Skip to main content
SpringerLink
Log in

Sex-Specific Tyrian Purple Genesis: Precursor and Pigment Distribution in the Reproductive System of the Marine Mollusc, Dicathais orbita

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Exploitation of Tyrian purple from muricid molluscs, since antiquity, has prompted much interest in its chemical composition. Nevertheless, there remains a paucity of information on the biosynthetic routes leading to observed sexual differences in pigmentation. A liquid chromatography-mass spectrometry (LQ-MS) method was developed to simultaneously quantify dye pigments and precursors in male and female Dicathais orbita. The prochromogen, tyrindoxyl sulfate, was detected for the first time, by using this method in hypobranchial gland extracts of both sexes. Intermediates tyrindoxyl, tyrindoleninone, and tyriverdin were detected in female hypobranchial glands, along with 6,6′-dibromoindigo, while males contained 6-bromoisatin and 6,6′-dibromoindirubin. Multivariate analysis revealed statistically significant differences in the dye composition of male and female hypobranchial glands (ANOSIM, P = 0.002), thus providing evidence for sex-specific genesis of Tyrian purple in the Muricidae. Dye precursors were also present in male and female gonoduct extracts, establishing a mechanism for the incorporation of bioactive intermediates into muricid egg masses. These findings provide a model for investigating sex-specific chemical divergences in marine invertebrates and support the involvement of Tyrian purple genesis in muricid reproduction.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alvares, M., and Salas, M. 1991. Marine, nitrogen-containing heterocyclic natural products- structures and syntheses of compounds containing indole units. Heterocycles 32:1391–1452.

    Google Scholar 

  • Andreotti, A., Bonaduce, I., Colombini, M., and ibechini, E. 2004. Characterization of natural indigo and Tyrian purple by mass spectrometric techniques. Rapid Commun. Mass. Spectrom. 18:1213–1220.

    Article  PubMed  CAS  Google Scholar 

  • Bailey, K. 1929. The Elder Pliny’s Chapters on Chemical Subjects, Part 1. Edward Arnold, London.

    Google Scholar 

  • Baker, J. 1974. Tyrian purple. Ancient dye, a modern problem. Endeavour 33:11–17.

    Article  CAS  Google Scholar 

  • Baker, J., and Duke, C. 1973. Isolation from the hypobranchial glands of marine molluscs of 6-bromo-2,2-dimethylthioindolin-3-one and 6-bromo-2-methylthioindoleninone as alternative precursors to Tyrian purple. Aust. J. Chem. 26:2153–2157.

    Article  CAS  Google Scholar 

  • Baker, J., and Duke, C. 1976. Isolation of choline ester salts of tyrindoxyl sulphate from the marine molluscs Dicathais orbita and Mancinella keineri. Tetrahedron Lett. 15:1233–1234.

    Article  Google Scholar 

  • Baker, J., and Sutherland, M. 1968. Pigments of marine animals VIII. Precursors of 6,6′-dibromoindigotin (Tyrian purple) from the mollusc Dicathais orbita (Gmelin). Tetrahedron Lett. 1:43–46.

    Article  Google Scholar 

  • Bandaranayake, W. 2006. The nature of pigments in marine invertebrates. Nat. Prod. Rep. 23:223–255.

    Article  PubMed  CAS  Google Scholar 

  • Benkendorff, K., Bremner, J., and Davis, A. 2000. Tyrian purple precursors in the egg masses of the Australian muricid, Dicathais orbita: A possible defensive role. J. Chem. Ecol. 26:1037–1050.

    Article  CAS  Google Scholar 

  • Benkendorff, K., Bremner, J., and Davis, A. 2001. Indole derivatives from the egg masses of muricid molluscs. Molecules 6:70–78.

    Article  CAS  Google Scholar 

  • Benkendorff, K., Westley, C., and Gallardo, C. 2004. Observations of purple pigments in the egg capsules, hypobranchial and reproductive glands from seven species of the Muricidae (Gastropoda: Mollusca). Invertebr. Reprod. Dev. 46:93–102.

    CAS  Google Scholar 

  • Christophersen, C. 1983. Marine indoles, pp. 259–285, in P. J. Scheuer (ed.). Marine Natural Products, Chemical and Biological PerspectivesAcademic, New York, U.S.A.

