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Actin genes and their expression in pacific white shrimp, Litopenaeus vannamei

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Abstract

Actin is a multi-functional gene family that can be divided into muscle-type actins and non-muscle-type actins. In this study, 37 unigenes encoding actins were identified from RNA-Seq data of Pacific white shrimp, Litopenaeus vannamei. According to phylogenetic analysis, four and three cDNAs belong to cytoplasmic- and heart-type actins and were named LvActinCT and LvActinHT, respectively. 10 cDNAs belong to the slow-type skeletal muscle actins, and 18 belong to the fast-type skeletal muscle actins; they were designated LvActinSSK and LvActinFSK, respectively. Some muscle actin genes formed gene clusters in the genome. Multiple alternative transcription starts sites (ATSSs) were found for LvActinCT1. Based on the early developmental expression profile, almost all LvActins were highly expressed between the early limb bud and post-larval stages. Using LvActinSSK5 as probes, slow-type muscle was localized in pleopod muscle and superficial ventral muscle. We also found three actin genes that were down-regulated in the hemocytes of white spot syndrome virus (WSSV)- and Vibrio parahaemolyticus-infected L. vannamei. This study provides valuable information on the actin gene structure of shrimp, furthers our understanding of the shrimp muscle system and helps us develop strategies for disease control and sustainable shrimp farming.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    Article  CAS  PubMed  Google Scholar 

  • Ascencio F, Aguirre-Guzmán G, Vázquez-Juárez R (2001) Differences in the susceptibility of American white shrimp larval substages (Litopenaeus vannamei) to four vibrio species. J Invertebr Pathol 78(4):215–219

    Article  PubMed  Google Scholar 

  • Bokwang K, Kyoungsun K, Chulwoong O, Mykles DL, Sunggu L, Hakjun K, Hyunwoo K (2009) Twelve actin-encoding cDNAs from the American lobster, Homarus americanus: cloning and tissue expression of eight skeletal muscle, one heart, and three cytoplasmic isoforms. Comp Biochem Physiol Part B Biochem Mol Biol 153(2): 178–184

    Article  Google Scholar 

  • Bond BJ, Davidson N (1986) The Drosophila melanogaster actin 5C gene uses two transcription initiation sites and three polyadenylation sites to express multiple mRNA species. Mol Cell Biol 6(6):2080–2088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davuluri RV, Suzuki Y, Sugano S, Plass C, Huang TH (2008) The functional consequences of alternative promoter use in mammalian genomes. Trends Genet 24(4):167–177

    Article  CAS  PubMed  Google Scholar 

  • Deng W, Wang Y, Liu Z, Cheng H, Xue Y (2014) HemI: A Toolkit for Illustrating Heatmaps. Plos One 9(11):e111988

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Saleh SC, Thieret R, Johnson P, Potter J (1984) Modification of Lys-237 on actin by 2, 4-pentanedione. Alteration of the interaction of actin with tropomyosin. J Biol Chem 259(17):11014–11021

    CAS  PubMed  Google Scholar 

  • Files JG, Carr S, Hirsh D (1983) Actin gene family of Caenorhabditis elegans. J Mol Biol 164(3):355–375

    Article  CAS  PubMed  Google Scholar 

  • Finn RD, Attwood TK, Babbitt PC, Bateman A, Bork P, Bridge AJ, Chang H-Y, Dosztányi Z, El-Gebali S, Fraser M (2016) InterPro in 2017—beyond protein family and domain annotations. Nucleic Acids Res 45(D1):D190–D199

    Google Scholar 

  • Fyrberg C, Ryan L, Mcnally L, Kenton M, Fyrberg E (1994) The actin protein superfamily. Soc General Physiol 49:173–178

    CAS  Google Scholar 

  • Hertzler PL, Freas WR (2009) Pleonal muscle development in the shrimp Penaeus (Litopenaeus) vannamei (Crustacea: Malacostraca: Decapoda: Dendrobranchiata). Arthropod Struct Dev 38(3):235–246

    Article  PubMed  Google Scholar 

  • Holmes KC, Kabsch W (1991) Muscle proteins: actin. Curr Opin Struct Biol 1(2):270–280

