Journal of Plant Research

, Volume 130, Issue 3, pp 485–490 | Cite as

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

JPR Symposium Fusion in Fertilization: Interdisciplinary Collaboration among Plant and Animal Scientists

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.

Keywords

Karyogamy Fertilization Polyploid Polyspermy Triploid Zygote 

References

  1. 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 3:1120–1123CrossRefPubMedGoogle Scholar
  2. Blackman VH (1898) On the cytological features of fertilization and related phenomena in Pinus silvestris L. Philos Trans R Soc Lond B Biol Sci 190:395–426CrossRefGoogle Scholar
  3. Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bleckmann A, Alter S, Dresselhaus T (2014) The beginning of a seed: regulatory mechanisms of double fertilization. Front Plant Sci 5:452CrossRefPubMedPubMedCentralGoogle Scholar
  5. Brawley SH (1991) The fast block against polyspermy in fucoid algae is an electrical block. Dev Biol 144:94–106CrossRefPubMedGoogle Scholar
  6. 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 129:1–22CrossRefGoogle Scholar
  7. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846CrossRefPubMedGoogle Scholar
  8. 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 16:738–749CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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 5:4645CrossRefPubMedPubMedCentralGoogle Scholar
  10. Faure JE, Digonnet C, Dumas C (1994) An in-vitro system for adhesion and fusion of maize gametes. Science 263:1598–1600CrossRefPubMedGoogle Scholar
  11. Grant V (1981) Plant Speciation, Ed 2. Columbia University, New YorkGoogle Scholar
  12. Guignard ML (1899) Sur les antherozoides et la double copulation sexuelle chez les vegetaux angiosperms. Rev Gén de Bot 11:129–135Google Scholar
  13. Hagerup O (1947) The spontaneous formation of haploid, polyploid, and aneuploid embryos in some orchids. Kongel Dan Vidensk Selsk Biol Medd 20:1–22Google Scholar
  14. 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 21:497–502CrossRefPubMedGoogle Scholar
  15. 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 5:4722CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hu CH, Ho KM (1963) Karyological studies of triploid rice plants. Bot Bull Acad Sin 4:30–36Google Scholar
  17. Iwao Y (2012) Egg activation in physiological polyspermy. Reproduction 144:11–22CrossRefPubMedGoogle Scholar
  18. Kasahara RD, Maruyama D, Hamamura Y, Sakakibara T, Twell D, Higashiyama T (2012) Fertilization recovery after defective sperm cell release in Arabidopsis. Curr Biol 22:1084–1089CrossRefPubMedGoogle Scholar
  19. Kato A (1997) Induced single fertilization in maize. Sex Plant Reprod 10:96–100CrossRefGoogle Scholar
  20. Kihara H, Ono T (1926) Chromosomenzahlen und systematische Gruppierung der Rumex-Arten. Z Zellforsch Mikr Anat 4:475–481CrossRefGoogle Scholar
  21. Köhler C, Mittelsten Scheid O, Erilova A (2010) The impact of the triploid block on the origin and evolution of polyploid plants. Trends Genet 26:142–148CrossRefPubMedGoogle Scholar
  22. 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 8:9–23CrossRefGoogle Scholar
  23. Leitch IJ, Bennett MD (1997) Polyploidy in angiosperms. Trends Plant Sci 2:470–476CrossRefGoogle Scholar
  24. Lloyd C, Chan J (2006) Not so divided: the common basis of plant and animal cell division. Nat Rev Mol Cell Biol 7:147–152CrossRefPubMedGoogle Scholar
  25. 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 25:317–323CrossRefPubMedGoogle Scholar
  26. 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 161:907–918CrossRefPubMedGoogle Scholar
  27. Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424CrossRefPubMedGoogle Scholar