    Google Scholar 

  • Christophersen, C., Watjen, F., Buchardt, O., and Anthoni, U. 1978. A revised structure of tyriverdin: The precursor to Tyrian purple. Tetrahedron. Lett. 34:2779–2781.

    CAS  Google Scholar 

  • Clark, R., and Cooksey, C. 1997. Bromoindirubins: the synthesis and properties of minor components of Tyrian purple and the composition of the colourant from Nucella lapillus. J. Soc. Dyers Colour 113:316–321.

    Article  CAS  Google Scholar 

  • Clarke, K., and Gorley, R. 2001. PRIMER v5: User Manual/Tutorial. PRIMER-E Ltd, Plymouth, U.K.

    Google Scholar 

  • Cole, W. 1685. Letter to the philosophical society of oxford containing observations on the purple fish. Phil. Trans. R. Soc. 15:1278.

    Article  Google Scholar 

  • Cooksey, C. 2001a. Tyrian Purple: 6,6′-dibromoindigo and related compounds. Molecules 6:736–769.

    CAS  Google Scholar 

  • Cooksey, C. 2001b. The synthesis and properties of 6-bromoindigo: Indigo blue or Tyrian purple? The effect of physical state on the colours of indigo and bromoindigos. Dyes in History and Archaeology 16–17:97–104.

    Google Scholar 

  • Cooksey, C. 2006. Marine indirubins, Indirubin, the Red Shade of Indigo. pp. 23–30, in L. Meijer, N. Guyard, A. L. Skaltsounis, and G. Eisenbrand (eds.). Life in Progress Editions, Roscoff, France.

    Google Scholar 

  • Cooksey, C., and Withnall, R. 2001. Chemical studies on Nucella lapillus. Dyes in History and Archaeology 16–17:91–96.

    Google Scholar 

  • Dubois, R. 1909. Recherches sur la pourpre et sur quelques autres pigments animaux. Arch. Zool. Expt. 42:471–590.

    Google Scholar 

  • Elsner, D., and Spanier, E. 1985. The dyeing with Murex extracts, an unusual dyeing method of wool to the biblical sky blue. Proceedings of the 7th International Wool and Textile Research Conference, Tokyo, Japan. 5:118–130.

  • Fleury, B., Coll, J., and Sammarco, P. 2006. Complementary (secondary) metabolites in a soft coral: Sex-specific variability, inter-clonal variability and competition. Mar. Ecol. 27:204–218.

    Article  CAS  Google Scholar 

  • Fretter, V. 1941. The genital ducts of some British stenoglossan prosobranchs. J. Mar. Biol. Ass. U.K. 25:173–211.

    Google Scholar 

  • Friedlander, P. 1909. Ueber den Farbstoff des antiken Purpura aus Murex brandaris. Ber. 42:765–770.

    CAS  Google Scholar 

  • Fujise, Y., Miwa, K., and Ito, S. 1980. Structure of tyriverdin, the intermediate precursor to Tyrian purple. Chem. Let. 6:631–632.

    Article  Google Scholar 

  • Gibson, C., and Wilson, S. 2003. Imposex still evident in Australia 10 years after tributyltin restrictions. Mar. Environ. Res. 55:101–112.

    Article  PubMed  CAS  Google Scholar 

  • Haubrichs, R. 2004. L’etude de la pourpre: Histoire d’une couleur, chimie et experimentations. Preist. Alp 20:133–160.

    Google Scholar 

  • Haubrichs, R. 2006. Natural history and iconography of purple shells, Indirubin, the Red Shade of Indigo. pp. 55–70, in L. Meijer, N. Guyard, A. L. Skaltsounis, and G. Eisenbrand (eds.). Life in Progress Editions, Roscoff, France.

    Google Scholar 

  • Higa, T., and Scheuer, P. 1976. Bisindoxyl-derived blue marine pigments. Heterocycles 4:227–230.

    CAS  Google Scholar 

  • Karapanagiotis, I., De, and Villemereuil, V. 2006. Identification of the colouring constituents of four natural indigoid dyes. Liq. Chromatogr. Relat. Technol. 29:1491–1502.

    Article  CAS  Google Scholar 

  • Kay, E., Wells, F., and Ponder, W. 1998. Class Gastropoda, Mollusca the Southern Synthesis Part B. p. 161, in P. Beesley, G. Ross, and A. Wells (eds.). CSIRO, Melbourne, Australia.

