The interaction between Tu-Izumo1 and Tu-JUNO is involved in turtles hybridization

in Reproduction
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  • 1 Provincial Key Lab of the Conservation and Exploitation Research of Biological Resources in Anhui, College of Life Sciences, Anhui Normal University, Wuhu, Anhui, China

Correspondence should be addressed to L Nie; Email: lwnie@ahnu.edu.cn
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The specificity of sperm–egg recognition is crucial to species independence, and two proteins (Izumo1 and JUNO) are essential for gamete adhesion/fusion in mammals. However, hybridization, which is very common in turtles, also requires specific recognition of sperm–egg binding proteins. In this study, we discovered that natural selection plays an important role in the codon usage bias of Tu-Izumo1 and Tu-JUNO. Positively selected sites and co-evolutionary analyses between Tu-Izumo1 and Tu-JUNO have been previously reported, and we confirm these results in a larger analysis containing 25 turtle species. We also showed that Tu-JUNO is expressed on the oocyte surface and that Tu-Izumo1 and Tu-JUNO interact with each other directly in different species hybridization combinations. Co-immunization assays revealed that this interaction is evolutionarily conserved in turtles. The results of avidity-based extracellular interaction screening between Tu-Izumo1 and Tu-JUNO for sperm–oocyte binding pairs (both within and across species) likely suggest that the interaction force between Izumo1 and JUNO has a certain correlation in whether the turtles can hybridize. Our results lay a theoretical foundation for the subsequent development of techniques to detect whether different turtle species can interbreed, which would provide the molecular basis for breeding management and species protection of turtles.

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  • Aydin H, Sultana A, Li S, Thavalingam A & Lee JE 2016 Molecular architecture of the human sperm IZUMO1 and egg Juno fertilization complex. Nature 534 562565. (https://doi.org/10.1038/nature18595)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bartholdson SJ, Bustamante LY, Crosnier C, Johnson S, Lea S, Rayner JC & Wright GJ 2012 Semaphorin-7A is an erythrocyte receptor for P. falciparum merozoite-specific TRAP homolog, MTRAP. PLoS Pathogens 8 e1003031. (https://doi.org/10.1371/journal.ppat.1003031)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bian X, Gandahi JA, Liu Y, Yang P, Liu Y, Zhang L, Zhang Q & Chen Q 2013 The ultrastructural characteristics of the spermatozoa stored in the cauda epididymidis in Chinese soft-shelled turtle Pelodiscus sinensis during the breeding season. Micron 44 202209. (https://doi.org/10.1016/j.micron.2012.06.010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bianchi E & Wright GJ 2015 Cross-species fertilization: the hamster egg receptor, Juno, binds the human sperm ligand, Izumo1. Philosophical Transactions of the Royal Society of London: Series B, Biological Sciences 370 20140101. (https://doi.org/10.1098/rstb.2014.0101)

    • Search Google Scholar
    • Export Citation
  • Bianchi E, Doe B, Goulding D & Wright GJ 2014 Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508 483487. (https://doi.org/10.1038/nature13203)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bushell KM, Söllner C, Schuster-Boeckler B, Bateman A & Wright GJ 2008 Large-scale screening for novel low-affinity extracellular protein interactions. Genome Research 18 622630. (https://doi.org/10.1101/gr.7187808)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Carpen JD, Schantz MV, Smits M, Skene DJ & Archer SN 2006 A silent polymorphism in the PER1 gene associates with extreme diurnal preference in humans. Journal of Human Genetics 51 11221125. (https://doi.org/10.1007/s10038-006-0060-y)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chalbi M, Barraud-Lange V, Ravaux B, Howan K, Rodriguez N, Soule P, Ndzoudi A, Boucheix C, Rubinstein E & Wolf JP et al.2014 Binding of sperm protein Izumo1 and its egg receptor Juno drives CD9 accumulation in the intercellular contact area prior to fusion during mammalian fertilization. Development 141 37323739. (https://doi.org/10.1242/dev.111534)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chaney JL & Clark PL 2015 Roles for synonymous codon usage in protein biogenesis. Annual Review of Biophysics 44 143166. (https://doi.org/10.1146/annurev-biophys-060414-034333)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Charrin S, Le Naour F, Silvie O, Milhiet PE, Boucheix C & Rubinstein E 2009 Lateral organization of membrane proteins: tetraspanins spin their web. Biochemical Journal 420 133154. (https://doi.org/10.1042/BJ20082422)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Creighton P & Houghton JA 1987 Visualization of pig sperm chromosomes by in-vitro penetration of zona-free hamster ova. Journal of Reproduction and Fertility 80 619622. (https://doi.org/10.1530/jrf.0.0800619)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dong J, Jiang H, Xiong L, Zan J, Liu J, Yang M, Zheng K, Wang Z & Nie L 2019 Detecting coevolution of positively selected in turtles sperm-egg fusion proteins. Mechanisms of Development 156 17. (https://doi.org/10.1016/j.mod.2019.02.001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fujihara Y, Lu Y, Noda T, Oji A, Larasati T, Kojimakita K, Yu Z, Matzuk RM, Matzuk MM & Ikawa M 2020 Spermatozoa lacking fertilization influencing membrane protein (FIMP) fail to fuse with oocytes in mice. PNAS 117 93939400. (https://doi.org/10.1073/pnas.1917060117)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Galtier N, Roux C, Rousselle M, Romiguier J, Figuet E, Glémin S, Bierne N & Duret L 2018 Codon usage bias in animals: disentangling the effects of natural selection, effective population size, and GC-biased gene conversion. Molecular Biology and Evolution 35 10921103. (https://doi.org/10.1093/molbev/msy015)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Grayson P & Civetta A 2012 Positive selection and the evolution of izumo genes in mammals. International Journal of Evolutionary Biology 2012 958164. (https://doi.org/10.1155/2012/958164)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W & Gascuel O 2010 New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59 307321. (https://doi.org/10.1093/sysbio/syq010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hanada A & Chang MC 1972 Penetration of zona-free eggs by spermatozoa of different species. Biology of Reproduction 6 300309. (https://doi.org/10.1093/biolreprod/6.2.300)