    Article  CAS  Google Scholar 

  • Hooper SL, Thuma JB (2005) Invertebrate muscles: muscle specific genes and proteins. Physiol Rev 85(3):1001–1060

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9(9):868–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiernan DA, Hertzler PL (2006) Muscle development in dendrobranchiate shrimp, with comparison with Artemia. Evol Dev 8(6):537–549

    Article  PubMed  Google Scholar 

  • Kimura K, Wakamatsu A, Suzuki Y, Ota T, Nishikawa T, Yamashita R, Yamamoto J, Sekine M, Tsuritani K, Wakaguri H (2006) Diversification of transcriptional modulation: large-scale identification and characterization of putative alternative promoters of human genes. Genome Res 16(1):55–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koyama H, Akolkar DB, Piyapattanakorn S, Watabe S (2012) Cloning, expression, and localization of two types of fast skeletal myosin heavy chain genes from black tiger and pacific white shrimps. J Exp Zool Part A Ecol Genet Physiol 317(10):608–621

    CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870

    Article  CAS  PubMed  Google Scholar 

  • Kusakabe T, Makabe KW, Satoh N (1992) Tunicate muscle actin genes. Structure and organization as a gene cluster. J Mol Biol 227(3):955–960

    Article  CAS  PubMed  Google Scholar 

  • Lee JJ, Shott RJ, Rose SJ, Thomas TL, Britten RJ, Davidson EH (1984) Sea urchin actin gene subtypes. J Mol Biol 172(2):149–176

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Bork P (2006) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23(1):127–128

  • Letunic I, Doerks T, Bork P (2014) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43(D1):D257–D260

    Google Scholar 

  • Liu B, Tang X, Zhan W (2011) Interaction between white spot syndrome virus VP26 and hemocyte membrane of shrimp, Fenneropenaeus chinensis. Aquaculture 314(1–4):13–17

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Macias MT, Sastre L (1990) Molecular cloning and expression of four actin isoforms during Artemia development. Nucleic Acids Res 18(17):5219–5225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milligan R, Flicker P (1987) Structural relationships of actin, myosin, and tropomyosin revealed by cryo-electron microscopy. J Cell Biol 105(1):29–39

    Article  CAS  PubMed  Google Scholar 

  • Moens PD, dos Remedios CG (1997) A conformational change in F-actin when myosin binds: fluorescence resonance energy transfer detects an increase in the radial coordinate of Cys-374. Biochemistry 36(24):7353–7360

    Article  CAS  PubMed  Google Scholar 

  • Ortega MA, Macias MT, Martinez JL, Palmero I, Sastre L (1992) Expression of actin isoforms in Artemia. Symp Soc Exp Biol 46:131–137

    CAS  PubMed  Google Scholar 

  • Pollard TD, Cooper JA (1986) Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu Rev Biochem 55(1):987

    Article  CAS  PubMed  Google Scholar 

  • Razzaq A, Schmitz S, Veigel C, Molloy JE, Geeves MA, Sparrow JC (1999) Actin residue Glu93 is identified as an amino acid affecting myosin binding. J Biol Chem 274(40):28321–28328

    Article  CAS  PubMed  Google Scholar 

  • Rombel IT, Sykes KF, Rayner S, Johnston SA (2002) ORF-FINDER: a vector for high-throughput gene identification. Gene 282(1):33–41

    Article  CAS  PubMed  Google Scholar 

  • Sun PS, Soderlund M Jr, Ye NCV D and Lu Y (2007) Isolation and characterization of two actins of the Pacific white shrimp, Litopenaeus vannamei. Mar Biol 151(6):2145–2151

    Article  Google Scholar 

  • Sutoh K (1983) Mapping of actin-binding sites on the heavy chain of myosin subfragment 1. Biochemistry 22(7):1579–1585

    Article  CAS  PubMed  Google Scholar 

  • Szilagyi L, Lu R (1982) Changes of lysine reactivities of actin in complex with myosin subfragment-1, tropomyosin and troponin. Biochim Biophys Acta (BBA) Protein Struct Mol Enzymol 709(2):204–211

