Domestication may affect the maternal mRNA profile in unfertilized eggs, potentially impacting the embryonic development of Eurasian perch (Perca fluviatilis)


Autoři: Tainá Rocha de Almeida aff001;  Maud Alix aff001;  Aurélie Le Cam aff002;  Christophe Klopp aff003;  Jérôme Montfort aff002;  Lola Toomey aff001;  Yannick Ledoré aff001;  Julien Bobe aff002;  Dominique Chardard aff001;  Bérénice Schaerlinger aff001;  Pascal Fontaine aff001
Působiště autorů: UR AFPA, University of Lorraine, INRA, Nancy, France aff001;  LPGP, UR1037 Fish Physiology and Genomics, INRA, Rennes, France aff002;  Sigenae, MIAT, INRA, Castanet-Tolosan, Toulouse, France aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226878

Souhrn

Domestication is an evolutionary process during which we expect populations to progressively adapt to an environment controlled by humans. It is accompanied by genetic and presumably epigenetic changes potentially leading to modifications in the transcriptomic profile in various tissues. Reproduction is a key function often affected by this process in numerous species, regardless of the mechanism. The maternal mRNA in fish eggs is crucial for the proper embryogenesis. Our working hypothesis is that modifications of maternal mRNAs may reflect potential genetic and/or epigenetic modifications occurring during domestication and could have consequences during embryogenesis. Consequently, we investigated the trancriptomic profile of unfertilized eggs from two populations of Eurasian perch. These two populations differed by their domestication histories (F1 vs. F7+–at least seven generations of reproduction in captivity) and were genetically differentiated (FST = 0.1055, p<0.05). A broad follow up of the oogenesis progression failed to show significant differences during oogenesis between populations. However, the F1 population spawned earlier with embryos presenting an overall higher survivorship than those from the F7+ population. The transcriptomic profile of unfertilized eggs showed 358 differentially expressed genes between populations. In conclusion, our data suggests that the domestication process may influence the regulation of the maternal transcripts in fish eggs, which could in turn explain differences of developmental success.

Klíčová slova:

Gene expression – Embryos – Transcriptome analysis – Domestic animals – Spawning – Microarrays – Fish farming – Oogenesis


Zdroje

1. Price EO. Behavioral Aspects of Animal Domestication. Q Rev Biol. 1984;59(1):1–32.

2. Price EO. Behavioral development in animals undergoing domestication. Appl Anim Behav Sci. 1999 Dec;65(3):245–71.

3. Christie MR, Marine ML, Fox SE, French RA, Blouin MS. A single generation of domestication heritably alters the expression of hundreds of genes. Nat Commun. 2016 Feb 17;7:10676. doi: 10.1038/ncomms10676 26883375

4. Beaumont C, Roussot O, Marissal-Avry N, Mormede P, Prunet P, Roubertoux P. Génétique et adaptation des animaux d’élevage: introduction. Inra Prod Anim. 2002;15(5):343–8.

5. Mignon-Grasteau S, Boissy A, Bouix J, Faure J-M, Fisher AD, Hinch GN, et al. Genetics of adaptation and domestication in livestock. Livest Prod Sci. 2005 Apr 1;93(1):3–14.

6. Vogt G. Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: insights from clonal, invasive, polyploid, and domesticated animals. Environ Epigenetics [Internet]. 2017 Mar 29 [cited 2019 May 28];3(1). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5804542/

7. Luyer JL, Laporte M, Beacham TD, Kaukinen KH, Withler RE, Leong JS, et al. Parallel epigenetic modifications induced by hatchery rearing in a Pacific salmon. Proc Natl Acad Sci. 2017 Dec 5;114(49):12964–9. doi: 10.1073/pnas.1711229114 29162695

8. Gavery MR, Nichols KM, Goetz GW, Middleton MA, Swanson P. Characterization of Genetic and Epigenetic Variation in Sperm and Red Blood Cells from Adult Hatchery and Natural-Origin Steelhead, Oncorhynchus mykiss. G3 Genes Genomes Genet. 2018 Nov 1;8(11):3723–36.

