期刊论文详细信息
BMC Genomics
Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes
Gilles Le Moullac2  Yannick Gueguen2  Nabila Gaertner-Mazouni5  Emeline Lhuillier1  Christophe Klopp3  Peva Levy2  Arnaud Huvet4  Vaihiti Teaniniuraitemoana2 
[1] Present address : GeT-Purpan, GenoToul, UDEAR UMR 1065 CNRS/UPS/U1056 INSERM, CHU PURPAN, Place du Dr Baylac, TSA 40031, 31059 Toulouse Cedex 9, France;Ifremer, UMR 241 EIO, Labex CORAIL, BP 7004, 98719 Taravao, Tahiti, Polynésie Française;INRA, Sigenae, UR875, Auzeville, BP 52627, 31326 Castanet-Tolosan, France;Ifremer, UMR 6539 LEMAR, BP 70, 29280 Plouzané, France;Université de la Polynésie Française, UMR 241 EIO, Labex CORAIL, BP 6570, 98702 Faa’a, Tahiti, Polynésie Française
关键词: Sex determinism;    Differential expression;    Transcriptome;    Gametogenesis;    Pinctada margaritifera;   
Others  :  1216572
DOI  :  10.1186/1471-2164-15-491
 received in 2014-01-23, accepted in 2014-06-13,  发布年份 2014
PDF
【 摘 要 】

Background

Black pearl farming is based on culture of the blacklip pearl oyster Pinctada margaritifera (Mollusca, lophotrochozoa), a protandrous hermaphrodite species. At first maturation, all individuals are males. The female sex appears progressively from two years old, which represents a limitation for broodstock conditioning for aquaculture production. In marine mollusks displaying hermaphroditic features, data on sexual determinism and differentiation, including the molecular sex determining cascade, are scarce. To increase genomic resources and identify the molecular mechanisms whereby gene expression may act in the sexual dimorphism of P. margaritifera, we performed gonad transcriptome analysis.

Results

The gonad transcriptome of P. margaritifera was sequenced from several gonadic samples of males and females at different development stages, using a Next-Generation-Sequencing method and RNAseq technology. After Illumina sequencing, assembly and annotation, we obtained 70,147 contigs of which 62.2% shared homologies with existing protein sequences, and 9% showed functional annotation with Gene Ontology terms. Differential expression analysis identified 1,993 differentially expressed contigs between the different categories of gonads. Clustering methods of samples revealed that the sex explained most of the variation in gonad gene expression. K-means clustering of differentially expressed contigs showed 815 and 574 contigs were more expressed in male and female gonads, respectively. The analysis of these contigs revealed the presence of known specific genes coding for proteins involved in sex determinism and/or differentiation, such as dmrt and fem-1 like for males, or foxl2 and vitellogenin for females. The specific gene expression profiles of pmarg-fem1-like, pmarg-dmrt and pmarg-foxl2 in different reproductive stages (undetermined, sexual inversion and regression) suggest that these three genes are potentially involved in the sperm-oocyte switch in P. margaritifera.

Conclusions

The study provides a new transcriptomic tool to study reproduction in hermaphroditic marine mollusks. It identifies sex differentiation and potential sex determining genes in P. margaritifera, a protandrous hermaphrodite species.

【 授权许可】

   
2014 Teaniniuraitemoana et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150701083204373.pdf 2677KB PDF download
Figure 8. 50KB Image download
Figure 7. 121KB Image download
Figure 6. 204KB Image download
Figure 5. 86KB Image download
Figure 4. 118KB Image download
Figure 3. 104KB Image download
Figure 2. 57KB Image download
Figure 1. 280KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】
  • [1]Le Pennec M, Anastas M, Bichet H, Buestel D, Cochard J, Cochennec-Laureau N, Coeroli M, Conte E, Correia A, Fougerousse-Tsing A, Langy S, Le Moullac G, Lo C, Peltzer L, Pham A: Huître Perlière et Perle de Tahiti. Faaa: French Polynesia: HQ Imaging; 2010:204.
  • [2]Saavedra C, Bachère E: Bivalve genomics. Aquaculture 2006, 256:1-14.
  • [3]Ma S, Sun Z, Chen K: Review of bivalve genomics and proteomics. J Tianjin Agric Coll 2009, 41–45:50.
