Immunology, 34(1): 13–21, https://doi.org/10.1016/j.it.2012.08.002.
Ren L P, Sun J, Chen S M et al. 2014. A transcriptomic analysis of Chrysanthemum nankingense provides insights into the basis of low temperature tolerance. BMC Genomics, 15(1): 844, https://doi.org/10.1186/1471-2164-15-844.
Schimo S, Wittig I, Pos K M et al. 2017. Cytochrome c oxidase biogenesis and metallochaperone interactions: steps in the assembly pathway of a bacterial complex. PLoS One, 12(1): e0170037, https://doi.org/10.1371/journal.pone.0170037.
Schormann N, Hayden K L, Lee P et al. 2019. An overview of structure, function, and regulation of pyruvate kinases. Protein Science, 28(10): 1771–1784, https://doi.org/10.1002/pro.3691.
Seal S V, Turner J D. 2021. The ‘Jekyll and Hyde’ of gluconeogenesis: early life adversity, later life stress, and metabolic disturbances. International Journal of Molecular Sciences, 22(7): 3344, https://doi.org/10.3390/ijms22073344.
Sharma S, Shen T, Chitranshi N et al. 2022. Retinoid X receptor: cellular and biochemical roles of nuclear receptor with a focus on neuropathological involvement. Molecular Neurobiology, 59(4): 2027–2050, https://doi.org/10.1007/s12035-021-02709-y.
Sisk C L. 2016. Hormone-dependent adolescent organization of socio-sexual behaviors in mammals. Current Opinion in Neurobiology, 38: 63–68, https://doi.org/10.1016/j.conb.2016.02.004.
Soyano K, Amagai T, Yamaguchi T et al. 2022. Endocrine regulation of maturation and sex change in groupers. Cells, 11(5): 825, https://doi.org/10.3390/cells11050825.
Stupack D G, Cheresh D A. 2004. A bit-role for integrins in apoptosis. Nature Cell Biology, 6(5): 388–389, https://doi.org/10.1038/ncb0504-388.
Szanto A, Narkar V, Shen Q et al. 2004. Retinoid X receptors: X-ploring their (patho) physiological functions. Cell Death & Differentiation, 11(2): S126–S143, https://doi.org/10.1038/sj.cdd.4401533.
Tang F J, Gao W Y, Li H Q et al. 2020. Biology and fishery ecology of Protosalanx chinensis: a review. Journal of Fisheries of China, 44(12): 2100–2111. (in Chinese with English abstract)
Tesch F W, Wendt T, Karlsson L. 1992. Influence of geomagnetism on the activity and orientation of the eel, Anguilla anguilla (L.), as evident from laboratory experiments. Ecology of Freshwater Fish, 1(1): 52–60, https://doi.org/10.1111/j.1600-0633.1992.tb00007.x.
Tinkle D W, Woodward D W. 1967. Relative movements of lizards in natural populations as determined from recapture radii. Ecology, 48(1): 166–168, https://doi.org/10.2307/1933431.
Totland M Z, Rasmussen N L, Knudsen L M et al. 2020. Regulation of gap junction intercellular communication by connexin ubiquitination: physiological and pathophysiological implications. Cellular and Molecular Life Sciences, 77(4): 573–591, https://doi.org/10.1007/s00018-019-03285-0.
von Boletzky S. 1989. Early ontogeny and evolution: the cephalopod model viewed from the point of developmental morphology. Geobios, 22(S2): 67–78, https://doi.org/10.1016/S0016-6995(89)80008-7.
Wang Q, Wang Y B, Li S G et al. 2022. Organelle biogenesis: ribosomes as organizer and performer. Science Bulletin, 67(16): 1614–1617, https://doi.org/10.1016/j.scib.2022.07.023.
Wang Z Y, Ragsdale C W. 2018. Multiple optic gland signaling pathways implicated in octopus maternal behaviors and death. The Journal of Experimental Biology, 221: jeb185751, https://doi.org/10.1242/jeb.185751.
Wells M J, Wells J. 1969. Pituitary analogue in the octopus. Nature, 222(5190): 293–294, https://doi.org/10.1038/222293a0.