    Google Scholar 

  • Koren, Z. 1995. High-performance liquid chromatographic analysis of an ancient Tyrian purple dyeing vat from Israel. Isr. J. Chem. 35:117–124.

    CAS  Google Scholar 

  • Koren, Z. 2006. HPLC-PDA analysis of brominated indirubinoid, indigoid and isatinoid dyes, Indirubin, the Red Shade of Indigo. pp. 45–53, in L. Meijer, N. Guyard, A. L. Skaltsounis, and G. Eisenbrand (eds.). Life in Progress Editions, Roscoff, France.

    Google Scholar 

  • Magiatis, P., and Skaltsounis, A. L. 2006. From Hexaplex trunculus to new kinase inhibitory indirubins, Indirubin, the Red Shade of Indigo. pp. 147–156, in L. Meijer, N. Guyard, A. L. Skaltsounis, and G. Eisenbrand (eds.). Life in Progress Editions, Roscoff, France.

    Google Scholar 

  • Marchini, D., Giordano, P., Amons, R., Bernini, L., and Dallai, R. 1993. Purification and primary structure of ceratotoxins A and B, two antibacterial peptides from the female reproductive accessory glands of the medfly Ceratitis capitata (Insecta: Diptera). Insect Biochem. Mol. Biol. 5:591–598.

    Article  Google Scholar 

  • Mcgovern, P., and Michel, R. 1990. Royal purple dye: The chemical reconstruction of the ancient Mediterranean industry. Acc. Chem. Res. 23:152–158.

    Article  CAS  Google Scholar 

  • Mcgovern, P., Lazar, J., and Michel, R. 1990. The analysis of indigoid dyes by mass-spectrometry. J. Soc. Dyers Colour 106:22–25.

    Article  CAS  Google Scholar 

  • Meijer, L., Skaltsounis, A. L., Magiatis, P., Polychronopoulos, P., Knockaert, M., Leost, M., yan, X., Vonica, C., Brivanlou, A., Dajani, R. et al. 2003. GSK-3-Selective inhibitors derived from Tyrian purple indirubins. Chem. Biol. 10:1255–1266.

    Article  PubMed  CAS  Google Scholar 

  • Michel, R., Lazar, J., and Mcgovern, P. 1992. The chemical composition of indigoid dyes from the hypobranchial glandular secretions of Murex molluscs. J. Soc. Dyers Colour 108:150–154.

    Google Scholar 

  • Middlefart, P. 1992a. Morphology and anatomy of Chicoreus brunneus (Link, 1807): Description of shell and soft part. T. M. M. P. 11:54–60.

    Google Scholar 

  • Middlefart, P. 1992b. Morphology and anatomy of Chicoreus ramosus (Linnaeus, 1758) soft parts. T. M. M. P. 11:54–60.

    Google Scholar 

  • Naegel, L., and Cooksey, C. 2002. Tyrian purple from marine muricids, especially from Plicopurpura pansa (Gould, 1853). J. Shellfish Res. 21:193–200.

    Google Scholar 

  • Palma, H., Paredes, J., and Cristi, E. 1991. 6,6′-dibromoindigotin en capsulas de embriones di Concholepas concholepas (Bruguiere, 1789). Medio. Ambiente. 11:93–95.

    Google Scholar 

  • Peck, A. 1970. Aristotles’ Historia Animalium. Harvard University Press, Great Britain.

    Google Scholar 

  • Polec-Pawlak, K., Puchalaska, M., Witiwska-Jarosz, J., and Jarosz, M. 2006. Mass spectrometry: An efficient tool for the identification of indirubin and indigo related dyestuffs, Indirubin, the Red Shade of Indigo. pp. 115–125, in L. Meijer, N. Guyard, A. L. Skaltsounis, and G. Eisenbrand (eds.). Life in Progress Editions, Roscoff, France.

    Google Scholar 

  • Puchalaska, M., Polec-Pawlak, K., Zandronza, I., Hryszko, H., and Jarosz, M. 2004. Identification of natural indigoid dyes in natural organic pigments used in historical art objects by high-performance liquid chromatography coupled to electrospray ionization mass spectrometry. J. Mass Spectrom. 39:1441–1449.

    Article  CAS  Google Scholar 

  • Rash, L., and Hodgson, W. 2002. Pharmacology and biochemistry of spider venoms. Toxicon 40:225–254.