  • [4]Romero A, Novoa B, Figueras A: Genomics, immune studies and diseases in bivalve aquaculture. Invertebr Surviv J 2012, 9:110-121.
  • [5]Gueguen Y, Montagnani C, Joubert C, Marie B, Belliard C, Tayalé A, Fievet J, Levy P, Piquemal D, Marin F, Le Moullac G, Ky C-L, Garen P, Lo C, Saulnier D: Characterization of molecular processes involved in the pearl formation in Pinctada margaritifera for the sustainable development of pearl farming industry in French Polynesia. In Recent Adv Pearl Res. Edited by Watabe S, Maeyama K, Nagasawa H. Tokyo: TERRAPUB; 2013:183-193.
  • [6]Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cléon I, Cochennec-Laureau N, Gueguen Y, Montagnani C: Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics 2010, 11:613.
  • [7]Marie B, Joubert C, Tayalé A, Zanella-cléon I, Belliard C, Piquemal D: Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell. Proc Natl Acad Sci U S A 2012, 109:20986-20991.
  • [8]Pouvreau S, Gangnery A, Tiapari J, Lagarde F, Garnier M, Bodoy A: Gametogenic cycle and reproductive effort of the tropical blacklip pearl oyster, Pinctada margaritifera (Bivalvia: Pteriidae), cultivated in Takapoto atoll (French Polynesia). Aquat Living Resour 2000, 13:37-48.
  • [9]Fournier J, Levesque E, Pouvreau S, Le Pennec M, Le Moullac G: Influence of plankton concentration on gametogenesis and spawning of the black lip pearl oyster Pinctada margaritifera in Ahe atoll lagoon (Tuamotu Archipelago, French polynesia). Mar Pollut Bull 2012, 65:463-470.
  • [10]Arnaud-Haond S, Goyard E, Vonau V, Herbaut C, Prou J, Saulnier D: Pearl formation: persistence of the graft during the entire process of biomineralization. Mar Biotechnol 2007, 9:113-16.
  • [11]Ky C-L, Blay C, Sham-Koua M, Vanaa V, Lo C, Cabral P: Family effect on cultured pearl quality in black-lipped pearl oyster Pinctada margaritifera and insights for genetic improvement. Aquat Living Resour 2013, 26:133-145.
  • [12]Vahirua-Lechat I, Laure F, LeCoz JR, Bianchini JP, Bellais M, Le Moullac G: Changes in fatty acid and sterol composition during oogenesis in the pearl oyster Pinctada margaritifera. Aquac Res 2008, 39:1739-1746.
  • [13]Chávez-Villalba J, Soyez C, Huvet A, Gueguen Y, Lo C, Moullac Le: G: Determination of gender in the pearl oyster Pinctada margaritifera. J Shellfish Res 2011, 30:231-240.
  • [14]Le Moullac G, Soyez C, Sham-Koua M, Levy P, Moriceau J, Vonau V, Maihota M, Cochard JC: Feeding the pearl oyster Pinctada margaritifera during reproductive conditioning. Aquac Res 2013, 44:404-411.
  • [15]Saucedo P, Monteforte M: Breeding cycle of pearl oysters Pinctada mazatlanica and Pteria sterna (Bivalvia: Pteriidae) at Bahia de la Paz, Baja California Sur, Mexico. J Shellfish Res 1997, 16:103-110.
  • [16]Tranter D: Reproduction in australian pearl oysters (Lamellibranchia). III. Pinctada albina (Lamarck): Breeding season and sexuality. Mar Freshw Res 1958, 9:191-216.
  • [17]Kimani E, Mavuti K, Mukiama T: The reproductive activity of the pearl oyster Pinctada imbricata Röding 1798 (Pteriidae) in Gazi Bay, Kenya. Trop Zool 2006, 19:159-174.
  • [18]Hwang J-J: Reproductive cycles of the pearl oysters, Pinctada fucata (Gould) and Pinctada margaritifera (Linnaeus) (Bivalvia: Pteriidae) in southwestern Taiwan waters. J Mar Sci Technol 2007, 15:67-75.
  • [19]Derbali A, Jarboui O, Ghorbel M, Dhieb K: Reproductive biology of the pearl oyster, Pinctada radiata (Mollusca: Pteriidae), in northern Kerkennah Island (Gulf of Gabes). Cah Biol Mar 2009, 50:215-222.
