Skip to main content

Ascidian Sexual Reproductive Strategies: Mechanisms of Sperm-Egg Interaction and Self-Sterility

  • Chapter
  • First Online:

Part of the book series: Diversity and Commonality in Animals ((DCA))

Abstract

Ascidians (protochordate) are hermaphrodites that release sperm and eggs nearly simultaneously. However, self-fertilization is prohibited by self-sterility mechanisms during interaction between sperm and the vitelline coat (VC) of the eggs in many ascidian species, including Ciona robusta(former name: Ciona intetsinalis type A) and Halocynthia roretzi. A recent genetic study in C. robusta revealed that two tightly linked gene pairs in loci A and B, i.e., the sperm PKDREJ-like receptor s-Themis-A and the VC fibrinogen-like ligand v-Themis-A, and s-Themis-B and v-Themis-B, which include highly variable regions among individuals, are responsible for self-recognition. Sperm recognizes an egg as a self-egg when both alleles of s/v-Themis-A and s/v-Themis-B possess the same haplotypes. When attached to the VC of self-eggs, acute and drastic Ca2+ influx takes place in the sperm head and flagella probably via the Ca2+-conducting cation channel in the C-terminal region of s-Themis-B, which results in sperm detachment from the VC or decrease in sperm motility. We recently identified v-Themis-like, an acid-extractable VC protein with no allelic polymorphism, as a new candidate that participates in self-sterility. This self-sterility mechanism is closely related to the self-incompatibility systems in angiosperms. A different ascidian, Halocynthia roretzi, utilizes a different self/nonself-recognition system during fertilization, using an EGF-like repeat-containing VC protein, HrVC70. Moreover, the genome database of H. roretzi contains four pairs of s/v-Themis homologs. These gene products may also play a role in self-sterility in this species. This chapter describes the historic and current understandings of the mechanisms of gamete interaction and self/nonself-recognition in ascidian fertilization.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Akasaka M, Harada Y, Sawada H (2010) Vitellogenin C-terminal fragments participate in fertilization as egg-coat binding partners of sperm trypsin-like proteases in the ascidian Halocynthia roretzi. Biochem Biophys Res Commun 392:479–484

    Article  CAS  PubMed  Google Scholar 

  • Akasaka M, Kato KH, Kitajima K, Sawada H (2013) Identification of novel isoforms of vitellogenin expressed in ascidian eggs. J Exp Zool B Mol Dev Evol 320:118–128

    Article  CAS  PubMed  Google Scholar 

  • Artavanis-Tsakonas S, Matsumoto K, Fortini ME (1995) Notch signaling. Science 268:225–232

    Article  CAS  PubMed  Google Scholar 

  • Ban S, Harada Y, Yokosawa H, Sawada H (2005) Highly polymorphic vitelline-coat protein HaVC80 from the ascidian, Halocynthia aurantium: Structural analysis and involvement in self/nonself recognition during fertilization. Dev Biol 286:440–451

    Article  CAS  PubMed  Google Scholar 

  • Brozovic M, Martin C, Dantec C, Dauga D, Mendez M, Simion P, Percher M, Laporte B, Scornavacca C, Di Gregorio A, Fujiwara S, Gineste M, Lowe EK, Piette J, Racioppi C, Ristoratore F, Sasakura Y, Takatori N, Brown TC, Delsuc F, Douzery E, Gissi C, McDougall A, Nishida H, Sawada H, Swalla BJ, Yasuo H, Lemaire P (2015) Aniseed 2015: a digital framework for the comparative developmental biology of ascidians. Nucleic Acid Res 44(D1):D808–D818

    Article  CAS  PubMed  Google Scholar 

  • Brunetti R, Gissi C, Pennati R, Caicci F, Gasparini F, Manni L (2015) Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis. J Zool Syst Evol 53:186–193

    Article  Google Scholar 

  • Casazza G, De Santis R, Pinto MR (1984) Sperm binding to eggs of Ciona intestinalis. Role of Ca2+. Exp Cell Res 155:261–266

    Article  CAS  PubMed  Google Scholar 

  • De Santis R, Pinto MR (1991) Gamete self-discrimination in ascidians: a role for the follicle cells. Mol Reprod Dev 29:47–50