  28. McWilliam JR, Mergen F (1958) Cytology of fertilization in Pinus. Bot Gaz 199:246–249CrossRefGoogle Scholar
  29. 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 208:200–209CrossRefPubMedGoogle Scholar
  30. 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 162:29–40CrossRefPubMedGoogle Scholar
  31. Nawaschin S (1898) Revision der Befruchtungsvorgange bei Lilium martagon und Fritillaria tenella. Bull Sci Acad Imp Sci Saint Pétersbourg 9:377–382Google Scholar
  32. Ohnishi Y, Hoshino R, Okamoto T (2014) Dynamics of male and female chromatin during karyogamy in rice zygotes. Plant Physiol 165:1533–1543CrossRefPubMedPubMedCentralGoogle Scholar
  33. Raghavan V (2003) Some reflections on double fertilization, from its discovery to the present. New Phytol 159:565–583CrossRefGoogle Scholar
  34. Ramsey J (2007) Unreduced gametes and neopolyploids in natural populations of Achillea borealis (Asteraceae). Heredity 98:143–150CrossRefPubMedGoogle Scholar
  35. Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501CrossRefGoogle Scholar
  36. Rhoades MM (1936) Note on the origin of triploidy in maize. J Genet 33:355–357CrossRefGoogle Scholar
  37. Rick CM (1945) A survey of cytogenetic causes of unfruitfulness in the tomato. Genetics 30:347–362PubMedPubMedCentralGoogle Scholar
  38. Runions CJ, Owens JN (1999) Sexual reproduction of interior spruce (Pinaceae). II. Fertilization to early embryo formation. Int J Plant Sci 160:641–652CrossRefGoogle Scholar
  39. Russell SD (1992) Double fertilization. Int Rev Cytol 140:357–390CrossRefGoogle Scholar
  40. Sandfaer J (1975) The occurrence of spontaneous triploids in different barley varieties. Hereditas 80:149–153CrossRefGoogle Scholar
  41. Sandfaer J (1979) Frequency of aneuploids in progenies of autotriploid barley, Hordeun vulgare L. Hereditas 90:213–217CrossRefGoogle Scholar
  42. Santelices B (2002) Recent advances in fertilization ecology of macroalgae. J Phycol 38:4–10CrossRefGoogle Scholar
  43. Schuel H (1984) The prevention of polyspermic fertilization in sea urchins. Biol Bull 167:271–309CrossRefGoogle Scholar
  44. 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 1:611–619CrossRefPubMedGoogle Scholar
  45. 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 142:779–792CrossRefPubMedGoogle Scholar
  46. Spielman M, Scott RJ (2008) Polyspermy barriers in plants: from preventing to promoting fertilization. Sex Plant Reprod 21:53–65CrossRefGoogle Scholar
  47. Sprague GF (1929) Hetero-fertilization in maize. Science 69:526–527CrossRefPubMedGoogle Scholar
  48. Sprague GF (1932) The nature and extent of hetero-fertilization in maize. Genetics 17:358–368PubMedPubMedCentralGoogle Scholar
  49. Suarez EY, Lopez AG, Naranjo CA (1992) Polyspermy versus unreduced male gametes as the origin of nonaploids (9x) common wheat plants. Caryologia 45:21–28CrossRefGoogle Scholar
  50. 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 277–314CrossRefGoogle Scholar
  51. Toda E, Ohnishi Y, Okamoto T (2016) Development of polyspermic rice zygotes. Plant Physiol 171:206–214CrossRefPubMedPubMedCentralGoogle Scholar
  52. Uchiumi T, Uemura I, Okamoto T (2007) Establishment of an in vitro fertilization system in rice (Oryza sativa L.). Planta 226:581–589CrossRefPubMedGoogle Scholar
  53. Wong JL, Wessel GM (2006) Defending the zygote: search for the ancestral animal block to polyspermy. Curr Top Dev Biol 72:1–151CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  • Takashi Okamoto
    • 1
  • Yukinosuke Ohnishi
    • 1
  • Erika Toda
    • 1
    • 2
  1. 1.Department of Biological SciencesTokyo Metropolitan UniversityTokyoJapan
  2. 2.Plant Breeding Innovation LaboratoryRIKEN Innovation CenterYokohamaJapan

Personalised recommendations