9. Rodriguez Barreto D, Garcia de Leaniz C, Verspoor E, Sobolewska H, Coulson M, Consuegra S. DNA Methylation Changes in the Sperm of Captive-Reared Fish: A Route to Epigenetic Introgression in Wild Populations. Mol Biol Evol [Internet]. [cited 2019 Jul 26]; Available from: https://academic.oup.com/mbe/advance-article/doi/10.1093/molbev/msz135/5513369

10. Anastasiadi D, Piferrer F. Epimutations in developmental genes underlie the onset of domestication in farmed European sea bass. Wittkopp P, editor. Mol Biol Evol. 2019 Jul 10;msz153.

11. Dobney K, Larson G. Genetics and animal domestication: new windows on an elusive process. J Zool. 2006;269(2):261–71.

12. Waaij VD, H E. A resource allocation model describing consequences of artificial selection under metabolic stress. J Anim Sci. 2004 Apr 1;82(4):973–81. doi: 10.2527/2004.824973x 15080316

13. Farquharson KA, Hogg CJ, Grueber CE. A meta-analysis of birth-origin effects on reproduction in diverse captive environments. Nat Commun. 2018 Mar 13;9(1):1055. doi: 10.1038/s41467-018-03500-9 29535319

14. Pelegri F. Maternal factors in zebrafish development. Dev Dyn. 2003 Nov;228(3):535–54. doi: 10.1002/dvdy.10390 14579391

15. Bicskei B, Bron JE, Glover KA, Taggart JB. A comparison of gene transcription profiles of domesticated and wild Atlantic salmon (Salmo salar L.) at early life stages, reared under controlled conditions. Bmc Genomics. 2014;15(1):884.

16. Bicskei B, Taggart JB, Glover KA, Bron JE. Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression. Genet Sel Evol [Internet]. 2016 Dec [cited 2018 Mar 6];48(1). Available from: http://www.gsejournal.org/content/48/1/20

17. Yeates SE, Einum S, Fleming IA, Holt WV, Gage MJG. Assessing risks of invasion through gamete performance: farm Atlantic salmon sperm and eggs show equivalence in function, fertility, compatibility and competitiveness to wild Atlantic salmon. Evol Appl. 2014 Apr 1;7(4):493–505. doi: 10.1111/eva.12148 24822083

18. Lanes CFC, Bizuayehu TT, de Oliveira Fernandes JM, Kiron V, Babiak I. Transcriptome of Atlantic Cod (Gadus morhua L.) Early Embryos from Farmed and Wild Broodstocks. Mar Biotechnol. 2013 Dec;15(6):677–94. doi: 10.1007/s10126-013-9527-y 23887676

19. Lanes CFC, Bizuayehu TT, Bolla S, Martins C, de Oliveira Fernandes JM, Bianchini A, et al. Biochemical composition and performance of Atlantic cod (Gadus morhua L.) eggs and larvae obtained from farmed and wild broodstocks. Aquaculture. 2012 Jan;324–325:267–75.

20. Zupa R, Rodríguez C, Mylonas CC, Rosenfeld H, Fakriadis I, Papadaki M, et al. Comparative Study of Reproductive Development in Wild and Captive-Reared Greater Amberjack Seriola dumerili (Risso, 1810). Qiu G-F, editor. PLOS ONE. 2017 Jan 5;12(1):e0169645. doi: 10.1371/journal.pone.0169645 28056063

21. Khendek A, Alix M, Viot S, Ledoré Y, Rousseau C, Mandiki R, et al. How does a domestication process modulate oogenesis and reproduction performance in Eurasian perch? Aquaculture. 2017 Apr;473:206–14.

22. Křišt’an J, Stejskal V, Policar T. Comparison of reproduction characteristics and broodstock mortality in farmed and wild eurasian perch (Perca fluviatilis L.) females during spawning season under controlled conditions. Turk J Fish Aquat Sci. 2012;12(2):191–197.

23. Teletchea F, Fontaine P. Levels of domestication in fish: implications for the sustainable future of aquaculture. Fish Fish. 2014 Jun 1;15(2):181–95.

24. Ben Khadher S, Fontaine P, Milla S, Agnèse J-F, Teletchea F. Genetic characterization and relatedness of wild and farmed Eurasian perch (Perca fluviatilis): Possible implications for aquaculture practices. Aquac Rep. 2016 May 1;3:136–46.

