Skip to main content
SpringerLink
Log in

The molecular foundations of zygosis

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Zygosis is the generation of new biological individuals by the sexual fusion of gamete cells. Our current understanding of eukaryotic phylogeny indicates that sex is ancestral to all extant eukaryotes. Although sexual development is extremely diverse, common molecular elements have been retained. HAP2-GCS1, a protein that promotes the fusion of gamete cell membranes that is related in structure to certain viral fusogens, is conserved in many eukaryotic lineages, even though gametes vary considerably in form and behaviour between species. Similarly, although zygotes have dramatically different forms and fates in different organisms, diverse eukaryotes share a common developmental programme in which homeodomain-containing transcription factors play a central role. These common mechanistic elements suggest possible common evolutionary histories that, if correct, would have profound implications for our understanding of eukaryogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Herranz G (2012) Origin of the terms embryo, gamete and zygote. Zygote 20:313–320

    PubMed  Google Scholar 

  2. Cavalier-Smith T (1995) Cell cycles, diplokaryosis and the archezoan origin of sex. Arch Protistenk 145:189–207

    Google Scholar 

  3. Kondrashov AS (1997) Evolutionary genetics of life cycles. Annu Rev Ecol Syst 28:391–435

    Google Scholar 

  4. Dacks J, Roger AJ (1999) The first sexual lineage and the relevance of facultative sex. J Mol Evol 48:779–783

    CAS  PubMed  Google Scholar 

  5. Speijer D, Lukeš J, Eliáš M (2015) Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. PNAS 112:8827–8834

    CAS  PubMed  Google Scholar 

  6. Pixell-Goodrich HLM (1915) Memoirs: on the life-history of the sporozoa of spatangoids, with observation on some allied forms. J Cell Sci s2(61):81–104

    Google Scholar 

  7. Dobell C (1914) A commentary on the genetics of the ciliate protozoa. J Gen 4:131–190

    Google Scholar 

  8. Raper JR (1959) Sexual versatility and evolutionary processes in Fungi. Mycologia 51:107–124

    Google Scholar 

  9. Saga Y, Okada H, Yanagisawa K (1983) Macrocyst development in Dictyostelium discoideum. II. Mating-type-specific cell fusion and acquisition of fusion-competence. J Cell Sci 60:157–168

    CAS  PubMed  Google Scholar 

  10. Ishida K, Hata T, Urushihara H (2005) Gamete fusion and cytokinesis preceding zygote establishment in the sexual process of Dictyostelium discoideum. Dev Growth Differ 47:25–35

    PubMed  Google Scholar 

  11. Bloomfield G, Paschke P, Okamoto M et al (2019) Triparental inheritance in Dictyostelium. Proc Natl Acad Sci USA 116:2187–2192

    CAS  PubMed  Google Scholar 

  12. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144

    CAS  PubMed  Google Scholar 

  13. Wong JL, Johnson MA (2010) Is HAP2-GCS1 an ancestral gamete fusogen? Trends Cell Biol 20:134–141

    CAS  PubMed  Google Scholar 

  14. Valansi C, Moi D, Leikina E et al (2017) Arabidopsis HAP2/GCS1 is a gamete fusion protein homologous to somatic and viral fusogens. J Cell Biol 216:571–581

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Pinello JF, Lai AL, Millet JK et al (2017) Structure-function studies link class II viral fusogens with the ancestral gamete fusion protein HAP2. Curr Biol 27:651–660

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Fédry J, Liu Y, Péhau-Arnaudet G et al (2017) The ancient gamete fusogen HAP2 is a eukaryotic class II fusion protein. Cell 168:904–915.e10

    PubMed  PubMed Central  Google Scholar 

  17. Hernández JM, Podbilewicz B (2017) The hallmarks of cell–cell fusion. Development 144:4481–4495

    PubMed  Google Scholar 

  18. Modis Y (2014) Relating structure to evolution in class II viral membrane fusion proteins. Curr Opin Virol 5:34–41

    CAS  PubMed  Google Scholar 

  19. Kielian M, Helenius A (1985) pH-induced alterations in the fusogenic spike protein of Semliki Forest virus. J Cell Biol 101:2284–2291

    CAS  PubMed  Google Scholar 

  20. Lescar J, Roussel A, Wien MW et al (2001) The fusion glycoprotein shell of semliki forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137–148