    Article  PubMed  Google Scholar 

  • De Santis R, Jamunno G, Rosati F (1980) A study of the chorion and the follicle cells in relation to the sperm-egg interaction in the ascidian, Ciona intestinalis. Dev Biol 74:490–499

    Article  PubMed  Google Scholar 

  • De Santis R, Pinto MR, Cotellin F, Rosati F, Monroy A, D’Alessio G (1983) A fucosyl glycoprotein component with sperm receptor and sperm-activating activity from the vitelline coat of Ciona intestinalis eggs. Exp Cell Res 148:508–513

    Article  PubMed  Google Scholar 

  • De Tomaso AW, Nyholm SV, Palmeri KJ, Ishizuka KJ, Ludington WB, Mitchel K, Weissman IL (2005) Isolation and characterization of a protochordate histocompatibility locus. Nature 438:454–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Florman HM, Melissa KJ, Sutton KA (2008) Regulating the acrosome reaction. Int J Dev Biol 82:503–510

    Article  CAS  Google Scholar 

  • Fuke TM (1983) Self and nonself recognition between gametes of the ascidian, Halocynthia roretzi. Roux’s Arch. Dev Biol 192:347–352

    Google Scholar 

  • Fuke M, Numakunai M (1996) Establishment of self-sterility of eggs in the ovary of the solitary ascidian, Halocynthia roretzi. Roux’s Arch Dev Biol 205:391–400

    Article  CAS  Google Scholar 

  • Fuke M, Numakunai T (1999) Self-sterility of eggs induced by exogenous and endogenous protease in the solitary ascidian Halacynthia roretzi. Mol Reprod Dev 52:99–106

    Article  CAS  Google Scholar 

  • Fukumoto M (1988) Fertilization in ascidians: apical processes and gamete fusion in Ciona intestinalis. J Cell Sci 89:1890196

    Google Scholar 

  • Fukumoto M (1990a) Morphological aspects of ascidian fertilization: acrosome reaction, apical processes and gamete fusion in Ciona intestinalis. Invertebr Reprod Dev 17:147–154

    Article  Google Scholar 

  • Fukumoto M (1990b) The acrosome reaction in Ciona intestinalis (Ascidia, Tunicata). Dev Growth Differ 32:51–55

    Article  Google Scholar 

  • Fukumoto M (1990c) Morphological aspects of ascidian fertiizattion. Zool Sci 7:989–998

    Google Scholar 

  • Gunaratne HJ, Moy GW, Kinukawa M, Miyata S, Mar SA, Vacquier VD (2007) The 10 sea urchin receptor for egg jelly proteins (SpREJ) aer members of the polycystic kidney disease-1 (PKD1) family. MBC. Genomics 8:235

    PubMed  Google Scholar 

  • Harada Y, Sawada H (2007) Proteins interacting with the ascian vitelline-coat sperm receptor HrVC70 as revealed by yeast two-hybrid screening. Mol Reprod Dev 74:1178–1187

    Article  CAS  PubMed  Google Scholar 

  • Harada Y, Sawada H (2008) Allorecognition mechanisms during ascidian fertilization. Int J Dev Biol 52:637–645

    Article  CAS  PubMed  Google Scholar 

  • Harada Y, Takagaki Y, Sugnagawa M, Saito T, Yamada L, Taniguchi H, Shobuchi E, Sawada H (2008) Mechanism of self-sterility in a hermaphroditic chordate. Science 320:548–550

    Article  CAS  PubMed  Google Scholar 

  • Hoshi M (1985) Lysin. In: Metz CB, Monroy A (eds) Biology of Fertilization, vol 2. Academic, Orlando, pp 431–462

    Chapter  Google Scholar 

  • Hoshi M (1986) Sperm glycosidase as a plausible mediator of sperm binding to the vitelline envelope in ascidians. Adv Exp Med Biol 207:251–260

    PubMed  CAS  Google Scholar 

  • Iwano M, Takayama S (2012) Self/non-self discrimination in angiosperm self-incompatibility. Curr Opin Plant Biol 15:78–83

    Article  PubMed  Google Scholar 

  • Kamei N, Glabe CC (2003) The species specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein. Genes Dev 17:2502–2507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawamura K, Nomura M, Kameda T, Shimamoto H, Nakauchi M (1991) Self-nonself recognition activity extracted from self-sterile eggs of the ascidian, Ciona intestinalis. Dev Growth Differ 33:139–148