25. Stepien CA, Haponski AE. Taxonomy, Distribution, and Evolution of the Percidae. In: Kestemont P, Dabrowski K, Summerfelt RC, editors. Biology and Culture of Percid Fishes [Internet]. Dordrecht: Springer Netherlands; 2015 [cited 2018 Mar 12]. p. 3–60. Available from: http://link.springer.com/10.1007/978-94-017-7227-3_1

26. Overton JL, Toner D, Policar T, Kucharczyk D. Commercial Production: Factors for Success and Limitations in European Percid Fish Culture. In: Kestemont P, Dabrowski K, Summerfelt RC, editors. Biology and Culture of Percid Fishes: Principles and Practices [Internet]. Dordrecht: Springer Netherlands; 2015 [cited 2019 May 29]. p. 881–90. Available from: https://doi.org/10.1007/978-94-017-7227-3_35

27. Steenfeldt S, Fontaine P, Overton JL, Policar T, Toner D, Falahatkar B, et al. Current Status of Eurasian Percid Fishes Aquaculture. In: Kestemont P, Dabrowski K, Summerfelt RC, editors. Biology and Culture of Percid Fishes: Principles and Practices [Internet]. Dordrecht: Springer Netherlands; 2015 [cited 2019 May 29]. p. 817–41. Available from: https://doi.org/10.1007/978-94-017-7227-3_32

28. Fontaine P, Wang N, Hermelink B. Broodstock Management and Control of the Reproductive Cycle. In: Kestemont P, Dabrowski K, Summerfelt RC, editors. Biology and Culture of Percid Fishes [Internet]. Springer Netherlands; 2015 [cited 2017 Mar 20]. p. 103–22. Available from: http://link.springer.com.bases-doc.univ-lorraine.fr/chapter/10.1007/978-94-017-7227-3_3

29. Gillet C, Dubois JP. A survey of the spawning of perch (Perca fluviatilis), pike (Esox lucius), and roach (Rutilus rutilus), using artificial spawning substrates in lakes. Hydrobiologia. 1995;300(1):409–415.

30. Wang N, Teletchea F, Kestemont P, Milla S, Fontaine P. Photothermal control of the reproductive cycle in temperate fishes: Photothermal control of reproduction. Rev Aquac. 2010 Dec;2(4):209–22.

31. Migaud H, Bell G, Cabrita E, McAndrew B, Davie A, Bobe J, et al. Gamete quality and broodstock management in temperate fish. Rev Aquac. 2013 May;5:S194–223.

32. Abdulfatah A, Fontaine P, Kestemont P, Gardeur J-N, Marie M. Effects of photothermal kinetics and amplitude of photoperiod decrease on the induction of the reproduction cycle in female Eurasian perch Perca fluviatilis. Aquaculture. 2011 Dec;322–323:169–76.

33. Sulistyo I. Reproductive cycle and plasma levels of sex steroids in female Eurasian perch Perca fluviatilis. Aquat Living Resour. 1998;11(2):101–10.

34. Schaerlinger B, Żarski D. Evaluation and Improvements of Egg and Larval Quality in Percid Fishes. In: Kestemont P, Dabrowski K, Summerfelt RC, editors. Biology and Culture of Percid Fishes [Internet]. Dordrecht: Springer Netherlands; 2015 [cited 2017 Mar 20]. p. 193–223. Available from: http://link.springer.com/10.1007/978-94-017-7227-3_6

35. Migaud H, Fontaine P, Kestemont P, Wang N, Brun-Bellut J. Influence of photoperiod on the onset of gonadogenesis in Eurasian perch Perca fluviatilis. Aquaculture. 2004 Nov;241(1–4):561–74.

36. Ben Ammar I, Teletchea F, Milla S, Ndiaye WN, Ledoré Y, Missaoui H, et al. Continuous lighting inhibits the onset of reproductive cycle in pikeperch males and females. Fish Physiol Biochem. 2015 Apr;41(2):345–56. doi: 10.1007/s10695-014-9987-7 25233876

37. Gabe M. Techniques histologiques. Paris: Masson; 1968. vi, 1113.

38. Rinchard J, Kestemont P. Comparative study of reproductive biology in single- and multiple-spawner cyprinid fish. I. Morphological and histological features. J Fish Biol. 1996;49(5):883–94.