    CAS  PubMed  Google Scholar 

  21. Feng J, Dong X, Pinello J et al (2018) Fusion surface structure, function, and dynamics of gamete fusogen HAP2. Elife 7:e39772

    PubMed  PubMed Central  Google Scholar 

  22. Fedry J, Forcina J, Legrand P et al (2018) Evolutionary diversification of the HAP2 membrane insertion motifs to drive gamete fusion across eukaryotes. PLoS Biol 16:e2006357

    PubMed  PubMed Central  Google Scholar 

  23. Baquero E, Fedry J, Legrand P et al (2019) Species-specific functional regions of the green alga gamete fusion protein HAP2 revealed by structural studies. Structure 27:113–124.e4

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2006) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8:64–71

    CAS  PubMed  Google Scholar 

  25. von Besser K, Frank AC, Johnson MA, Preuss D (2006) Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133:4761–4769

    Google Scholar 

  26. Liu Y, Tewari R, Ning J et al (2008) The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes Dev 22:1051–1068

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Hirai M, Arai M, Mori T et al (2008) Male fertility of malaria parasites is determined by GCS1, a plant-type reproduction factor. Curr Biol 18:607–613

    CAS  PubMed  Google Scholar 

  28. Steele RE, Dana CE (2009) Evolutionary history of the HAP2/GCS1 gene and sexual reproduction in metazoans. PLoS One 4:e7680

    PubMed  PubMed Central  Google Scholar 

  29. Ebchuqin E, Yokota N, Yamada L et al (2014) Evidence for participation of GCS1 in fertilization of the starlet sea anemone Nematostella vectensis: implication of a common mechanism of sperm–egg fusion in plants and animals. Biochem Biophys Res Commun 451:522–528

    CAS  PubMed  Google Scholar 

  30. Cole ES, Cassidy-Hanley D, Pinello JF et al (2014) Function of the male-gamete-specific fusion protein HAP2 in a seven-sexed ciliate. Curr Biol 24:2168–2173

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Okamoto M, Yamada L, Fujisaki Y et al (2016) Two HAP2-GCS1 homologs responsible for gamete interactions in the cellular slime mold with multiple mating types: implication for common mechanisms of sexual reproduction shared by plants and protozoa and for male-female differentiation. Dev Biol 415:6–13

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Sprunck S, Rademacher S, Vogler F et al (2012) Egg cell–secreted EC1 triggers sperm cell activation during double fertilization. Science 338:1093–1097

    CAS  PubMed  Google Scholar 

  33. Liu Y, Pei J, Grishin N, Snell WJ (2015) The cytoplasmic domain of the gamete membrane fusion protein HAP2 targets the protein to the fusion site in Chlamydomonas and regulates the fusion reaction. Development 142:962–971

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Wong JL, Leydon AR, Johnson MA (2010) HAP2(GCS1)-dependent gamete fusion requires a positively charged carboxy-terminal domain. PLoS Genet 6:e1000882

    PubMed  PubMed Central  Google Scholar 

  35. Mori T, Hirai M, Kuroiwa T, Miyagishima S (2010) The functional domain of GCS1-based gamete fusion resides in the amino terminus in plant and parasite species. PLoS One 5:e15957

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Heiman MG, Walter P (2000) Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating. J Cell Biol 151:719–730

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Jin H, Carlile C, Nolan S, Grote E (2004) Prm1 prevents contact-dependent lysis of yeast mating pairs. Eukaryot Cell 3:1664–1673

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Aguilar PS, Engel A, Walter P (2007) The plasma membrane proteins Prm1 and Fig1 ascertain fidelity of membrane fusion during yeast mating. Mol Biol Cell 18:547–556

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Aguilar PS, Baylies MK, Fleissner A et al (2013) Genetic basis of cell-cell fusion mechanisms. Trends Genet 29:427–437

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Fu C, Heitman J (2017) PRM1 and KAR5 function in cell–cell fusion and karyogamy to drive distinct bisexual and unisexual cycles in the Cryptococcus pathogenic species complex. PLoS Genet 13:e1007113

    PubMed  PubMed Central  Google Scholar 

  41. Aydin H, Sultana A, Li S et al (2016) Molecular architecture of the human sperm IZUMO1 and egg JUNO fertilization complex. Nature 534:562–565

