Skip to main content

Development of polyspermic zygote and possible contribution of polyspermy to polyploid formation in angiosperms

Abstract

Fertilization is a general feature of eukaryotic uni- and multicellular organisms to restore a diploid genome from female and male gamete haploid genomes. In angiosperms, polyploidization is a common phenomenon, and polyploidy would have played a major role in the long-term diversification and evolutionary success of plants. As for the mechanism of formation of autotetraploid plants, the triploid-bridge pathway, crossing between triploid and diploid plants, is considered as a major pathway. For the emergence of triploid plants, fusion of an unreduced gamete with a reduced gamete is generally accepted. In addition, the possibility of polyspermy has been proposed for maize, wheat and some orchids, although it has been regarded as an uncommon mechanism of triploid formation. One of the reasons why polyspermy is regarded as uncommon is because it is difficult to reproduce the polyspermy situation in zygotes and to analyze the developmental profiles of polyspermic triploid zygotes. Recently, polyspermic rice zygotes were successfully produced by electric fusion of an egg cell with two sperm cells, and their developmental profiles were monitored. Two sperm nuclei and an egg nucleus fused into a zygotic nucleus in the polyspermic zygote, and the triploid zygote divided into a two-celled embryo via mitotic division with a typical bipolar microtubule spindle. The two-celled proembryos further developed and regenerated into triploid plants. These suggest that polyspermic plant zygotes have the potential to form triploid embryos, and that polyspermy in angiosperms might be a pathway for the formation of triploid plants.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Antoine AF, Faure JE, Dumas C, Feijó JA (2001) Differential contribution of cytoplasmic Ca2+ and Ca2+ influx to gamete fusion and egg activation in maize. Nat Cell Biol 3:1120–1123

    CAS  Article  PubMed  Google Scholar 

  • Blackman VH (1898) On the cytological features of fertilization and related phenomena in Pinus silvestris L. Philos Trans R Soc Lond B Biol Sci 190:395–426

    Article  Google Scholar 

  • Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bleckmann A, Alter S, Dresselhaus T (2014) The beginning of a seed: regulatory mechanisms of double fertilization. Front Plant Sci 5:452

    Article  PubMed  PubMed Central  Google Scholar 

  • Brawley SH (1991) The fast block against polyspermy in fucoid algae is an electrical block. Dev Biol 144:94–106

    CAS  Article  PubMed  Google Scholar 

  • Bretagnolle F, Thompson JD (1995) Tansley Review No. 78. Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol 129:1–22

    Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, dePamphilis CW (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Denninger P, Bleckmann A, Lausser A, Vogler F, Ott T, Ehrhardt DW, Frommer WB, Sprunck S, Dresselhaus T, Grossmann G (2014) Male–female communication triggers calcium signatures during fertilization in Arabidopsis. Nat Commun 5:4645

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Faure JE, Digonnet C, Dumas C (1994) An in-vitro system for adhesion and fusion of maize gametes. Science 263:1598–1600

    CAS  Article  PubMed  Google Scholar 

  • Grant V (1981) Plant Speciation, Ed 2. Columbia University, New York

    Google Scholar 

  • Guignard ML (1899) Sur les antherozoides et la double copulation sexuelle chez les vegetaux angiosperms. Rev Gén de Bot 11:129–135

    Google Scholar 

  • Hagerup O (1947) The spontaneous formation of haploid, polyploid, and aneuploid embryos in some orchids. Kongel Dan Vidensk Selsk Biol Medd 20:1–22

    Google Scholar 

  • Hamamura Y, Saito C, Awai C, Kurihara D, Miyawaki A, Nakagawa T, Kanaoka MM, Sasaki N, Nakano A, Berger F, Higashiyama T (2011) Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana. Curr Biol 21:497–502

    CAS  Article  PubMed  Google Scholar 

  • Hamamura Y, Nishimaki M, Takeuchi H, Geitmann A, Kurihara D, Higashiyama T (2014) Live imaging of calcium spikes during double fertilization in Arabidopsis. Nat Commun 5:4722