39. Żarski D, Bokor Z, Kotrik L, Urbanyi B, Horváth A, Targońska K, et al. A new classification of a preovulatory oocyte maturation stage suitable for the synchronization of ovulation in controlled reproduction of Eurasian perch, Perca fluviatilis L. Reprod Biol. 2011 Nov 1;11(3):194–209. doi: 10.1016/s1642-431x(12)60066-7 22139334

40. Żarski D, Horváth á., Kotrik L, Targońska K, Palińska K, Krejszeff S, et al. Effect of different activating solutions on the fertilization ability of Eurasian perch, Perca fluviatilis L., eggs. J Appl Ichthyol. 2012 Dec;28(6):967–72.

41. Alix M, Chardard D, Ledoré Y, Fontaine P, Schaerlinger B. An alternative developmental table to describe non-model fish species embryogenesis: application to the description of the Eurasian perch (Perca fluviatilis L. 1758) development. EvoDevo [Internet]. 2015 Dec [cited 2016 Sep 23];6(1). Available from: http://www.evodevojournal.com/content/6/1/39 doi: 10.1186/2041-9139-6-3

42. Alix M, Zarski D, Chardard D, Fontaine P, Schaerlinger B. Deformities in newly hatched embryos of Eurasian perch populations originating from two different rearing systems. J Zool. 2017 Jun;302(2):126–37.

43. Pasquier J, Cabau C, Nguyen T, Jouanno E, Severac D, Braasch I, et al. Gene evolution and gene expression after whole genome duplication in fish: the PhyloFish database. BMC Genomics [Internet]. 2016 Dec [cited 2017 Mar 20];17(1). Available from: http://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-016-2709-z

44. Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008 Apr 15;36(10):3420–35. doi: 10.1093/nar/gkn176 18445632

45. Ozerov MY, Ahmad F, Gross R, Pukk L, Kahar S, Kisand V, et al. Highly Continuous Genome Assembly of Eurasian Perch (Perca fluviatilis) Using Linked-Read Sequencing. G3 Genes Genomes Genet. 2018 Dec 1;8(12):3737–43.

46. Mi H, Muruganujan A, Huang X, Ebert D, Mills C, Guo X, et al. Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0). Nat Protoc. 2019 Mar;14(3):703. doi: 10.1038/s41596-019-0128-8 30804569

47. Aljanabi S. Universal and rapid salt-extraction of high quality genomic DNA for PCR- based techniques. Nucleic Acids Res. 1997 Nov 15;25(22):4692–3. doi: 10.1093/nar/25.22.4692 9358185

48. Ben Khadher S, Agnèse J-F, Milla S, Teletchea F, Fontaine P. Patterns of genetic structure of Eurasian perch (Perca fluviatilis L.) in Lake Geneva at the end of the spawning season. J Gt Lakes Res. 2015 Sep;41(3):846–52.

49. Leclerc D, Wirth T, Bernatchez L. Isolation and characterization of microsatellite loci in the yellow perch (Perca flavescens), and cross- species amplification within the family Percidae. Mol Ecol. 2000 Jul;9(7):995–7. doi: 10.1046/j.1365-294x.2000.00939-3.x 10886663

50. Wirth T, Saint-Laurent R, Bernatchez L. Isolation and characterization of microsatellite loci in the walleye (Stizostedion vitreum), and cross-species amplification within the family Percidae. Mol Ecol. 1999 Nov;8(11):1960–2. doi: 10.1046/j.1365-294x.1999.00778-3.x 10620241

51. Borer SO, Miller LM, Kapuscinski AR. Microsatellites in walleye Stizostedion vitreum. Mol Ecol. 1999;8(2):336–8. 10065550

52. Li L, Wang HP, Givens C, Czesny S, Brown B. Isolation and characterization of microsatellites in yellow perch (Perca flavescens). Mol Ecol Notes. 2007;7(4):600–3.

53. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012 Jun 15;28(12):1647–9. doi: 10.1093/bioinformatics/bts199 22543367

54. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, Chikli L, et al. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Montpellier, France: Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II; 2004.