    • Search Google Scholar
    • Export Citation
  • Ikawa M, Inoue N, Benham AM & Okabe M 2010 Fertilization: a sperm’s journey to and interaction with the oocyte. Journal of Clinical Investigation 120 984994. (https://doi.org/10.1172/JCI41585)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Inoue N, Ikawa M, Isotani A & Okabe M 2005 The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434 234238. (https://doi.org/10.1038/nature03362)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jean C, Haghighirad F, Zhu Y, Chalbi M, Ziyyat A, Rubinstein E, Gourier C, Yip P, Wolf JP & Lee JE et al.2019 Juno, the receptor of sperm IZUMO1, is expressed by the human oocyte and is essential for human fertilisation. Human Reproduction 34 118126. (https://doi.org/10.1093/humrep/dey340)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jégou A, Ziyyat A, Barraud-Lange V, Perez E, Wolf JP, Pincet F & Gourier C 2011 CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization. PNAS 108 1094610951. (https://doi.org/10.1073/pnas.1017400108)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kerr JS & Wright GJ 2012 Avidity-based extracellular interaction screening (AVEXIS) for the scalable detection of low-affinity extracellular receptor-ligand interactions. Journal of Visualized Experiments 61 e3881. (https://doi.org/10.3791/3881)

    • Search Google Scholar
    • Export Citation
  • Kumar S, Stecher G & Tamura K 2016 MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33 18701874. (https://doi.org/10.1093/molbev/msw054)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lamas-Toranzo I, Hamze JG, Bianchi E, Fernández-Fuertes B, Pérez-Cerezales S, Laguna-Barraza R, Fernández-González R, Lonergan P, Gutiérrez-Adán A & Wright GJ et al.2020 TMEM95 is a sperm membrane protein essential for mammalian fertilization. eLife 9 e53913. (https://doi.org/10.7554/eLife.53913)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Li YH, Hou Y, Ma W, Yuan JX, Zhang D, Sun QY & Wang WH 2004 Localization of CD9 in pig oocytes and its effects on sperm-egg interaction. Reproduction 127 151157. (https://doi.org/10.1530/rep.1.00006)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Librado P & Rozas J 2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 14511452. (https://doi.org/10.1093/bioinformatics/btp187)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lorenzetti D, Poirier C, Zhao M, Overbeek PA, Harrison W & Bishop CE 2014 A transgenic insertion on mouse chromosome 17 inactivates a novel immunoglobulin superfamily gene potentially involved in sperm–egg fusion. Mammalian Genome 25 141148. (https://doi.org/10.1007/s00335-013-9491-x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Matsuo M, Shiino Y, Yamada N, Ozeki Y & Okawa M 2007 A novel SNP in hPer2 associates with diurnal preference in a healthy population. Sleep and Biological Rhythms 5 141145. (https://doi.org/10.1111/j.1479-8425.2007.00264.x)

    • Search Google Scholar
    • Export Citation
  • McCord WP 1997 Mauremys pritchardi, a new batagrid turtles from Myanmar and Yunnan, China. Chelonian Conservation and Biology 2 555562.