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hu CH, Ho KM (1963) Karyological studies of triploid rice plants. Bot Bull Acad Sin 4:30–36

    Google Scholar 

  • Iwao Y (2012) Egg activation in physiological polyspermy. Reproduction 144:11–22

    CAS  Article  PubMed  Google Scholar 

  • Kasahara RD, Maruyama D, Hamamura Y, Sakakibara T, Twell D, Higashiyama T (2012) Fertilization recovery after defective sperm cell release in Arabidopsis. Curr Biol 22:1084–1089

    CAS  Article  PubMed  Google Scholar 

  • Kato A (1997) Induced single fertilization in maize. Sex Plant Reprod 10:96–100

    Article  Google Scholar 

  • Kihara H, Ono T (1926) Chromosomenzahlen und systematische Gruppierung der Rumex-Arten. Z Zellforsch Mikr Anat 4:475–481

    Article  Google Scholar 

  • Köhler C, Mittelsten Scheid O, Erilova A (2010) The impact of the triploid block on the origin and evolution of polyploid plants. Trends Genet 26:142–148

    Article  PubMed  Google Scholar 

  • Kranz E, von Wiegen P, Lörz H (1995) Early cytological events after induction of cell division in egg cells and zygote development following in vitro fertilization with angiosperm gametes. Plant J 8:9–23

    Article  Google Scholar 

  • Leitch IJ, Bennett MD (1997) Polyploidy in angiosperms. Trends Plant Sci 2:470–476

    Article  Google Scholar 

  • Lloyd C, Chan J (2006) Not so divided: the common basis of plant and animal cell division. Nat Rev Mol Cell Biol 7:147–152

    CAS  Article  PubMed  Google Scholar 

  • Maruyama D, Hamamura Y, Takeuchi H, Susaki D, Nishimaki M, Kurihara D, Kasahara RD, Higashiyama T (2013) Independent control by each female gamete prevents the attraction of multiple pollen tubes. Dev Cell 25:317–323

    CAS  Article  PubMed  Google Scholar 

  • Maruyama D, Völz R, Takeuchi H, Mori T, Igawa T, Kurihara D, Kawashima T, Ueda M, Itoh M, Umeda M, Nishikawa S, Groß-Hardt R, Higashiyama T (2015) Rapid elimination of the persistent synergid through a cell fusion mechanism. Cell 161:907–918

    CAS  Article  PubMed  Google Scholar 

  • Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424

    CAS  Article  PubMed  Google Scholar 

  • McWilliam JR, Mergen F (1958) Cytology of fertilization in Pinus. Bot Gaz 199:246–249

    Article  Google Scholar 

  • Nagasato C, Motomura T, Ichimura T (1999) Influence of centriole behaviour on the first spindle formation in zygotes of the brown alga Fucus distichus (Fucales, Phaeophyceae). Dev Biol 208:200–209

    CAS  Article  PubMed  Google Scholar 

  • Navara CS, First NL, Schatten G (1994) Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster. Dev Biol 162:29–40

    CAS  Article  PubMed  Google Scholar 

  • Nawaschin S (1898) Revision der Befruchtungsvorgange bei Lilium martagon und Fritillaria tenella. Bull Sci Acad Imp Sci Saint Pétersbourg 9:377–382

    Google Scholar 

  • Ohnishi Y, Hoshino R, Okamoto T (2014) Dynamics of male and female chromatin during karyogamy in rice zygotes. Plant Physiol 165:1533–1543

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Raghavan V (2003) Some reflections on double fertilization, from its discovery to the present. New Phytol 159:565–583

    CAS  Article  Google Scholar 

  • Ramsey J (2007) Unreduced gametes and neopolyploids in natural populations of Achillea borealis (Asteraceae). Heredity 98:143–150