    Article  CAS  Google Scholar 

  • Uddowla MH, Salma U, Kim H-W (2013) Molecular characterization of four actin cDNAs and effects of 20-hydroxyecdysone on their expression in swimming crab, Portunus trituberculatus (Miers, 1876). Animal Cells Syst 17(3):203–212

    Article  CAS  Google Scholar 

  • Varadaraj K, Kumari SS, Skinner DM (1996) Actin-encoding cDNAs and gene expression during the intermolt cycle of the Bermuda land crab Gecarcinus lateralis. Gene 171(2):177–184

    Article  CAS  PubMed  Google Scholar 

  • Venkatesh B, Tay BH, Elgar G, Brenner S (1996) Isolation, characterization and evolution of nine pufferfish (Fugu rubripes) actin genes. J Mol Biol 259(4):655–665

    Article  CAS  PubMed  Google Scholar 

  • Vigoreaux JO, Tobin SL (1987) Stage-specific selection of alternative transcriptional initiation sites from the 5C actin gene of Drosophila melanogaster. Genes Dev 1(1):1161–1171

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Li F, Dong B, Zhang X, Zhang C, Xiang J (2006) Discovery of the genes in response to white spot syndrome virus (WSSV) infection in Fenneropenaeus chinensis through cDNA microarray. Mar Biotechnol 8(5):491–500

    Article  PubMed  Google Scholar 

  • Wang HC, Wang HC, Leu JH, Kou GH, Wang HJ, Lo CF (2007) Protein expression profiling of the shrimp cellular response to white spot syndrome virus infection. Dev Comp Immunol 31(7):672–686

    Article  CAS  PubMed  Google Scholar 

  • Wei J, Zhang X, Yu Y, Huang H, Li F, Xiang J (2014) Comparative transcriptomic characterization of the early development in Pacific white shrimp Litopenaeus vannamei. PLoS One 9(9):e106201

    Article  PubMed  PubMed Central  Google Scholar 

  • Welch MD, Rosenblatt J, Skoble J, Portnoy DA, Mitchison TJ (1998) Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281(5373):105–108

    Article  CAS  PubMed  Google Scholar 

  • Wen L, Dong Q, Yan X (2011) Proteomic analysis of differentially expressed proteins in hemolymph of Scylla serrata response to white spot syndrome virus infection. Aquaculture 314(1–4):53–57

    Google Scholar 

  • Xie X, Yang F (2005) Interaction of white spot syndrome virus VP26 protein with actin. Virology 336(1):93

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Li F, Jiang H, Yu Y, Liu C, Li S, Wang B, Xiang J (2010) Proteomic analysis of differentially expressed proteins in lymphoid organ of Fenneropenaeus chinensis response to Vibrio anguillarum stimulation. Fish Shellfish Immunol 29(2):186–194

    Article  PubMed  Google Scholar 

  • Zhou L, Li S, Wang Z, et al (2017) An eclosion hormone-like gene participates in the molting process of Palaemonid shrimp Exopalaemon carinicauda. Dev Genes Evol 227(3):189–199

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (31672632, 41506189, 41376165), China Agriculture Research System-47 (CARS-47) and The Scientific and Technological Innovation Project Financially Supported by Qingdao National Laboratory for Marine Science and Technology (2015ASKJ02-3). In addition, we thank Q. Guo for guidance in in situ hybridization experiment technology.

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Authors and Affiliations

  1. Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Xiaoxi Zhang, Xiaojun Zhang, Jianbo Yuan, Jiangli Du, Fuhua Li & Jianhai Xiang

  2. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Xiaoxi Zhang, Xiaojun Zhang, Jianbo Yuan, Jiangli Du, Fuhua Li & Jianhai Xiang

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Xiaoxi Zhang & Jiangli Du

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  1. Xiaoxi Zhang
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Correspondence to Xiaoxi Zhang.

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Zhang, X., Zhang, X., Yuan, J. et al. Actin genes and their expression in pacific white shrimp, Litopenaeus vannamei . Mol Genet Genomics 293, 479–493 (2018). https://doi.org/10.1007/s00438-017-1397-y

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  • DOI: https://doi.org/10.1007/s00438-017-1397-y

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