55. Cavanaugh JE, Neath AA. The Akaike information criterion: Background, derivation, properties, application, interpretation, and refinements. WIREs Comput Stat. 2019;11(3):e1460.

56. R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing. [Internet]. Vienna, Austria.; Available from: URL https://www.R-project.org/.

57. Hedrick PW. Perspective: Highly Variable Loci and Their Interpretation in Evolution and Conservation. Evolution. 1999;53(2):313–8. doi: 10.1111/j.1558-5646.1999.tb03767.x 28565409

58. Dekens MPS, Pelegri FJ, Maischein H-M, Nüsslein-Volhard C. The maternal-effect gene futile cycle is essential for pronuclear congression and mitotic spindle assembly in the zebrafish zygote. Dev Camb Engl. 2003 Sep;130(17):3907–16.

59. McGinnity P, Prodohl P, Ferguson A, Hynes R, Maoileidigh N o., Baker N, et al. Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proc R Soc B Biol Sci. 2003 Dec 7;270(1532):2443–50.

60. Lund I, Steenfeldt SJ, Suhr KI, Hansen BW. A comparison of fatty acid composition and quality aspects of eggs and larvae from cultured and wild broodstock of common sole (Solea solea L.). Aquac Nutr. 2008 Dec;14(6):544–55.

61. Bicskei B, Taggart JB, Glover KA, Bron JE. Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression. Genet Sel Evol [Internet]. 2016 Dec [cited 2018 Mar 6];48(1). Available from: http://www.gsejournal.org/content/48/1/20

62. Huang Y, Wange RL. T Cell Receptor Signaling: Beyond Complex Complexes. J Biol Chem. 2004 Jul 9;279(28):28827–30. doi: 10.1074/jbc.R400012200 15084594

63. Partula S. Surface markers of fish T-cells. Fish Shellfish Immunol. 1999 May 1;9(4):241–57.

64. Laing KJ, Hansen JD. Fish T cells: Recent advances through genomics. Dev Comp Immunol. 2011 Dec 1;35(12):1282–95. doi: 10.1016/j.dci.2011.03.004 21414347

65. Żarski D, Nguyen T, Le Cam A, Montfort J, Dutto G, Vidal MO, et al. Transcriptomic Profiling of Egg Quality in Sea Bass (Dicentrarchus labrax) Sheds Light on Genes Involved in Ubiquitination and Translation. Mar Biotechnol. 2017 Feb;19(1):102–15. doi: 10.1007/s10126-017-9732-1 28181038

66. Mommens M, Fernandes JM, Tollefsen KE, Johnston IA, Babiak I. Profiling of the embryonic Atlantic halibut (Hippoglossus hippoglossus L.) transcriptome reveals maternal transcripts as potential markers of embryo quality. BMC Genomics. 2014 Sep 30;15(1):829.

67. Robenek H, Hofnagel O, Buers I, Lorkowski S, Schnoor M, Robenek MJ, et al. Butyrophilin controls milk fat globule secretion. Proc Natl Acad Sci. 2006 Jul 5;103(27):10385–90. doi: 10.1073/pnas.0600795103 16801554

68. Żarski D, Palińska K, Targońska K, Bokor Z, Kotrik L, Krejszeff S, et al. Oocyte quality indicators in Eurasian perch, Perca fluviatilis L., during reproduction under controlled conditions. Aquaculture. 2011 Mar;313(1–4):84–91.

69. Crews ST. Control of cell lineage-specific development and transcription by bHLH–PAS proteins. Genes Dev. 1998 Mar 1;12(5):607–20. doi: 10.1101/gad.12.5.607 9499397

70. Amano T, Tokunaga K, Kakegawa R, Yanagisawa A, Takemoto A, Tatemizo A, et al. Expression analysis of circadian genes in oocytes and preimplantation embryos of cattle and rabbits. Anim Reprod Sci. 2010 Sep;121(3–4):225–35. doi: 10.1016/j.anireprosci.2010.05.020 20619978