    Article  PubMed  CAS  Google Scholar 

  • Roller, R., Rickett, J., and Stickle, W. 1995. The hypobranchial gland of the estuarine snail Stramonita haemastoma canaliculata (Gray) (Prosobranchia: Muricidae): a light electron microscopical study. Am. Malacol. Bull. 11:177–190.

    Google Scholar 

  • Roseghini, M., Severini, C., Falconieri, E., and Erspamer, V. 1996. Choline esters and biogenic amines in the hypobranchial gland of 55 molluscan species of the neogastropod Muricidae Superfamily. Toxicon 34:33–55.

    Article  PubMed  CAS  Google Scholar 

  • Rosetto, M., Manetti, A., Giordano, P., Marri, L., Amos, R., Baldari, C., Marchini, D., and Dallai, R. 1996. Molecular characterization of ceratotoxin C, a novel antibacterial female-specific peptide of the ceratotoxin family from the medfly Ceratitis capitata. Eur. J. Biochem. 241:330–337.

    Article  PubMed  CAS  Google Scholar 

  • Susse, P., and Krampe, C. 1979. 6,6′-dibromo-indigo, a main component of Tyrian purple. Its crystal structure and light absorption. Naturwissenschaften 66:110.

    Article  Google Scholar 

  • Szostek, B., Orska-Gawrys, J., Surowiec, I., and Trojanowicz, M. 2003. Investigation of natural dyes occurring in historical Coptic textiles by high-performance liquid chromatography with UV-Vis and mass spectrometric detection. J. Chromatogr. 1012:179–192.

    Article  CAS  Google Scholar 

  • Verhecken, A. 1989. The indole pigments of Mollusca. Annales de la Societe Royale Zoologique de Belgique 119:181–197.

    Google Scholar 

  • Vine, K., Locke, J., anson, M., Benkendorff, K., Pyne, S., and Bremner, J. 2007. In vitro cytotoxicity evaluation of some substituted isatin derivatives. Bioorg. Med. Chem. 15:931–938.

    Article  PubMed  CAS  Google Scholar 

  • Westley, C., Vine, K., and Benkendorff, K. 2006. A proposed functional role for indole derivatives in reproduction and defense of the Muricidae (Neogastropoda: Mollusca), Indirubin, the Red Shade of Indigo. pp. 31–44, in L. Meijer, N. Guyard, A. L. Skaltsounis, and G. Eisenbrand (eds.). Life in Progress Editions, Roscoff, France.

    Google Scholar 

  • Withnall, R., Patel, D., Cooksey, C., and Naegel, L. 2003. Chemical studies of the purple dye of Purpura pansa. Dyes in History and Archaeology 1617:91–96.

    Google Scholar 

  • Wouters, J. 1992. A new method for the analysis of blue and purple dyes in textiles. Dyes in History and Archaeology 10:17–21.

    Google Scholar 

  • Wouters, J., and Verhecken, A. 1991. High-performance liquid chromatography of blue and purple indigoid natural dyes. J. Soc. Dyers Colour. 107:266–269.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. D. Jardine (Flinders Advanced Analytical Laboratory) for assistance with the LC-MS analyses. We are also grateful to Ms. A. Bogdanovic for preparation of male extracts, Dr. C. McIver, Assoc. Prof. J. Mitchell and Dr. C. Lenehan for providing useful feedback on the draft manuscript, and Inge Boesken Kanold for personal observations and images. We appreciate the provision of a Flinders University Postgraduate Scholarship to C. Westley. This research was supported by a Philanthropic research grant to K. Benkendorff.

Author information

Authors and Affiliations

  1. School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, S.A., 5001, Australia

    Chantel Westley & Kirsten Benkendorff

Authors
  1. Chantel Westley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kirsten Benkendorff
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kirsten Benkendorff.

APPENDIX 

APPENDIX 

Table 3 Characteristics of indigoid and indirubin standards and diagnostic parameters obtained by liquid chromatography-mass spectrometry
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Westley, C., Benkendorff, K. Sex-Specific Tyrian Purple Genesis: Precursor and Pigment Distribution in the Reproductive System of the Marine Mollusc, Dicathais orbita . J Chem Ecol 34, 44–56 (2008). https://doi.org/10.1007/s10886-007-9402-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-007-9402-2

Keywords

Search

Navigation