    CAS  Article  PubMed  Google Scholar 

  • Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501

    Article  Google Scholar 

  • Rhoades MM (1936) Note on the origin of triploidy in maize. J Genet 33:355–357

    Article  Google Scholar 

  • Rick CM (1945) A survey of cytogenetic causes of unfruitfulness in the tomato. Genetics 30:347–362

    CAS  PubMed  PubMed Central  Google Scholar 

  • Runions CJ, Owens JN (1999) Sexual reproduction of interior spruce (Pinaceae). II. Fertilization to early embryo formation. Int J Plant Sci 160:641–652

    Article  Google Scholar 

  • Russell SD (1992) Double fertilization. Int Rev Cytol 140:357–390

    Article  Google Scholar 

  • Sandfaer J (1975) The occurrence of spontaneous triploids in different barley varieties. Hereditas 80:149–153

    Article  Google Scholar 

  • Sandfaer J (1979) Frequency of aneuploids in progenies of autotriploid barley, Hordeun vulgare L. Hereditas 90:213–217

    Article  Google Scholar 

  • Santelices B (2002) Recent advances in fertilization ecology of macroalgae. J Phycol 38:4–10

    Article  Google Scholar 

  • Schuel H (1984) The prevention of polyspermic fertilization in sea urchins. Biol Bull 167:271–309

    CAS  Article  PubMed  Google Scholar 

  • Scott RJ, Armstrong SJ, Doughty J, Spielman M (2008) Double fertilization in Arabidopsis thaliana involves a polyspermy block on the egg but not the central cell. Mol Plant 1:611–619

    CAS  Article  PubMed  Google Scholar 

  • Snook RR, Hosken DJ, Karr TL (2011) The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg. Reproduction 142:779–792

    Article  PubMed  Google Scholar 

  • Spielman M, Scott RJ (2008) Polyspermy barriers in plants: from preventing to promoting fertilization. Sex Plant Reprod 21:53–65

    Article  Google Scholar 

  • Sprague GF (1929) Hetero-fertilization in maize. Science 69:526–527

    CAS  Article  PubMed  Google Scholar 

  • Sprague GF (1932) The nature and extent of hetero-fertilization in maize. Genetics 17:358–368

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suarez EY, Lopez AG, Naranjo CA (1992) Polyspermy versus unreduced male gametes as the origin of nonaploids (9x) common wheat plants. Caryologia 45:21–28

    Article  Google Scholar 

  • Tarin JJ (2000) Fertilization in protozoa and metazoan animals: a comparative overview. In: Tarin JJ, Cano A (Eds.) Fertilization in protozoa and metazoan animals cellular and molecular aspects. Springer, Berlin, pp 277–314

    Google Scholar 

  • Toda E, Ohnishi Y, Okamoto T (2016) Development of polyspermic rice zygotes. Plant Physiol 171:206–214

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Uchiumi T, Uemura I, Okamoto T (2007) Establishment of an in vitro fertilization system in rice (Oryza sativa L.). Planta 226:581–589

    CAS  Article  PubMed  Google Scholar 

  • Wong JL, Wessel GM (2006) Defending the zygote: search for the ancestral animal block to polyspermy. Curr Top Dev Biol 72:1–151

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Ms. T. Mochizuki (Tokyo Metropolitan University) for isolating rice gametes. This work was supported in part by the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grants-in-Aid no. 26113715 to T.O.) and the Japan Society for the Promotion of Science (Grant-in-Aid no. 16K14742 to T.O.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takashi Okamoto.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Okamoto, T., Ohnishi, Y. & Toda, E. Development of polyspermic zygote and possible contribution of polyspermy to polyploid formation in angiosperms. J Plant Res 130, 485–490 (2017). https://doi.org/10.1007/s10265-017-0913-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-017-0913-9

Keywords

  • Karyogamy
  • Fertilization
  • Polyploid
  • Polyspermy
  • Triploid
  • Zygote