  • [20]Tranter D: Reproduction in australian pearl oysters (Lamellibranchia). IV. Pinctada margaritifera (Linnaeus). Mar Freshw Res 1958, 9:509-525.
  • [21]Penman DJ, Piferrer F: Fish gonadogenesis. Part I: Genetic and environmental mechanisms of sex determination. Rev Fish Sci 2008, 16:16-34.
  • [22]Piferrer F, Guiguen Y: Fish gonadogenesis. Part II: Molecular biology and genomics of sex differentiation. Rev Fish Sci 2008, 16:35-55.
  • [23]Valenzuela DM, Murphy AJ, Frendewey D, Gale NW, Economides AN, Auerbach W, Poueymirou WT, Adams NC, Rojas J, Yasenchak J, Chernomorsky R, Boucher M, Elsasser AL, Esau L, Zheng J, Griffiths JA, Wang X, Su H, Xue Y, Dominguez MG, Noguera I, Torres R, Macdonald LE, Stewart AF, DeChiara TM, Yancopoulos GD: High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat Biotechnol 2003, 21:652-9.
  • [24]Chávez-Villalba J, Cochard J-C, Le Pennec M, Barret J, Enríquez-Díaz M, Cáceres-Martínez C: Effect of temperature and feeding regimes on gametogenesis and larval production in the oyster Crassotrea gigas. J Shellfish Res 2003, 22:721-731.
  • [25]Dutertre M, Beninger PG, Barillé L, Papin M, Rosa P, Barillé A-L, Haure J: Temperature and seston quantity and quality effects on field reproduction of farmed oysters, Crassostrea gigas, in Bourgneuf Bay, France. Aquat Living Resour 2009, 22:319-329.
  • [26]Saout C, Quéré C, Donval A, Paulet Y-M, Samain J-F: An experimental study of the combined effects of temperature and photoperiod on reproductive physiology of Pecten maximus from the Bay of Brest (France). Aquaculture 1999, 172:301-314.
  • [27]Thielley M: Etude cytologique de la gamétogenèse, de la sex-ratio et du cycle de reproduction chez l’huître perlière Pinctada margaritifera (L) var. cumingii (Jameson), (mollusque, bivalves). Comparaison avec le cycle de Pinctada maculata (Gould). PhD thesis. Université française du pacifique; 1993:233.
  • [28]Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf A-M, Lovell-Badge R, Goodfellow PN: A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990, 346:240-244.
  • [29]Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R: Male development of chromosomally female mice transgenic for Sry. Nature 1991, 351:117-121.
  • [30]Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M: DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 2002, 417:559-563.
  • [31]Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M: A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A 2008, 105:2469-2474.
  • [32]Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH: The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009, 461:267-271.
  • [33]Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strüssmann CA: A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A 2012, 109:2955-2959.
  • [34]Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M: Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 2012, 191:163-170.
  • [35]Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadai T, Venkatesh B, Suzuki Y, Kikuchi K: A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet 2012, 8:e1002798.
  • [36]Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, Cabau C, Bouchez O, Fostier A, Guiguen Y: An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol 2012, 22:1423-1428.
  • [37]Koopman P: Sry, Sox9 and mammalian sex determination. In Genes Mech Vertebr Sex Determ. Volume 91. Edited by Scherer G, Schmid M. Basel: Birkhäuser Basel; 2001::25-56. Experientia Supplementum
  • [38]Ottolenghi C: Foxl2 is required for commitment to ovary differentiation. Hum Mol Genet 2005, 14:2053-2062.
  • [39]Guo X, Hedgecock D, Hershberger WK, Cooper K, Allen K: Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution 1998, 52:394-402.
  • [40]Hedrick PW, Hedgecock D: Sex determination: genetic models for oysters. J Hered 2010, 101:602-611.
  • [41]Naimi A, Martinez A-S, Specq M-L, Mrac A, Diss B, Mathieu M, Sourdaine P: Identification and expression of a factor of the DM family in the oyster Crassostrea gigas. Comp Biochem Physiol A Mol Integr Physiol 2009, 152:189-196.
  • [42]Naimi A, Martinez A-S, Specq M-L, Diss B, Mathieu M, Sourdaine P: Molecular cloning and gene expression of Cg-Foxl2 during the development and the adult gametogenetic cycle in the oyster Crassostrea gigas. Comp Biochem Physiol B Biochem Mol Biol 2009, 154:134-142.
