Dynamics of fatty acid regulatory genes during ovarian development in Penaeus monodon

in Reproduction
Authors:
Pacharawan Deenarn National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Khlong Luang, Pathum Thani, Thailand

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Punsa Tobwor National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Khlong Luang, Pathum Thani, Thailand

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Rungnapa Leelatanawit National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Khlong Luang, Pathum Thani, Thailand

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Somjai Wongtriphop Shrimp Genetic Improvement Center, Chaiya, Surat Thani, Thailand

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Jutatip Khudet Shrimp Genetic Improvement Center, Chaiya, Surat Thani, Thailand

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Nitsara Karoonuthaisiri National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Khlong Luang, Pathum Thani, Thailand

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Vanicha Vichai National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Khlong Luang, Pathum Thani, Thailand

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Wananit Wimuttisuk National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Khlong Luang, Pathum Thani, Thailand

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Correspondence should be addressed to W Wimuttisuk; Email: wananit.wim@biotec.or.th
DOI:
https://doi.org/10.1530/REP-18-0143
Volume/Issue:
Volume 156: Issue 6
Page Range:
527–544
Article Type:
Research Article
Online Publication Date:
Dec 2018
Copyright:
© 2018 Society for Reproduction and Fertility 2018
Restricted access
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The delay in ovarian maturation in farmed black tiger shrimp Penaeus monodon has resulted in the widespread practice of feeding broodstock with the polychaete Perinereis nuntia and their unilateral eyestalk ablation. Although this practice alters fatty acid content in shrimp ovaries and hepatopancreas, its effects on fatty acid regulatory genes are yet to be systematically examined. Here, microarray analysis was performed on hepatopancreas and ovary cDNA collected from P. monodon at different ovarian maturation stages, revealing that 72 and 58 genes in fatty acid regulatory pathways were differentially expressed in hepatopancreas and ovaries respectively. Quantitative real-time PCR analysis revealed that ovarian maturation was associated with higher expression levels of acetyl-CoA acetyltransferase, acyl-CoA dehydrogenase, acyl-CoA oxidase 3 and long-chain fatty acid transport protein 4 in hepatopancreas, whereas the expression levels of 15 fatty acid regulatory genes were increased in shrimp ovaries. To distinguish the effects of different treatments, transcriptional changes were examined in P. monodon with stage 1 ovaries before polychaete feeding, after 1 month of polychaete feeding and after eyestalk ablation. Polychaete feeding resulted in lower expression levels of enoyl-CoA hydratase and acyl-CoA synthetase medium-chain family member 4, while the expression level of phosphatidylinositide phosphatase SAC1 was higher in shrimp hepatopancreas and ovaries. Additionally, eyestalk ablation resulted in a higher expression level of long-chain fatty acid-CoA ligase 4 in both tissues. Together, our findings describe the dynamics of fatty acid regulatory pathways during crustacean ovarian development and provide potential target genes for alternatives to eyestalk ablation in the future.

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Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Alava VR, Quinitio ET, De Pedro JB, Orosco ZGA & Wille M 2007 Reproductive performance, lipids and fatty acids of mud crab Scylla serrata (Forsskål) fed dietary lipid levels. Aquaculture Research 38 1442–1451. (https://doi.org/10.1111/j.1365-2109.2007.01722.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Benzie JAH 1997 A review of the effect of genetics and environment on the maturation and larval quality of the giant tiger prawn, Penaeus monodon. Aquaculture 155 69–85. (https://doi.org/10.1016/S0044-8486(97)00110-5)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bray W & Lawrence A 1992 Reproduction of Penaeus species in captivity. Marine Shrimp Culture: Principles and Practices. Eds Fast Arlo W., Lester L. James. pp 93–170, Elsevier Science, (https://doi.org/10.1016/C2009-0-01033-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Castille FC & Lawrence AL 1989 The relationship between maturation and the size and biochemical composition of the gonads and digestive glands of the shrimp Penaeus aztecus Ives and Penaeus setiferus (L). Journal of Crustacean Biology 9 202–211. (https://doi.org/10.2307/1548500)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chen K, Li E, Xu C, Wang X, Lin H, Qin JG & Chen L 2015 Evaluation of different lipid sources in diet of pacific white shrimp Litopenaeus vannamei at low salinity. Aquaculture Reports 2 163–168. (https://doi.org/10.1016/j.aqrep.2015.10.003)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Clesceri LS, Eaton AD, Greenberg AE, Association APH, Association AWW & Federation WE 1998 Standard Methods for the Examination of Water and Wastewater. American Public Health Association.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • de Hoon MJL, Imoto S, Nolan J & Miyano S 2004 Open source clustering software. Bioinformatics 20 1453–1454. (https://doi.org/10.1093/bioinformatics/bth078)