    Article  Google Scholar 

  • Khalturin K, Kurn U, Pinnow N, Bosch TC (2005) Towards a molecular code for individuality in the absence of MHC: screening for individually variable genes in the urochordate Ciona intestinalis. Dev Comp Immunol 29:759–773

    Article  CAS  PubMed  Google Scholar 

  • Kürn U, Sommer F, Bosch TC, Khalturin K (2007a) In the urochordate Ciona intestinalis zona pellucida domain proteins vary among individuals. Dev Comp Immunol 31:1242–1254

    Article  CAS  PubMed  Google Scholar 

  • Kürn U, Sommer F, Hemmrich G, Bosch TC, Khalturin K (2007b) Allorecognition in urochordates: identification of a highly variable complement receptor-like protein expressed in follicle cells of Ciona. Dev Comp Immunol 31:360–371

    Article  CAS  PubMed  Google Scholar 

  • Lambert CC (1989) Ascidian eggs release glycosidase activity which aids in the block against polyspermy. Development 105:415–420

    PubMed  CAS  Google Scholar 

  • Lambert CC, Koch R (1988) Sperm binding and penetration during ascidian fertilization. Dev Growth Differ 30:325–336

    Article  Google Scholar 

  • Marino R, Pinto MR, Cotelli F, Lamia CL, De Santis R (1998) The hsp70 protein is involved in the acquisition of gamete self-sterility in the ascidian Ciona intestinalis. Development 125:899–907

    PubMed  CAS  Google Scholar 

  • Marino R, De Santis R, Giuliano P, Pinto MR (1999) Follicle cell proteasome activity and acid extract from the egg vitelline coat prompt the onset of self-sterility in Ciona intestinalis oocytes. Proc Natl Acad Sci U S A 96:9633–9636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto M, Hirata J, Hirohashi N, Hoshi M (2002) Sperm-egg binding mediated by sperm α-L-fucosidase in the ascidian, Halocynthia roretzi. Zool Sci 19:43–48

    Article  CAS  PubMed  Google Scholar 

  • Matsuura K, Sawada H, Yokosawa H (1993) Purification and properites of N-acetylglucosaminidase from eggs of the ascidian, Halocynthia roretzi. Eur J Biochem 218:535–541

    Article  CAS  PubMed  Google Scholar 

  • Matsuura K, Sawada H, Yokosawa H (1995) N-Acetylglucosaminidase inhibitor isolated from the vitelline coat of ascidian eggs is a candidate sperm receptor. Biochem Biophys Res Commun 213:311–316

    Article  CAS  PubMed  Google Scholar 

  • Mengerink KJ, Vacquier VD (2001) Glycobiology of sperm-egg interactions in deuterostomes. Glycobiology 11:37R–43R

    Article  CAS  PubMed  Google Scholar 

  • Mengerink KJ, Moy GW, Vacquier VD (2002) suREJ3, a polycystin-1 protein, is cleaved a thte GPS domain and localizes to the acrosomal regions of sea urchin sperm. J Biol Chem 277:943–948

    Article  CAS  PubMed  Google Scholar 

  • Morgan TH (1910) Cross- and self-fertilization in Ciona intestinalis. Roux Arch Entwicklungsmech 30:206–235

    Article  Google Scholar 

  • Morgan TH (1923) Removal of the block to self-fertilization in the ascidian Ciona. Proc Natl Acad Sci U S A 9:170–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan TH (1939) The genetic and the physiological problems of self-sterility in Ciona. III. Induced self-fertilization. J Exp Zool 80:19–54

    Article  CAS  Google Scholar 

  • Morgan TH (1942) The genetic and the physiological problems of self-sterility in Ciona. V. The genetic problem. J Exp Zool 90:199–228

    Article  Google Scholar 

  • Morgan TH (1944) The genetic and the physiological problems of self-sterility in Ciona. VI. Theoretical discussion of genetic data. J Exp Zool 95:37–59