  • [43]Santerre C, Sourdaine P, Martinez A-S: Expression of a natural antisense transcript of Cg-Foxl2 during the gonadic differentiation of the oyster Crassostrea gigas: first demonstration in the gonads of a lophotrochozoa species. Sex Dev 2012, 6:210-21.
  • [44]Matsumoto T, Masaoka T, Fujiwara A, Nakamura Y, Satoh N, Awaji M: Reproduction-related genes in the pearl oyster genome. Zoolog Sci 2013, 30:826-850.
  • [45]Dheilly NM, Lelong C, Huvet A, Favrel P: Development of a Pacific oyster (Crassostrea gigas) 31,918-feature microarray: identification of reference genes and tissue-enriched expression patterns. BMC Genomics 2011, 12:468.
  • [46]Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
  • [47]Takeuchi T, Kawashima T, Koyanagi R, Gyoja F, Tanaka M, Ikuta T, Shoguchi E, Fujiwara M, Shinzato C, Hisata K, Fujie M, Usami T, Nagai K, Maeyama K, Okamoto K, Aoki H, Ishikawa T, Masaoka T, Fujiwara A, Endo K, Endo H, Nagasawa H, Kinoshita S, Asakawa S, Watabe S, Satoh N: Draft genome of the pearl oyster Pinctada fucata: a platform for understanding bivalve biology. DNA Res 2012, 19:117-130.
  • [48]Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, Yang P, Zhang L, Wang X, Qi H, Xiong Z, Que H, Xie Y, Holland PWH, Paps J, Zhu Y, Wu F, Chen Y, Wang J, Peng C, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z, Zhu Q, Feng Y, Mount A, Hedgecock D, et al.: The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490:49-54.
  • [49]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
  • [50]Tamura K, Stecher G, Peterson D, Filipski A, Kumar S: MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013, 30:2725-2729.
  • [51]Anders S, Huber W: Differential expression analysis for sequence count data. Genome Biol 2010, 11:R106.
  • [52]Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995, 57:289-300.
  • [53]Howe EA, Sinha R, Schlauch D, Quackenbush J: RNA-Seq analysis in MeV. Bioinformatics 2011, 27:3209-3210.
  • [54]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 2001, 25:402-8.
  • [55]Andersen CL, Jensen JL, Ørntoft TF: Normalization of real-time quantitative reverse transcription-PCR data : a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Reseach 2004, 64:5245-5250.
  • [56]Kopp A: Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet 2012, 28:175-184.
  • [57]Kanai Y, Hiramatsu R, Matoba S, Kidokoro T: From SRY to SOX9: mammalian testis differentiation. J Biochem 2005, 138:13-9.
  • [58]Doniach T, Hodgkin J: A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev Biol 1984, 106:223-235.
  • [59]Wallace RA: Vitellogenesis and oocyte growth in nonmammalian vertebrates. In Dev Biol Vol 1 Oogenes. Edited by Browder LW. Boston, MA: Springer US; 1985:127-177.
  • [60]Kueng P, Nikolova Z, Djonov V, Hemphill A, Rohrbach V, Boehlen D, Zuercher G, Andres A-C, Ziemiecki A: A novel family of serine/threonine kinases participating in spermiogenesis. J Cell Biol 1997, 139:1851-1859.
  • [61]Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier A-C, Klugmann C, Klasen C, Holter NI, Riethmacher D, Schütz G, Cooney AJ, Lovell-Badge R, Treier M: Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
  • [62]Strauss TJ, Castrillon DH, Hammes SR: GATA-like protein-1 (GLP-1) is required for normal germ cell development during embryonic oogenesis. Reproduction 2011, 141:173-181.
  • [63]Oliver B, Pauli D, Mahowald AP: Genetic evidence that the ovo locus is involved in Drosophila germ line sex determination. Genetics 1990, 125:535-550.
  • [64]Redon E, Bosseboeuf A, Rocancourt C, Da Silva C, Wincker P, Mazan S, Sourdaine P: Stage-specific gene expression during spermatogenesis in the dogfish (Scyliorhinus canicula). Reproduction 2010, 140:57-71.
  • [65]Llera-Herrera R, García-Gasca A, Abreu-Goodger C, Huvet A, Ibarra AM: Identification of male gametogenesis expressed genes from the scallop Nodipecten subnodosus by suppressive subtraction hybridization and pyrosequencing. PLoS One 2013, 8:e73176.