71. Amano T, Matsushita A, Hatanaka Y, Watanabe T, Oishi K, Ishida N, et al. Expression and Functional Analyses of Circadian Genes in Mouse Oocytes and Preimplantation Embryos: Cry1 Is Involved in the Meiotic Process Independently of Circadian Clock Regulation1. Biol Reprod. 2009 Mar 1;80(3):473–83. doi: 10.1095/biolreprod.108.069542 19020302

72. Alvarez JD, Chen D, Storer E, Sehgal A. Non-cyclic and Developmental Stage-Specific Expression of Circadian Clock Proteins During Murine Spermatogenesis1. Biol Reprod. 2003 Jul 1;69(1):81–91. doi: 10.1095/biolreprod.102.011833 12606319

73. Anglesio MS, Evdokimova V, Melnyk N, Zhang L, Fernandez CV, Grundy PE, et al. Differential expression of a novel ankyrin containing E3 ubiquitin-protein ligase, Hace1, in sporadic Wilms’ tumor versus normal kidney. Hum Mol Genet. 2004 Sep 15;13(18):2061–74. doi: 10.1093/hmg/ddh215 15254018

74. Hollstein R, Parry DA, Nalbach L, Logan CV, Strom TM, Hartill VL, et al. HACE1 deficiency causes an autosomal recessive neurodevelopmental syndrome. J Med Genet. 2015 Dec;52(12):797–803. doi: 10.1136/jmedgenet-2015-103344 26424145

75. Iimura A, Yamazaki F, Suzuki T, Endo T, Nishida E, Kusakabe M. The E3 ubiquitin ligase Hace1 is required for early embryonic development in Xenopus laevis. BMC Dev Biol. 2016 Sep 21;16:31. doi: 10.1186/s12861-016-0132-y 27653971

76. Daugaard M, Nitsch R, Razaghi B, McDonald L, Jarrar A, Torrino S, et al. Hace1 controls ROS generation of vertebrate Rac1-dependent NADPH oxidase complexes. Nat Commun [Internet]. 2013 Jul 17 [cited 2018 Apr 3];4. Available from: http://www.nature.com/doifinder/10.1038/ncomms3180

77. Razaghi B, Steele SL, Prykhozhij SV, Stoyek MR, Hill JA, Cooper MD, et al. hace1 Influences zebrafish cardiac development via ROS‐dependent mechanisms. Dev Dyn. 2018 Feb 1;247(2):289–303. doi: 10.1002/dvdy.24600 29024245

78. Castets M-D, Schaerlinger B, Silvestre F, Gardeur J-N, Dieu M, Corbier C, et al. Combined analysis of Perca fluviatilis reproductive performance and oocyte proteomic profile. Theriogenology. 2012 Jul;78(2):432–442.e13. doi: 10.1016/j.theriogenology.2012.02.023 22578620

79. Schomer B, Epel D. Redox Changes during Fertilization and Maturation of Marine Invertebrate Eggs. Dev Biol. 1998 Nov;203(1):1–11. doi: 10.1006/dbio.1998.9044 9806768

80. Buchet-Poyau K, Courchet J, Hir HL, Séraphin B, Scoazec J-Y, Duret L, et al. Identification and characterization of human Mex-3 proteins, a novel family of evolutionarily conserved RNA-binding proteins differentially localized to processing bodies. Nucleic Acids Res. 2007 Feb 1;35(4):1289–300. doi: 10.1093/nar/gkm016 17267406

81. Kimelman D, Martin BL. Anterior–posterior patterning in early development: three strategies. Wiley Interdiscip Rev Dev Biol. 2012 Mar 1;1(2):253–66. doi: 10.1002/wdev.25 23801439

82. Draper BW, Mello CC, Bowerman B, Hardin J, Priess JR. MEX-3 Is a KH Domain Protein That Regulates Blastomere Identity in Early C. elegans Embryos. Cell. 1996 Oct 18;87(2):205–16. doi: 10.1016/s0092-8674(00)81339-2 8861905

83. Takada H, Kawana T, Ito Y, Kikuno RF, Mamada H, Araki T, et al. The RNA-binding protein Mex3b has a fine-tuning system for mRNA regulation in early Xenopus development. Development. 2009 Jul 15;136(14):2413–22. doi: 10.1242/dev.029165 19542354


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