    • Search Google Scholar
    • Export Citation
  • Nishimura K, Han L, Bianchi E, Wright GJ, De Sanctis D & Jovine L 2016 The structure of sperm Izumo1 reveals unexpected similarities with Plasmodium invasion proteins. Current Biology 26 R661R662. (https://doi.org/10.1016/j.cub.2016.06.028)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Noda T, Lu Y, Fujihara Y, Oura S, Koyano T, Kobayashi S, Matzuk MM & Ikawa M 2020 Sperm proteins SOF1, TMEM95, and SPACA6 are required for sperm-oocyte fusion in mice. PNAS 117 1149311502. (https://doi.org/10.1073/pnas.1922650117)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ohto U, Ishida H, Krayukhina E, Uchiyama S, Inoue N & Shimizu T 2016 Structure of IZUMO1–JUNO reveals sperm–oocyte recognition during mammalian fertilization. Nature 534 566569. (https://doi.org/10.1038/nature18596)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pan D, Chen K, Zhu X, Zheng G, Liu Y, Chen Y & Li KB 2009 The morphologic characters of hybrid (Mauremys mutica ♀ × Cuora trifasciata ♂) and comparison with their paren. Acta Hydrobiologica Sinica 33 620626. (https://doi.org/10.3724/SP.J.1035.2009.40620)

    • Search Google Scholar
    • Export Citation
  • Ronquist F & Huelsenbeck JP 2003 MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19 15721574. (https://doi.org/10.1093/bioinformatics/btg180)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Satouh Y, Inoue N, Ikawa M & Okabe M 2012 Visualization of the moment of mouse sperm-egg fusion and dynamic localization of IZUMO1. Journal of Cell Science 125 49854990. (https://doi.org/10.1242/jcs.100867)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sheng Z, Qin Z, Chen Z, Zhao Y & Zhong J 2007 The factors shaping synonymous codon usage in the genome of Burkholderia mallei. Journal of Genetics and Genomics 34 362372. (https://doi.org/10.1016/S1673-8527(0760039-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stothard P 2000 The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. BioTechniques 28 1102, 1104. (https://doi.org/10.2144/00286ir01)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sueoka N 1988 Directional mutation pressure and neutral molecular evolution. PNAS 85 26532657. (https://doi.org/10.1073/pnas.85.8.2653)

  • Suzuki D, Yabe T & Hikida T 2013 Hybridization between Mauremys japonica and Mauremys reevesii inferred by nuclear and mitochondrial DNA analyses. Journal of Herpetology 48 445454. (https://doi.org/10.1670/11-320)

    • Search Google Scholar
    • Export Citation
  • Vicens A & Roldan ERS 2014 Coevolution of positively selected IZUMO1 and CD9 in rodents: evidence of interaction Between gamete fusion proteins? Biology of Reproduction 90 113. (https://doi.org/10.1095/biolreprod.113.116871)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang HC, Badger J, Kearney P & Li M 2001 Analysis of codon usage patterns of bacterial genomes using the self-organizing map. Molecular Biology and Evolution 18 792800. (https://doi.org/10.1093/oxfordjournals.molbev.a003861)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wong WS, Yang Z, Goldman N & Nielsen R 2004 Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168 10411051. (https://doi.org/10.1534/genetics.104.031153)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Xia X, Wang L, Nie L, Huang Z, Jiang Y, Jing W & Liu L 2011 Interspecific hybridization between Mauremys reevesii and Mauremys sinensis: evidence from morphology and DNA sequence data. African Journal of Biotechnology 10 67166724. (https://doi.org/10.5897/AJB11.063)

    • Search Google Scholar
    • Export Citation
  • Yang Z 2007 PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24 15861591. (https://doi.org/10.1093/molbev/msm088)

  • Zhong J, Li Y, Zhao S, Liu S & Zhang Z 2007 Mutation pressure shapes codon usage in the GC-Rich genome of foot-and-mouth disease virus. Virus Genes 35 767776. (https://doi.org/10.1007/s11262-007-0159-z)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhou GB, Liu GS, Meng QG, Liu Y, Hou YP, Wang XX, Li N & Zhu SE 2009 Tetraspanin CD9 in bovine oocytes and its role in fertilization. Journal of Reproduction and Development 55 305308. (https://doi.org/10.1262/jrd.20099)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ziyyat A, Rubinstein E, Monier-Gavelle F, Barraud V, Kulski O, Prenant M, Boucheix C, Bomsel M & Wolf JP 2006 CD9 controls the formation of clusters that contain tetraspanins and the integrin α6β1, which are involved in human and mouse gamete fusion. Journal of Cell Science 119 416424. (https://doi.org/10.1242/jcs.02730)

    • PubMed
    • Search Google Scholar
    • Export Citation