  • [66]Wang S, Hou R, Bao Z, Du H, He Y, Su H, Zhang Y, Fu X, Jiao W, Li Y, Zhang L, Wang S, Hu X: Transcriptome sequencing of Zhikong scallop (Chlamys farreri) and comparative transcriptomic analysis with Yesso scallop (Patinopecten yessoensis). PLoS One 2013, 8:e63927.
  • [67]Huang X-D, Zhao M, Liu W-G, Guan Y-Y, Shi Y, Wang Q, Wu S-Z, He M-X: Gigabase-scale transcriptome analysis on four species of pearl oysters. Mar Biotechnol 2013, 15:253-264.
  • [68]Erdman SE, Burtis KC: The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J 1993, 12:527-535.
  • [69]Feng Z, Shao M, Sun D, Zhang Z: Cloning, characterization and expression analysis of Cf-dmrt4-like gene in Chlamys farreri. J Fish Sci China 2010, 17:930-940.
  • [70]Yu F-F, Wang M-F, Zhou L, Gui J-F, Yu X-Y: Molecular cloning and expression characterization of Dmrt2 in Akoya pearl oysters, Pinctada martensii. J Shellfish Res 2011, 30:247-254.
  • [71]Yu F-F, Wang M-F, Zhou L, Gui J-F, Yu X-Y: Cloning and expression characterization of Dmrt5 in Pinctada martensii. Acta Hydrobiol Sin 2009, 33:844-850.
  • [72]Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, Pasantes J, Bricarelli FD, Keutel J, Hustert E, Wolf U, Tommerup N, Schempp W, Scherer G: Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 1994, 79:1111-1120.
  • [73]Knower KC, Kelly S, Ludbrook LM, Bagheri-Fam S, Sim H, Bernard P, Sekido R, Lovell-Badge R, Harley VR: Failure of SOX9 regulation in 46XY disorders of sex development with SRY, SOX9 and SF1 mutations. PLoS One 2011, 6:e17751.
  • [74]Barrionuevo F, Scherer G: SOX E genes: SOX9 and SOX8 in mammalian testis development. Int J Biochem Cell Biol 2010, 42:433-436.
  • [75]Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P: A male-specific role for SOX9 in vertebrate sex determination. Development 1996, 122:2813-2822.
  • [76]da Silva Morais S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R: Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 1996, 14:62-68.
  • [77]Spotila LD, Spotila JR, Hall SE: Sequence and expression analysis of WT1 and Sox9 in the red-eared slider turtle, Trachemys scripta. J Exp Zool 1998, 281:417-427.
  • [78]Santerre C, Sourdaine P, Adeline B, Martinez A-S: Cg-SoxE and Cg-β-catenin, two new potential actors of the sex-determining pathway in a hermaphrodite lophotrochozoan, the Pacific oyster Crassostrea gigas. Comp Biochem Physiol A Mol Integr Physiol 2014, 167:68-76.
  • [79]Hodgkin J: Sex determination in the nematode C. elegans: analysis of TRA-3 suppressors and characterization of FEM genes. Genetics 1986, 114:15-52.
  • [80]Ventura-Holman T, Seldin MF, Li W, Maher JF: The murine fem1 gene family: homologs of the Caenorhabditis elegans sex-determination protein FEM-1. Genomics 1998, 54:221-230.
  • [81]Krakow D, Sebald E, King LM, Cohn DH: Identification of human FEM1A, the ortholog of a C. elegans sex-differentiation gene. Gene 2001, 279:213-219.
  • [82]Ventura-Holman T, Maher JF: Sequence, organization, and expression of the human FEM1B gene. Biochem Biophys Res Commun 2000, 267:317-320.
  • [83]Ventura-Holman T, Lu D, Si X, Izevbigie EB, Maher JF: The Fem1c genes: conserved members of the Fem1 gene family in vertebrates. Gene 2003, 314:133-139.
  • [84]Adell T, Müller WEG: Isolation and characterization of five Fox (Forkhead) genes from the sponge Suberites domuncula. Gene 2004, 334:35-46.
  • [85]Magie CR, Pang K, Martindale MQ: Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 2005, 215:618-630.
  • [86]Tu Q, Brown CT, Davidson EH, Oliveri P: Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev Biol 2006, 300:49-62.