    Article  Google Scholar 

  • Moy GW, Mendoza LM, Schulz JR, Swanson WJ, Grabe CG, Vacquier VD (1996) The sea urchin sperm receptor for egg jelly is a modulator with extensive homology to the human polycystic kidney disease protein, PKD1. J Cell Biol 133:809–817

    Article  CAS  PubMed  Google Scholar 

  • Murabe N, Hoshi M (2002) Re-examination of sibling cross-sterility in the ascidian, Ciona intestinalis: genetic background of the self-sterility. Zool Sci 19:527–538

    Article  PubMed  Google Scholar 

  • Nakazawa S, Shirae-Kurayamashi M, Otsuka K, Sawada H (2015) Proteomics of ionomycin-induced ascidian sperm reaction: released and exposed sperm proteins in the ascidian Ciona insetinalis. Proteomics (in press). doi:https://doi.org/10.1002/pmic.201500162

    Article  PubMed  CAS  Google Scholar 

  • Otsuka K, Yamada L, Sawada H (2013) cDNA cloning, localization, and candidate binding partners of acid-extractable vitelline-coat protein Ci-v-Themis-like in the ascidian Ciona intestinalis. Mol Reprod Dev 80:840–848

    Article  CAS  PubMed  Google Scholar 

  • Pinto MR, De Stantis R, Marino R, Usui N (1995) Specific induction of self-discrimination by follicle cells in Ciona intestinalis. Dev Growth Differ 37:287–291

    Article  Google Scholar 

  • Rosati F, De Santis R (1978) Studies on fertlization in the ascidains I. Self-sterility and specific recognition between gametes of Ciona intestinalis. Exp Cell Res 112:111–119

    Article  CAS  PubMed  Google Scholar 

  • Rosati F, De Santis R (1980) Role of the surface carbohydrates in sperm-egg interaction in Ciona intestinalis. Nature 283:762–764

    Article  CAS  PubMed  Google Scholar 

  • Saito Y, Hirose E, Watanabe H (1994) Allorecognition in compound ascidians. Int J Dev Biol 38:237–247

    PubMed  CAS  Google Scholar 

  • Saito T, Shiba K, Inaba K, Yamada L, Sawada H (2012) Self-incompatiblity response induced by calcium increase in seprm of the ascidian Ciona intestinalis. Proc Natl Acad Sci U S A 109:4158–4162

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakairi K, Shirai H (1991) Possible MIS production by follicle cell in spontaneous oocyte maturation of the ascidian Halocynthia roretzi. Dev Growth Diff 33:155–162

    Article  CAS  Google Scholar 

  • Sawada H (2002) Ascidian sperm lysin system. Zool Sci 19:139–151

    Article  CAS  PubMed  Google Scholar 

  • Sawada H, Pinto MR, De Santis R (1998) Participation of sperm proteasome in fertilization of the Phlebobranch ascidian Ciona intestinalis. Mol Reprod Dev 50:493–498

    Article  CAS  PubMed  Google Scholar 

  • Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, Kodama E, Takizawa S, Yokosawa H (2002) Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci U S A 99:1223–1228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawada H, Tanaka E, Ban S, Yamasaki C, Fujino J, Ooura K, Abe Y, Matsumoto K, Yokosawa H (2004) Self/nonself recognition in ascidian fertilization: Vitelline coat protein HrVC70 is a candidate allorecognition molecule. Proc Natl Acad Sci U S A 101:15615–15620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawada H, Akasaka M, Yokota N, Sakai N (2005) Modification of ascidian fertilization related gamete proteins by ubiquitination, proteolysis, and glycosylation. In: Tokumoto T (ed) New impact on protein modifications in the regulation of reproductive system. Research Signpost, Trivandrum, pp 61–81

    Google Scholar 

  • Sawada H, Mino M, Akasaka M (2014a) Sperm proteases and extracellular ubiquitin-proteasome system involved in fertilization of ascidians and sea urchins. In: Sutovsky P (ed) Posttranslational protein modifications in the reproductive system, Advances in Experimental Medicince and Biology, vol 759. Springer, New York/Heidelberg/Dordrecht/London, pp 1–11

    Google Scholar 

  • Sawada H, Morita M, Iwano M (2014b) Self/non-self recognition mechanisms in sexual reproduction: new insight into the self-incompatibility system shared by flowering plants and hermaphroditic animals. Biochem Biophys Res Commun 450:1142–1148