  • Ding L-Y, Jin M, Sun P, Lu Y, Ma H-N, Yuan Y, Fu H-Y & Zhou Q-C 2017 Cloning, tissue expression of the fatty acid-binding protein (Pt-FABP1) gene, and effects of dietary phospholipid levels on fabp and vitellogenin gene expression in the female swimming crab Portunus trituberculatus. Aquaculture 474 57–65. (https://doi.org/10.1016/j.aquaculture.2017.03.029)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dy-Peñaflorida V & Millamena OM 1990 Variation in the biochemical composition of Penaeus monodon tissues during the reproductive cycle. Israeli Journal of Aquaculture-Bamidgeh 42 84–90.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Edgar R, Domrachev M & Lash AE 2002 Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research 30 207–210. (https://doi.org/10.1093/nar/30.1.207)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Elwood RW, Barr S & Patterson L 2009 Pain and stress in crustaceans? Applied Animal Behaviour Science 118 128–136. (https://doi.org/10.1016/j.applanim.2009.02.018)

  • Girish BP, Swetha CH & Reddy PS 2014 Hepatopancreas but not ovary is the site of vitellogenin synthesis in female fresh water crab, Oziothelphusa senex senex. Biochemical and Biophysical Research Communications 447 323–327. (https://doi.org/10.1016/j.bbrc.2014.03.148)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gong Y-N, Li W-W, Sun J-L, Ren F, He L, Jiang H & Wang Q 2010 Molecular cloning and tissue expression of the fatty acid-binding protein (Es-FABP) gene in female Chinese mitten crab (Eriocheir sinensis). BMC Molecular Biology 11 71. (https://doi.org/10.1186/1471-2199-11-71)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Greenberg AE, Clesceri LS & Eaton AD 1992 Standard Methods for the Examination of Waste and Wastewater. Washington, D.C.: American Public Health Society, American Water Works Association, Water Environment Federation.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hoa ND, Wouters R, Wille M, Thanh V, Dong TK, Hao NV & Sorgeloos P 2009 A fresh-food maturation diet with an adequate HUFA composition for broodstock nutrition studies in black tiger shrimp Penaeus monodon (Fabricius, 1798). Aquaculture 297 116–121. (https://doi.org/10.1016/j.aquaculture.2009.09.005)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Huang J-H, Jiang S-G, Lin H-Z, Zhou F-L & Ye L 2008 Effects of dietary highly unsaturated fatty acids and astaxanthin on the fecundity and lipid content of pond-reared Penaeus monodon (Fabricius) broodstock. Aquaculture Research 39 240–251. (https://doi.org/10.1111/j.1365-2109.2007.01868.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Karoonuthaisiri N, Sittikankeaw K, Preechaphol R, Kalachikov S, Wongsurawat T, Uawisetwathana U, Russo JJ, Ju J, Klinbunga S & Kirtikara K 2008 ReproArray(GTS): a cDNA microarray for identification of reproduction-related genes in the giant tiger shrimp Penaeus monodon and characterization of a novel nuclear autoantigenic sperm protein (NASP) gene. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 4 90–99. (https://doi.org/10.1016/j.cbd.2008.11.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kasnir M, Harlina & Rosmiati 2014 Water quality parameter analysis for the feasibility of shrimp culture in Takalar regency, Indonesia. Journal of Aquaculture Research and Development 5 273. (https://doi.org/10.4172/2155-9546.1000273)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kung SY, Chan SM, Hui JH, Tsang WS, Mak A & He JG 2004 Vitellogenesis in the sand shrimp, Metapenaeus ensis: the contribution from the hepatopancreas-specific vitellogenin gene (MeVg2). Biology of Reproduction 71 863–870. (https://doi.org/10.1095/biolreprod.103.022905)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lee FY & Chang CF 1999 Hepatopancreas is the likely organ of vitellogenin synthesis in the freshwater prawn, Macrobrachium rosenbergii. Journal of Experimental Zoology 284 798–806. (https://doi.org/10.1002/(SICI)1097-010X(19991201)284:7<798::AID-JEZ10>3.0.CO;2-C)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lee J-H, Kim BK, Seo Y-I, Choi JH, Kang S-W, Kang C-K, Park W-G & Kim H-W 2014 Four cDNAs encoding lipoprotein receptors from shrimp (Pandalopsis japonica): structural characterization and expression analysis during maturation. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 169 51–62. (https://doi.org/10.1016/j.cbpb.2013.12.005)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leelatanawit R, Klanchui A, Uawisetwathana U & Karoonuthaisiri N 2012 Validation of reference genes for real-time PCR of reproductive system in the black tiger shrimp. PLoS ONE 7 e52677. (https://doi.org/10.1371/journal.pone.0052677)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leelatanawit R, Uawisetwathana U, Klinbunga S & Karoonuthaisiri N 2011 A cDNA microarray, UniShrimpChip, for identification of genes relevant to testicular development in the black tiger shrimp (Penaeus monodon). BMC Molecular Biology 12 15. (https://doi.org/10.1186/1471-2199-12-15)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Li W-W, Jin X-K, He L, Gong Y-N, Jiang H & Wang Q 2011 Molecular cloning and tissue expression of the fatty acid-binding protein (Es-FABP9) gene in the reproduction seasons of Chinese mitten crab, Eriocheir sinensis. Molecular Biology Reports 38 5169–5177. (https://doi.org/10.1007/s11033-010-0666-1)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • López-Greco LS & Rodríguez EM 1999 Annual reproduction and growth of adult crabs Chasmagnathus granulata (Crustacea, Brachyura, Grapsidae). Cahiers De Biologie Marine 40 155–164.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Magalhaes T, Mossolin EC & Mantelatto FL 2012 Gonadosomatic and hepatosomatic indexes of the freshwater shrimp Macrobrachium olfersii (Decapoda, Palaemonidae) from São Sebastião Island, Southeastern Brazil. Pan-American Journal of Aquatic Science 7 1–9.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Makinouchi S, Sugama K, Ruchimat T, Tridjoko Sutarmat T & Lante S 1995 Effects of eyestalk ablation on maturation, spawning, hatching, molting and growth of precocious pond reared Penaeus monodon. Aquaculture Science 43 103–108. (https://doi.org/10.11233/aquaculturesci1953.43.103)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Marsden G, Mather P & Richardson N 2007 Captivity, ablation and starvation of the prawn Penaeus monodon affects protein and lipid content in ovary and hepatopancreas tissues. Aquaculture 271 507–515. (https://doi.org/10.1016/j.aquaculture.2007.04.076)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mekuchi M, Ohira T, Kawazoe I, Jasmani S, Suitoh K, Kim YK, Jayasankar V, Nagasawa H & Wilder MN 2008 Characterization and expression of the putative ovarian lipoprotein receptor in the kuruma prawn, Marsupenaeus japonicus. Zoological Science 25 428–437. (https://doi.org/10.2108/zsj.25.428)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Meunpol O, Duangjai E, Yoonpun R & Piyatiratitivorakul S 2010 Detection of prostaglandin E2 in polychaete Perinereis sp. and its effect on Penaeus monodon oocyte development in vitro. Fisheries Science 76 281–286. (https://doi.org/10.1007/s12562-009-0208-8)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Millamena OM & Pascual FP 1990 Tissue lipid content and fatty acid composition of Penaeus monodon Fabricius broodstock from the wild. Journal of the World Aquaculture Society 21 116–121. (https://doi.org/10.1111/j.1749-7345.1990.tb00531.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Paibulkichakul C, Piyatiratitivorakul S, Sorgeloos P & Menasveta P 2008 Improved maturation of pond-reared black tiger shrimp (Penaeus monodon) using fish oil and astazanthin feed supplements. Aquaculture 282 83–89. (https://doi.org/10.1016/j.aquaculture.2008.06.006)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Parra-Peralbo E & Culi J 2011 Drosophila lipophorin receptors mediate the uptake of neutral lipids in oocytes and imaginal disc cells by an endocytosis-independent mechanism. PLoS Genetics 7 e1001297. (https://doi.org/10.1371/journal.pgen.1001297)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Quinitio ET, Hara A, Yamauchi K & Nakao S 1994 Changes in the steroid hormone and vitellogenin levels during the gametogenic cycle of the giant tiger shrimp, Penaeus monodon. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 109 21–26. (https://doi.org/10.1016/0742-8413(94)00044-B)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ravikumar G & Vijayaprakash NB 2013 Lipophorin receptor: the insect lipoprotein receptor. Resonance 18 748–755. (https://doi.org/10.1007/s12045-013-0096-1)