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Ohto U, Ishida H, Krayukhina E et al (2016) Structure of IZUMO1-JUNO reveals sperm-oocyte recognition during mammalian fertilization. Nature 534:566–569

    CAS  PubMed  Google Scholar 

  43. Herberg S, Gert KR, Schleiffer A, Pauli A (2018) The Ly6/uPAR protein Bouncer is necessary and sufficient for species-specific fertilization. Science 361:1029–1033

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    CAS  PubMed  Google Scholar 

  45. Liu Y, Misamore MJ, Snell WJ (2010) Membrane fusion triggers rapid degradation of two gamete-specific, fusion-essential proteins in a membrane block to polygamy in Chlamydomonas. Development 137(9):1473–1481

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Nakel T, Tekleyohans DG, Mao Y et al (2017) Triparental plants provide direct evidence for polyspermy induced polyploidy. Nat Commun 8:1033

    PubMed  PubMed Central  Google Scholar 

  47. Grossniklaus U (2017) Polyspermy produces tri-parental seeds in maize. Curr Biol 27:R1300–R1302

    CAS  PubMed  Google Scholar 

  48. Ferris PJ, Woessner JP, Goodenough UW (1996) A sex recognition glycoprotein is encoded by the plus mating-type gene fus1 of Chlamydomonas reinhardtii. MBoC 7:1235–1248

    CAS  PubMed  Google Scholar 

  49. Vještica A, Merlini L, Nkosi PJ, Martin SG (2018) Gamete fusion triggers bipartite transcription factor assembly to block re-fertilization. Nature 560:397–400

    PubMed  Google Scholar 

  50. Hull CM, Boily M-J, Heitman J (2005) Sex-specific homeodomain proteins Sxi1alpha and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot Cell 4:526–535

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Rothschild L (1954) Polyspermy. Q Rev Biol 29:332–342

    CAS  PubMed  Google Scholar 

  52. Bianchi E, Wright GJ (2016) Sperm meets egg: the genetics of mammalian fertilization. Annu Rev Genet 50:93–111

    CAS  PubMed  Google Scholar 

  53. Beale KM, Leydon AR, Johnson MA (2012) Gamete fusion is required to block multiple pollen tubes from entering an Arabidopsis ovule. Curr Biol 22:1090–1094

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Maruyama D, Völz R, Takeuchi H et al (2015) Rapid elimination of the persistent synergid through a cell fusion mechanism. Cell 161:907–918

    CAS  PubMed  Google Scholar 

  55. Tekleyohans DG, Mao Y, Kägi C et al (2017) Polyspermy barriers: a plant perspective. Curr Opin Plant Biol 35:131–137

    PubMed  Google Scholar 

  56. Okada H, Hirota Y, Moriyama R et al (1986) Nuclear fusion in multinucleated giant cells during the sexual development of Dictyostelium discoideum. Dev Biol 118:95–102

    CAS  Google Scholar 

  57. Abrams EW, Zhang H, Marlow FL et al (2012) Dynamic assembly of brambleberry mediates nuclear envelope fusion during early development. Cell 150:521–532

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Ning J, Otto TD, Pfander C et al (2013) Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates. Genes Dev 27:1198–1215

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Rogers JV, Rose MD (2014) Kar5p is required for multiple functions in both inner and outer nuclear envelope fusion in Saccharomyces cerevisiae. G3 (Bethesda) 5:111–121

    Google Scholar 

  60. Garg SG, Martin WF (2016) Mitochondria, the cell cycle, and the origin of sex via a syncytial eukaryote common ancestor. Genome Biol Evol 8:1950–1970

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Bowman JL, Sakakibara K, Furumizu C, Dierschke T (2016) Evolution in the cycles of life. Annu Rev Genet 50:133–154

    CAS  PubMed  Google Scholar 

  62. Strathern J, Hicks J, Herskowitz I (1981) Control of cell type in yeast by the mating type locus: the α1–α2 hypothesis. J Mol Biol 147:357–372

    CAS  PubMed  Google Scholar 

  63. Shepherd JCW, McGinnis W, Carrasco AE et al (1984) Fly and frog homoeo domains show homologies with yeast mating type regulatory proteins. Nature 310:70