Wells M J, Wells J. 1975. Optic gland implants and their effects on the gonads of Octopus. Journal of Experimental Biology, 62(3): 579–588, https://doi.org/10.1242/jeb.62.3.579.
Wisby W J, Hasler A D. 1954. Effect of olfactory occlusion on migrating silver salmon (O. kisutch). Journal of the Fisheries Research Board of Canada, 11(4): 472–478, https://doi.org/10.1139/f54-031.
Wodinsky J. 1977. Hormonal inhibition of feeding and death in Octopus: control by optic gland secretion. Science, 198(4320): 948–951, https://doi.org/10.1126/science.198.4320.948.
Wu C W, Chi C F, He G Y et al. 2010. Isolation via enrichment and characterization of ten polymorphic microsatellite loci in the cuttlefish, Sepiella maindroni de Rochebruns. Acta Oceanologica Sinica, 29(6): 121–124, https://doi.org/10.1007/s13131-010-0083-2.
Wu Y T, Guo B Y, Qi P Z et al. 2017. Research progress on aquatic aging model animals. Journal of Zhejiang Ocean University (Natural Science), 36(1): 63–71. (in Chinese with English abstract)
Wu Y T, Guo B Y, Qi P Z et al. 2018. Cloning of the Phb2 gene and analysis of its developmental stage distribution in Sepiella japonica. Journal of Fishery Sciences of China, 25(1): 9–17. (in Chinese with English abstract)
Xia L M, Guo B Y, Ye Y Y et al. 2016. Determination of genetic diversity of the cuttlefish Sepiella japonica inhabiting Chinese coastal waters using the mitochondrial D-loop region: the valuable inspiration to artificial releasing project. Biochemical Systematics and Ecology, 69: 274–282, https://doi.org/10.1016/j.bse.2016.05.015.
Xu R Y, Pan L Q, Yang Y Y et al. 2020. Characterizing transcriptome in female scallop Chlamys farreri provides new insights into the molecular mechanisms of reproductive regulation during ovarian development and spawn. Gene, 758: 144967, https://doi.org/10.1016/j.gene.2020.144967.
Yin F, Sun P, Peng S M et al. 2013. The respiration, excretion and biochemical response of the juvenile common Chinese cuttlefish, Sepiella maindroni at different temperatures. Aquaculture, 402–403: 127–132, https://doi.org/10.1016/j.aquaculture.2013.03.018.
Yu X X, Chi C F, Wu C W. 2010. Review on gonadotropin-releasing hormone in the invertebrates. Journal of Zhejiang Ocean University (Natural Science), 29(4): 360–366, 372. (in Chinese with English abstract)
Yu X X, Wu C W, Chi C F. 2011. Brain microstructure and optic gland ultrastructure in Sepiella maindroni. Oceanologia et Limnologia Sinica, 42(2): 300–304, https://doi.org/10.11693/hyhz201102022022. (in Chinese with English abstract)
Zhang J Y, He M C, Xiang Z L et al. 2019. Transcriptome analysis for identifying possible causes of post-reproductive death of Sepia esculenta based on brain tissue. Genes & Genomics, 41(6): 629–645, https://doi.org/10.1007/s13258-019-00811-z.
7 Acknowledgment
Thank Yang SUN and Yu CHEN from Zhejiang Ocean University for their contributions to the breeding and sampling of experimental animals.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by the National Key R&D Program of China (No. 2019YFD0901204), the Hong Kong, Macao and Taiwan Science and Technology Cooperation Project (No. 2014DFT30120), the Zhejiang Provincial Natural Science Foundation of China (No. Y14C190008), the National Natural Science Foundation of China (Nos. 31101937, 31872547), and the Science Foundation of Donghai Laboratory (No. DH-2022KF0209)
Rights and permissions
About this article
Cite this article
Dong, Z., Zhao, J., Guo, F. et al. Transcriptome profiling and RXR gene family identification reveals the molecular mechanism of rapid aging after spawning of cuttlefish Sepiella japonica. J. Ocean. Limnol. (2024). https://doi.org/10.1007/s00343-023-3029-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00343-023-3029-1