  • Rider BF & Mellon MG 1946 Colorimetric determination of nitrites. Industrial and Engineering Chemistry Analytical Edition 18 96–99.

  • Rodríguez-Vázquez M, Vaquero D, Parra-Peralbo E, Mejía-Morales JE & Culi J 2015 Drosophila lipophorin receptors recruit the lipoprotein LTP to the plasma membrane to mediate lipid uptake. PLoS Genetics 11 e1005356. (https://doi.org/10.1371/journal.pgen.1005356)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rotllant G, Wade NM, Arnold SJ, Coman GJ, Preston NP & Glencross BD 2015 Identification of genes involved in reproduction and lipid pathway metabolism in wild and domesticated shrimps. Marine Genomics 22 55–61. (https://doi.org/10.1016/j.margen.2015.04.001)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Santiago AC 1977 Successful spawning of cultured Penaeus monodon Fabricius after eyestalk ablation. Aquaculture 11 185–196. (https://doi.org/10.1016/0044-8486(77)90111-9)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shailender M, Amarnath D, Kishor B & Suresh BCH 2013 Effect of unilateral eyestalk ablation in reproductive cycle of Penaeus monodon (Fabricius) after spawning under laboratory conditions. International Journal of Chemical and Life Sciences 2 1121–1125.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Smyth G & Wettenhall J 2004 limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20 3705–3706. (https://doi.org/10.1093/bioinformatics/bth449)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Söderhäll I, Tangprasittipap A, Liu H, Sritunyalucksana K, Prasertsan P, Jiravanichpaisal P & Söderhäll K 2006 Characterization of a hemocyte intracellular fatty acid-binding protein from crayfish (Pacifastacus leniusculus) and shrimp (Penaeus monodon). FEBS Journal 273 2902–2912.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sorensen JG, Nielsen MM, Kruhoffer M, Justesen J & Loeschcke V 2005 Full genome gene expression analysis of the heat stress response in Drosophila melanogaster. Cell Stress Chaperones 10 312–328. (https://doi.org/10.1379/CSC-128R1.1)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Strickland JDH & Parsons TR 1972 A Practical Handbook of Seawater Analysis. Fisheries Research Board of Canada Bulletin.