    CAS  PubMed  Google Scholar 

  64. Dranginis AM (1990) Binding of yeast al and α2 as a heterodimer to the operator DNA of a haploid-specific gene. Nature 347:682

    CAS  PubMed  Google Scholar 

  65. Kelly M, Burke J, Smith M et al (1988) Four mating-type genes control sexual differentiation in the fission yeast. EMBO J 7:1537–1547

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Kämper J, Reichmann M, Romeis T et al (1995) Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81:73–83

    PubMed  Google Scholar 

  67. Banham AH, Asante-Owusu RN, Gottgens B et al (1995) An N-terminal dimerization domain permits homeodomain proteins to choose compatible partners and initiate sexual development in the mushroom Coprinus cinereus. Plant Cell 7:773–783

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Derelle R, Lopez P, Guyader HL, Manuel M (2007) Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evolut Dev 9:212–219

    CAS  Google Scholar 

  69. Joo S, Wang MH, Lui G et al (2018) Common ancestry of heterodimerizing TALE homeobox transcription factors across Metazoa and Archaeplastida. BMC Biol 16:136

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Levine RP, Ebersold WT (1960) The genetics and cytology of Chlamydomonas. Annu Rev Microbiol 14:197–216

    CAS  PubMed  Google Scholar 

  71. Goodenough UW, Armbrust EV, Campbell AM, Ferris PJ (1995) Molecular genetics of sexuality in Chlamydomonas. Annu Rev Plant Physiol Plant Mol Biol 46:21–44

    CAS  Google Scholar 

  72. Lee J-H, Lin H, Joo S, Goodenough U (2008) Early sexual origins of homeoprotein heterodimerization and evolution of the plant KNOX/BELL family. Cell 133:829–840

    CAS  PubMed  Google Scholar 

  73. Nishimura Y, Shikanai T, Nakamura S et al (2012) Gsp1 triggers the sexual developmental program including inheritance of chloroplast DNA and mitochondrial DNA in Chlamydomonas reinhardtii. Plant Cell 24:2401–2414

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Sakakibara K, Ando S, Yip HK et al (2013) KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science 339:1067–1070

    CAS  PubMed  Google Scholar 

  75. Horst NA, Katz A, Pereman I et al (2016) A single homeobox gene triggers phase transition, embryogenesis and asexual reproduction. Nat Plants 2:15209

    CAS  PubMed  Google Scholar 

  76. Coelho SM, Peters AF, Charrier B et al (2007) Complex life cycles of multicellular eukaryotes: new approaches based on the use of model organisms. Gene 406:152–170

    CAS  PubMed  Google Scholar 

  77. Coelho SM, Godfroy O, Arun A et al (2011) OUROBOROS is a master regulator of the gametophyte to sporophyte life cycle transition in the brown alga Ectocarpus. PNAS 108:11518–11523

    CAS  PubMed  Google Scholar 

  78. Arun A, Coelho SM, Peters AF et al (2019) Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae. eLife 8:e43101

    PubMed  PubMed Central  Google Scholar 

  79. Bloomfield G, Skelton J, Ivens A et al (2010) Sex determination in the social amoeba Dictyostelium discoideum. Science 330:1533–1536

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Hedgethorne K, Eustermann S, Yang J-C et al (2017) Homeodomain-like DNA binding proteins control the haploid-to-diploid transition in Dictyostelium. Sci Adv 3:e1602937

    PubMed  PubMed Central  Google Scholar 

  81. Birky CW (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet 35:125–148

    CAS  PubMed  Google Scholar 

  82. Breton S, Stewart DT (2015) Atypical mitochondrial inheritance patterns in eukaryotes. Genome 58:423–431

    CAS  PubMed  Google Scholar 

  83. Sager R, Lane D (1972) Molecular basis of maternal inheritance. PNAS 69:2410–2413

    CAS  PubMed  Google Scholar 

  84. Boynton JE, Harris EH, Burkhart BD et al (1987) Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. PNAS 84:2391–2395

    CAS  PubMed  Google Scholar 

  85. Yan Z, Hull CM, Heitman J et al (2004) SXI1alpha controls uniparental mitochondrial inheritance in Cryptococcus neoformans. Curr Biol 14:R743–R744