    Article  CAS  PubMed  Google Scholar 

  • Scofield VL, Schlumpberger JM, Weissman IL (1982a) Protochordate allorecognition is controlled by a MHC-like gene complex. Nature 295:499–503

    Article  CAS  PubMed  Google Scholar 

  • Scofield VL, Schlumpberger JM, Weissman IL (1982b) Colony specificity in the colonial tunicate Botryllus and the origins of vertebrate immunity. Am Zool 22:783–794

    Article  Google Scholar 

  • Sommer F, Awazu S, Anton-Erxleben F, Jian D, Klimovich AV, Samoilovich MP, Stow Y, Krüss M, Gelhaus C, Kürn U, Bosch TC, Khalturin K (2012) Blood system formation in the urochordate Ciona intestinalis requires the variable receptor vCRL1. Mol Biol Evol 29:3081–3093

    Article  CAS  PubMed  Google Scholar 

  • Sutton KA, Jungnickel ML, Ward CJ, Harris PC, Florman HM (2006) Functional characgterization of PKEREJ, a male sperm cell-restricted polycystin. J Cell Physiol 209:493–500

    Article  CAS  PubMed  Google Scholar 

  • Sutton KA, Jungnickel MK, Florman HM (2008) A polycystin-1 controles postcopulatory reproductive selection in mice. Proc Natl Acad Sci U S A 105:8661–8666

    Article  PubMed  PubMed Central  Google Scholar 

  • Takayama S, Isogai A (2005) Self-incompatibility in plants. Ann Rev Plant Biol 56:467–489

    Article  CAS  Google Scholar 

  • Urayama S, Harada Y, Nakagawa Y, Ban S, Akasaka M, Kawasaki N, Sawada H (2008) Ascidian sperm glycosylphosphatidylinositol-anchored CRISP-like protein as a binding partner for an allorecognizable sperm receptor on the vitelline coat. J Biol Chem 283:21725–21733

    Article  CAS  PubMed  Google Scholar 

  • Vacquier VD, Moy GW (1997) The fucose sulfate polymer of egg jelly binds to sperm REJ and is the inducer of the sea urchin sperm acrosome reaction. Dev Biol 192:125–135

    Article  CAS  PubMed  Google Scholar 

  • Vacquier VD, Sawanson WJ (2011) Selection in the rapid evolusion of gamete recognition proteins in marine invertebrates. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a002931

  • Voskoboynik A, Newman AM, Corey DM, Sahoo D, Pushkarev D, Neff NF, Passarelli B, Koh W, Ishizuka KJ, Palmeri KJ, Dimov IK, Keasar C, Fan HC, Mantalas GL, Sinha R, Penland L, Quake SR, Weissman IL (2013) Identification of a colonial chordate histocompatibility gene. Science 341:384–387

    Article  CAS  PubMed  Google Scholar 

  • Weissman IL, Saito Y, Rinkevich B (1990) Allorecognition histocompatibility in a protochordate species: is the relationship to MHC somatic or structural? Immunol Rev 113:227–241

    Article  CAS  PubMed  Google Scholar 

  • Yamada L, Saito T, Taniguchi H, Sawada H, Harada Y (2009) Comprehensive egg coat proteome of the ascidian Ciona intestinalis reveals gamete recognition molecules involved in self-sterility. J Biol Chem 284:9402–9410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi A, Saito T, Yamada L, Taniguchi H, Harada Y, Sawada H (2011) Identification and localization of the sperm CRISP family protein CiUrabin involved in gamete interaction in the ascidian Ciona intestinalis. Mol Reprod Dev 78:488–497

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported in part by Grant-in-Aids for Scientific Research on Innovative Areas from MEXT, Japan to HS (21112001, 21112002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hitoshi Sawada .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Japan KK, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sawada, H., Nakazawa, S., Shirae-Kurabayashi, M. (2018). Ascidian Sexual Reproductive Strategies: Mechanisms of Sperm-Egg Interaction and Self-Sterility. In: Kobayashi, K., Kitano, T., Iwao, Y., Kondo, M. (eds) Reproductive and Developmental Strategies. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56609-0_23

Download citation

Publish with us

Policies and ethics