  • [87]Shimeld SM, Boyle MJ, Brunet T, Luke GN, Seaver EC: Clustered Fox genes in lophotrochozoans and the evolution of the bilaterian Fox gene cluster. Dev Biol 2010, 340:234-248.
  • [88]Liu X-L, Zhang Z-F, Shao M-Y, Liu J-G, Muhammad F: Sexually dimorphic expression of foxl2 during gametogenesis in scallop Chlamys farreri, conserved with vertebrates. Dev Genes Evol 2012, 222:279-286.
  • [89]Fabioux C, Corporeau C, Quillien V, Favrel P, Huvet A: In vivo RNA interference in oyster - vasa silencing inhibits germ cell development. FEBS J 2009, 276:2566-2573.
  • [90]Dheilly NM, Lelong C, Huvet A, Kellner K, Dubos M-P, Riviere G, Boudry P, Favrel P: Gametogenesis in the Pacific oyster Crassostrea gigas: a microarrays-based analysis identifies sex and stage specific genes. PLoS One 2012, 7:e36353.
  • [91]Sousa JT, Milan M, Bargelloni L, Pauletto M, Matias D, Joaquim S, Matias AM, Quillien V, Leitão A, Huvet A: A microarray-based analysis of gametogenesis in two Portuguese populations of the European clam Ruditapes decussatus. PLoS One 2014, 9:e92202.
  • [92]Zanetti S, Grinschgl S, Meola M, Belfiore M, Rey S, Bianchi P, Puoti A: The sperm-oocyte switch in the C. elegans hermaphrodite is controlled through steady-state levels of the fem-3 mRNA. RNA 2012, 18:1385-1394.
  • [93]Santerre C, Sourdaine P, Marc N, Mingant C, Robert R, Martinez A-S: Oyster sex determination is influenced by temperature - first clues in spat during first gonadic differentiation and gametogenesis. Comp Biochem Physiol A Mol Integr Physiol 2013, 165:61-69.
  • [94]Bedard N, Yang Y, Gregory M, Cyr DG, Suzuki J, Yu X, Chian R-C, Hermo L, O’Flaherty C, Smith CE, Clarke HJ, Wing SS: Mice lacking the USP2 deubiquitinating enzyme have severe male subfertility associated with defects in fertilization and sperm motility. Biol Reprod 2011, 85:594-604.
  • [95]Sutovsky P, Moreno R, Ramalho-santos J, Dominko T, Thompson WE, Schatten G: A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci 2001, 114:1665-1675.
  • [96]Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, Kodama E, Takizawa S, Yokosawa H: Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci U S A 2002, 99:1223-1228.
  • [97]Moor RM, Dai Y, Lee C, Fulka J: Oocyte maturation and embryonic failure. Hum Reprod Update 1998, 4:223-236.
  • [98]Murchison EP, Stein P, Xuan Z, Pan H, Zhang MQ, Schultz RM, Hannon GJ: Critical roles for Dicer in the female germline. Genes Dev 2007, 21:682-693.
  • [99]Bettegowda A, Smith GW: Mechanisms of maternal mRNA regulation: implications for mammalian early embryonic development. Front Biosci 2007, 12:3713-3726.
  • [100]Kably Ambe A, Ruiz Anguas J, Carballo Mondragón E, de Lau Corona C, Karchmer Krivitsky S: Correlation between follicle levels of superoxide dismutase and oocyte quality, fertilization rates and embryo development. Ginecol Obstet Mex 2004, 72:335-344.
  • [101]Allegrucci C, Thurston A, Lucas E, Young L: Epigenetics and the germline. Reproduction 2005, 129:137-149.
  • [102]Li E: Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002, 3:662-673.
  • [103]Gavery MR, Roberts SB: Predominant intragenic methylation is associated with gene expression characteristics in a bivalve mollusc. PeerJ 2013, 1:e215.
  • [104]Riviere G, Wu G-C, Fellous A, Goux D, Sourdaine P, Favrel P: DNA methylation is crucial for the early development in the oyster C. gigas. Mar Biotechnol 2013, 15:739-753.
  • [105]Roberts SB, Gavery MR: Is there a relationship between DNA methylation and phenotypic plasticity in invertebrates? Front Physiol 2012, 2:116.
  文献评价指标  
  下载次数:103次 浏览次数:339次