    CAS  PubMed  Google Scholar 

  86. Yan Z, Hull CM, Sun S et al (2007) The mating type-specific homeodomain genes SXI1α and SXI2a coordinately control uniparental mitochondrial inheritance in Cryptococcus neoformans. Curr Genet 51:187–195

    CAS  PubMed  Google Scholar 

  87. Nunnari J, Marshall WF, Straight A et al (1997) Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. MBoC 8:1233–1242

    CAS  PubMed  Google Scholar 

  88. Mehta K, Ananthanarayanan V (2019) Cortical tethering of mitochondria by the dynein anchor Mcp5 enables uniparental mitochondrial inheritance during fission yeast meiosis. bioRxiv 525196

  89. Bloomfield G (2013) Sex in dictyostelia. In: Romeralo M, Baldauf S, Escalante R (eds) Dictyostelids: evolution, genomics and cell biology. Springer, Berlin, pp 129–148

    Google Scholar 

  90. Hurst GD, Werren JH (2001) The role of selfish genetic elements in eukaryotic evolution. Nat Rev Genet 2:597–606

    CAS  PubMed  Google Scholar 

  91. Cleveland LR (1947) The origin and evolution of meiosis. Science 105:287–289

    CAS  PubMed  Google Scholar 

  92. Hurst LD, Nurse P (1991) A note on the evolution of meiosis. J Theor Biol 150:561–563

    CAS  PubMed  Google Scholar 

  93. Kondrashov AS (1994) Gradual origin of amphimixis by natural selection. Lect Math Life Sci 25:27–51

    Google Scholar 

  94. Crow JF, Kimura M (1965) Evolution in sexual and asexual populations. Am Nat 99:439–450

    Google Scholar 

  95. Hickey DA (1982) Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101:519–531

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Hickey DA (1993) Molecular symbionts and the evolution of sex. J Hered 84:410–414

    CAS  PubMed  Google Scholar 

  97. Clark T (2018) HAP2/GCS1: mounting evidence of our true biological EVE? PLoS Biol 16:e3000007

    PubMed  PubMed Central  Google Scholar 

  98. Koonin EV, Dolja VV, Krupovic M (2015) Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479–480:2–25

    PubMed  PubMed Central  Google Scholar 

  99. Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231–236

    CAS  PubMed  Google Scholar 

  100. Raymann K, Brochier-Armanet C, Gribaldo S (2015) The two-domain tree of life is linked to a new root for the Archaea. PNAS 112:6670–6675

    CAS  PubMed  Google Scholar 

  101. Zaremba-Niedzwiedzka K, Caceres EF, Saw JH et al (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358

    CAS  PubMed  Google Scholar 

  102. Cunha VD, Gaia M, Gadelle D et al (2017) Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet 13:e1006810

    PubMed  PubMed Central  Google Scholar 

  103. Spang A, Eme L, Saw JH et al (2018) Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLoS Genet 14:e1007080

    PubMed  PubMed Central  Google Scholar 

  104. Cunha VD, Gaia M, Nasir A, Forterre P (2018) Asgard archaea do not close the debate about the universal tree of life topology. PLoS Genet 14:e1007215

    PubMed  PubMed Central  Google Scholar 

  105. Bergerat A, de Massy B, Gadelle D et al (1997) An atypical topoisomerase II from archaea with implications for meiotic recombination. Nature 386:414

    CAS  PubMed  Google Scholar 

  106. Goodenough U, Heitman J (2014) Origins of eukaryotic sexual reproduction. Cold Spring Harb Perspect Biol 6:a016154

    PubMed  PubMed Central  Google Scholar 

  107. Heitman J (2015) Evolution of sexual reproduction: a view from the fungal kingdom supports an evolutionary epoch with sex before sexes. Fungal Biol Rev 29:108–117

    PubMed  PubMed Central  Google Scholar 

  108. Perrin N (2012) What uses are mating types? The “Developmental Switch” model. Evolution 66:947–956

    PubMed  Google Scholar 

  109. Medina EM, Turner JJ, Gordân R et al (2016) Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi. Elife 5:e09492

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Templebridge Bio Ltd, London, UK

    Gareth Bloomfield

Authors
  1. Gareth Bloomfield
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bloomfield, G. The molecular foundations of zygosis. Cell. Mol. Life Sci. 77, 323–330 (2020). https://doi.org/10.1007/s00018-019-03187-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03187-1

Keywords

Search

Navigation