  • Sui LY, Sun HX, Wu XG, Wille M, Cheng YX & Sorgeloos P 2011 Effect of dietary HUFA on tissue fatty acid composition and reproductive performance of Chinese mitten crab Eriocheir sinensis (H. Milne-Edwards) broodstock. Aquaculture International 19 269–282. (https://doi.org/10.1007/s10499-010-9379-7)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sun Y, Zhang Y, Liu Y, Xue S, Geng X, Hao T & Sun J 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 e95827. (https://doi.org/10.1371/journal.pone.0095827)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Treerattrakool S, Panyim S, Chan S, Withyachumnarnkul B & Udomkit A 2008 Molecular characterization of gonad-inhibiting hormone of Penaeus monodon and elucidation of its inhibitory role in vitellogenin expression by RNA interference. FEBS Journal 275 970–980. (https://doi.org/10.1111/j.1742-4658.2008.06266.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Uawisetwathana U, Leelatanawit R, Klanchui A, Prommoon J, Klinbunga S & Karoonuthaisiri N 2011 Insights into eyestalk ablation mechanism to induce ovarian maturation in the black tiger shrimp. PLoS ONE 6 e24427. (https://doi.org/10.1371/journal.pone.0024427)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vogt G 1994 Life-cycle and functional cytology of the hepatopancreatic cells of Astacus astacus (Crustacea, Decapoda). Zoomorphology 114 83–101. (https://doi.org/10.1007/BF00396642)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wang W, Wu X, Liu Z, Zheng H & Cheng Y 2014 Insights into hepatopancreatic functions for nutrition metabolism and ovarian development in the crab Portunus trituberculatus: gene discovery in the comparative transcriptome of different hepatopancreas stages. PLoS ONE 9 e84921. (https://doi.org/10.1371/journal.pone.0084921)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wei B, Yang Z, Wang J, Chen A, Shi Q & Cheng Y 2017 Effects of dietary lipids on the hepatopancreas transcriptome of Chinese mitten crab (Eriocheir sinensis). PLoS ONE 12 e0182087. (https://doi.org/10.1371/journal.pone.0182087)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wen XB, Chen LQ, Ai CX, Zhou ZL & Jiang HB 2001 Variation in lipid composition of Chinese mitten-handed crab, Eriocheir sinensis during ovarian maturation. Comparative Biochemistry and Physiology B 130 95–104. (https://doi.org/10.1016/S1096-4959(01)00411-0)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wongsurawat T, Leelatanawit R, Thamniemdee N, Uawisetwathana U, Karoonuthaisiri N, Menasveta P & Klinbunga S 2010 Identification of testis-relevant genes using in silico analysis from testis ESTs and cDNA microarray in the black tiger shrimp (Penaeus monodon). BMC Molecular Biology 11 55. (https://doi.org/10.1186/1471-2199-11-55)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wouters R, Lavens P, Nieto J & Sorgeloos P 2001a Penaeid shrimp broodstock nutrition: an updated review on research and development. Aquaculture 202 1–21. (https://doi.org/10.1016/S0044-8486(01)00570-1)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wouters R, Piguave X, Calderon J & Sorgeloos P 2001b Ovarian maturation and haemolymphatic vitellogenin concentration of Pacific white shrimp Litopeaneus vannamei (Boone) fed increasing levels of total dietary lipids and HUFA. Aquaculture Research 32 573–582. (https://doi.org/10.1046/j.1365-2109.2001.00580.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yan H, Xue M, Liu H, Wang L, Liu Q & Jiang L 2017 Energy reserves and gonad steroid levels during the reproductive cycle of the Japanese mantis shrimp Oratosquilla oratoria De Haan, 1844 (Stomatopoda: Squillidae) in Pikou Bay, Dalian, China. Journal of Crustacean Biology 37 99–108. (https://doi.org/10.1093/jcbiol/ruw016)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yu ZB, Mu CK, Song WW, Li RH, Chen YE & Wang CL 2015 Screening of genes related to ovarian development in the swimming crab, Portunus trituberculatus, by suppression subtractive hybridization. Genetics and Molecular Research Journal 14 18675–18686. (https://doi.org/10.4238/2015.December.28.16)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zeng X, Ye H, Yang Yn, Wang G & Huang H 2013 Molecular cloning and functional analysis of the fatty acid-binding protein (Sp-FABP) gene in the mud crab (Scylla paramamosain). Genetics and Molecular Biology 36 140–147. (https://doi.org/10.1590/S1415-47572013005000007)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zmora N, Trant J, Chan S-M & Chung JS 2007 Vitellogenin and its messenger RNA during ovarian development in the female blue crab, Callinectes sapidus: gene expression, synthesis, transport, and cleavage. Biology of Reproduction 77 138–146. (https://doi.org/10.1095/biolreprod.106.055483)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation