Cite this paper:
HUI Min, CUI Zhaoxia, LIU Yuan, SONG Chengwen. Transcriptome profiles of embryos before and after cleavage in Eriocheir sinensis: identification of developmental genes at the earliest stages[J]. Journal of Oceanology and Limnology, 2017, 35(4): 770-781

Transcriptome profiles of embryos before and after cleavage in Eriocheir sinensis: identification of developmental genes at the earliest stages

HUI Min1, CUI Zhaoxia1,2,3, LIU Yuan1, SONG Chengwen1,4
1 Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 National & Local Joint Engineering Laboratory of Ecological Mariculture, Qingdao 266071, China;
3 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China;
4 University of Chinese Academy of Sciences, Beijing 100049, China
Abstract:
In crab, embryogenesis is a complicated developmental program marked by a series of critical events. RNA-Sequencing technology offers developmental biologists a way to identify many more developmental genes than ever before. Here, we present a comprehensive analysis of the transcriptomes of Eriocheir sinensis oosperms (Os) and embryos at the 2-4 cell stage (Cs), which are separated by a cleavage event. A total of 18 923 unigenes were identified, and 403 genes matched with gene ontology (GO) terms related to developmental processes. In total, 432 differentially expressed genes (DEGs) were detected between the two stages. Nine DEGs were specifically expressed at only one stage. These DEGs may be relevant to stage-specific molecular events during development. A number of DEGs related to ‘hedgehog signaling pathway’, ‘Wnt signaling pathway’ ‘germplasm’, ‘nervous system’, ‘sensory perception’ and ‘segment polarity’ were identified as being up-regulated at the Cs stage. The results suggest that these embryonic developmental events begin before the early cleavage event in crabs, and that many of the genes expressed in the two transcriptomes might be maternal genes. Our study provides ample information for further research on the molecular mechanisms underlying crab development.
Key words:    mitten crabs|embryo development|fertilized egg|cleavage|transcriptomics   
Received: 2015-12-18   Revised: 2016-03-03
Tools
PDF (819 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by HUI Min
Articles by CUI Zhaoxia
Articles by LIU Yuan
Articles by SONG Chengwen
References:
Aanes H, Winata C L, Lin C H, Chen J P, Srinivasan K G, Lee S G P, Lim A Y M, Hajan H S, Collas P, Bourque G, Gong Z Y, Korzh V, Aleström P, Mathavan S. 2011. Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res., 21(8):1 328-1 338.
Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol., 11(10):R106.
Calvo E, Walter M, Adelman Z N, Jimenez A, Onal S, Marinotti O, James A A. 2005. Nanos (nos) genes of the vector mosquitoes, Anopheles gambiae, Anopheles stephensi and Aedes aegypti. Insect Biochem. Mol. Biol., 35(7):789-798.
Chen S L, Zhang Z J, Shao C W et al. 2014. Whole-genome sequence of a flatfish provides insights into zw sex chromosome evolution and adaptation to a benthic lifestyle. Nature Genetics, 46(3):253-260.
Chicoine J, Benoit P, Gamberi C, Paliouras M, Simonelig M, Lasko P. 2007. Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev. Cell, 13(5):691-704.
Conesa A, Götz S, García-Gómez J M, Terol J, Talón M, Robles M. 2005. Blast2GO:a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18):3 674-3 676.
Cox M P, Peterson D A, Biggs P J. 2010. SolexaQA:At-aglance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics, 11:485.
Dearden P K. 2006. Germ cell development in the Honeybee(Apis mellifera); Vasa and Nanos expression. BMC Dev.Biol., 6(1):6.
Du N S, Zhao Y L, Lai W. 1992. Studies on the embryonic development of Eriocheir sinensis. In:Memoir of Crustacean (the Third Set). Ocean University of Qingdao Press, Qingdao, p.128-135. (in Chinese)
Extavour C G, Pang K, Matus D Q, Martindale M Q. 2005. Vasa and nanos expression patterns in a sea anemone and the evolution of bilaterian germ cell specification mechanisms. Evol. Dev., 7(3):201-215.
Extavour C G. 2005. The fate of isolated blastomeres with respect to germ cell formation in the amphipod crustacean Parhyale hawaiensis. Dev. Biol., 277(2):387-402.
Flach G, Johnson M H, Braude P R, Taylor R A, Bolton V N. 1982. The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J., 1(6):681-686.
Grabherr M G, Haas B J, Yassour M, Levin J Z, Thompson D A, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q D, Chen Z H, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren B W, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol., 29(7):644-652.
He L, Jiang H, Cao D D, Liu L H, Hu S N, Wang Q. 2013. Comparative transcriptome analysis of the accessory sex gland and testis from the Chinese Mitten Crab (Eriocheir sinensis). PLoS One, 8(1):e53915.
Hui M, Liu Y, Song C W, Li Y D, Shi G H, Cui Z X. 2014. Transcriptome changes in Eriocheir sinensis megalopae after desalination provide insights into osmoregulation and stress adaption in larvae. PLoS One, 9(12):e114187.
Jen J C, Chan W M, Bosley T M et al. 2004. Mutations in a human ROBO gene disrupt hindbrain axon pathway crossing and morphogenesis. Science, 304(5676):1 509-1 513.
Jiang H, Wong W H. 2008. SeqMap:mapping massive amount of oligonucleotides to the genome. Bioinformatics, 24(20):2 395-2 396.
Jiang H, Wong W H. 2009. Statistical inferences for isoform expression in RNA-Seq. Bioinformatics, 25(8):1 026-1 032.
Kane D A, Kimmel C B. 1993. The zebrafish midblastula transition. Development, 119(2):447-456.
Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. 2004. The KEGG resource for deciphering the genome. Nucl. Acids Res., 32(S1):D277-D280.
Kim C H, Hwang S G. 1995. The complete larval development of the mitten crab Eriocheir sinensis H. Milne Edwards, 1853 (Decapoda, Brachyura, Grapsidae) reared in the laboratory and a key to the known zoeae of the Varuninae. Crustaceana, 68(7):793-812.
Kobayashi S, Yamada M, Asaoka M, Kitamura T. 1996. Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature, 380(6576):708-711.
Kuballa A V, Holton T A, Paterson B, Elizur A. 2011. Moult cycle specific differential gene expression profiling of the crab Portunus pelagicus. BMC Genomics, 12(1):147.
Lanes C F C, Bizuayehu T T, de Oliveira Fernandes J M, Kiron V, Babiak I. 2013. Transcriptome of Atlantic cod (Gadus morhua L.) early embryos from farmed and wild broodstocks. Mar. Biotechnol., 15(6):677-694.
Laufer H, Biggers W J. 2001. Unifying concepts learned from methyl farnesoate for invertebrate reproduction and postembryonic development. Am. Zool., 41(3):442-457.
Li E C, Wang S L, Li C, Wang X D, Chen K, Chen L Q. 2014. Transcriptome sequencing revealed the genes and pathways involved in salinity stress of Chinese mitten crab, Eriocheir sinensis. Physiol. Genomics, 46(5):177-190.
Li Q, Xie J, He L, Wang Y L, Duan Z L, Yang H D, Wang Q. 2015a. Identification of ADAM10 and ADAM17 with potential roles in the spermatogenesis of the Chinese mitten crab, Eriocheir sinensis. Gene, 562(1):117-127.
Li Y D, Hui M, Cui Z X, Liu Y, Song C W, Shi G H. 2015b. Comparative transcriptomic analysis provides insights into the molecular basis of the metamorphosis and nutrition metabolism change from zoeae to megalopae in Eriocheir sinensis. Comp. Biochem. Phys. Part D, 13:1-9.
Lutz D, Wolters-Eisfeld G, Schachner M, Kleene R. 2014. Cathepsin E generates a sumoylated intracellular fragment of the cell adhesion molecule L1 to promote neuronal and Schwann cell migration as well as myelination. J. Neurochem, 128(5):713-724.
Mahone M, Saffman E E, Lasko P F. 1997. Localized BicaudalC RNA encodes a protein containing a KH domain, the RNA binding motif of FMR1. EMBO J., 16(13):4152.
Matsuoka T, Ikeda T, Fujimaki K, Satou Y. 2013. Transcriptome dynamics in early embryos of the ascidian, Ciona intestinalis. Dev. Biol., 384(2):375-385.
Mortazavi A, Williams B A, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5(7):621-628.
Obermann H, Samalecos A, Osterhoff C, Schröder B, Heller R, Kirchhoff C. 2003. HE6, a two-subunit heptahelical receptor associated with apical membranes of efferent and epididymal duct epithelia. Mol. Reprod. Dev., 64(1):13-26.
Oldham S, Böhni R, Stocker H, Brogiolo W, Hafen E. 2000. Genetic control of size in Drosophila. Philos. Trans. R. Soc. Lond. B Biol. Sci., 355(1399):945-952.
Ou J T, Meng Q H, Li Y, Xiu Y J, Du J, Gu W, Wu T, Li W J, Ding Z F, Wang W. 2012. Identification and comparative analysis of the Eriocheir sinensis microRNA transcriptome response to Spiroplasma eriocheiris infection using a deep sequencing approach. Fish Shellfish Immunol., 32(2):345-352.
Sellars M J, Trewin C, McWilliam S M, Glaves R S E, Hertzler P L. 2015. Transcriptome profiles of Penaeus(Marsupenaeus) japonicus animal and vegetal halfembryos:identification of sex determination, germ line, mesoderm, and other developmental genes. Mar. Biotechnol., 17(3):252-265.
Song C W, Cui Z X, Hui M, Liu Y, Li Y D, Li X H. 2015. Comparative transcriptomic analysis provides insights into the molecular basis of brachyurization and adaptation to benthic lifestyle in Eriocheir sinensis. Gene, 558(1):88-98.
Sui L Y, Wille M, Cheng Y X, Wu X G, Sorgeloos P. 2011. Larviculture techniques of Chinese mitten crab Eriocheir sinensis. Aquaculture, 315(1-2):16-19.
Sun Y, Zhang Y C, Liu Y C, Xue S X, Geng X Y, Hao T, Sun J S. 2014. Changes in the organics metabolism in the hepatopancreas induced by eyestalk ablation of the Chinese mitten crab Eriocheir sinensis determined via transcriptome and DGE analysis. PLoS One, 9(4):e95827.
Tang D Y, Yu Y, Zhao X J, Schachner M, Zhao W J. 2015. Single chain fragment variable antibodies developed by using as target the 3rd fibronectin type III homologous repeat fragment of human neural cell adhesion molecule L1 promote cell migration and neuritogenesis. Exp. Cell Res., 330(2):336-345.
Tautz D. 1988. Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature, 332(6161):281-284.
Ventura T, Manor R, Aflalo E D, Chalifa-Caspi V, Weil S, Sharabi O, Sagi A. 2013. Post-Embryonic transcriptomes of the prawn Macrobrachium rosenbergii:multigenic succession through metamorphosis. PLoS One, 8(1):e55322.
Vesterlund L, Jiao H, Unneberg P, Hovatta O, Kere J. 2011. The zebrafish transcriptome during early development. BMC Dev. Biol., 11(1):30.
Wójcik D, Normant M. 2014. Gonad maturity in female Chinese mitten crab Eriocheir sinensis from the southern Baltic Sea-the first description of ovigerous females and the embryo developmental stage. Oceanologia, 56(4):779-787.
Yang H X, Zhou Y, Gu J L, Xie S Y, Xu Y, Zhu G F, Wang L, Huang J Y, Ma H, Yao J H. 2013. Deep mRNA sequencing analysis to capture the transcriptome landscape of zebrafish embryos and larvae. PLoS One, 8(5):e64058.
Zeng V, Villanueva K E, Ewen-Campen B S, Alwes F, Browne W E, Extavour C G. 2011. De novo assembly and characterization of a maternal and developmental transcriptome for the emerging model crustacean Parhyale hawaiensis. BMC Genomics, 12(1):581.
Zhang W, Wan H L, Jiang H, Zhao Y L, Zhang X W, Hu S N, Wang Q. 2011. A transcriptome analysis of mitten crab testes (Eriocheir sinensis). Genet. Mol. Biol., 34(1):136-141.
Zhao J C, Wang Y L, Li Q, Zhu ML, Sun W J, Wu T M, Wang Q, He L. 2016. Molecular cloning and characterization of p38 gene in the Chinese mitten crab, Eriocheir sinensis. Aquac. Res., 47(4):1 353-1 363.
Copyright © Haiyang Xuebao