Skip to main content
SpringerLink
Log in

Bioluminescence of a firefly pupa: involvement of a luciferase isotype in the dim glow of pupae and eggs in the Japanese firefly, Luciola lateralis

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

We isolated cDNA for a luciferase isotype, LlLuc2, from the ovary of the Japanese firefly, Luciola lateralis. The gene product LlLuc2 showed 59% amino acid identity with LlLuc1, which had been isolated from the adult L. lateralis lantern. Molecular phylogenetic analysis indicated that LlLuc2 is an orthologue of LcLuc2 from Luciola cruciata. The spectral maxima of the luminescence by recombinant LlLuc1 and LlLuc2 were 550 and 539 nm, respectively. Quantitative PCR analysis revealed that LlLuc1 was expressed predominantly in larvae and adults, and LlLuc2 was expressed in eggs and pupae, which glow dimly, and we found that the in vivo luminescence spectra of the egg and pupa in L. lateralis were in good agreement with the in vitro luminescence spectrum by LlLuc2. These results suggest that, in L. lateralis, LlLuc1 is responsible for the yellowish luminescence of larval and adult lanterns, and LlLuc2 is responsible for the dim, greenish glow of eggs and whole pupae. Similar results were obtained in L. cruciata.

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

Similar content being viewed by others

References

  1. M. A. Branham, Lampyridae Latreille, 1817, in Handbook of Zoology, Vol. IV, Arthropoda: Insecta, Teilband 39, Coleoptera, Beetles. Vol. 2: Morphology and Systematics, ed. R. A. B. Leschen, R. G. Beutel and J. F. Lawrence, Walter de Gruyter, Berlin, 2010, pp. 141–149.

    Google Scholar 

  2. M. A. Branham, J. W. Wenzel, The origin of photic behavior and the evolution of sexual communication in fireflies (Coleoptera: Lampyridae), Cladistics, 2003, 19, 1–22.

    Article  Google Scholar 

  3. R. De Cock, E. Matthysen, Aposematism and bioluminescence: experimental evidence from glow-worm larvae (Coleoptera: Lampyridae), Evol. Ecol., 1999, 13, 619–639.

    Article  Google Scholar 

  4. R. Sagegami-Oba, N. Takahashi, Y. Oba, The evolutionary process of bioluminescence and aposematism in cantharoid beetles (Coleoptera: Elateroidea) inferred by the analysis of 18S ribosomal DNA, Gene, 2007, 400, 104–113.

    Article  CAS  Google Scholar 

  5. S. Watasé, On the Fireflies (Hotaru no Hanashi), Kaiseikan, Tokyo, Japan, 1902, (in Japanese).

    Google Scholar 

  6. Y. K. Okada, Two Japanese aquatic glowworms, Trans. Entomol. Soc. London, 1928, 76, 101–108 + 1 plt.

    Article  Google Scholar 

  7. S. Kanda, Firefly (Hotaru), Nippon Hakko Seibutsu Kenkyu Kai, Tokyo, Japan, 1935, (in Japanese).

    Google Scholar 

  8. W. D. McElroy, H. H. Seliger, E. H. White, Mechanism of bioluminescence, chemiluminescence and enzyme function in the oxidation of firefly luciferin, Photochem. Photobiol., 1969, 10, 153–170.

    Article  CAS  Google Scholar 

  9. S. Inouye, Firefly luciferase: an adenylate-forming enzyme for multicatalytic functions, Cell. Mol. Life Sci., 2010, 67, 387–404.

    Article  CAS  Google Scholar 

  10. V. R. Viviani, D. Amaral, R. Prado, F. G. C. Arnoldi, A new blue-shifted luciferase from the Brazilian Amydetes fanestratus (Coleoptera: Lampyridae) firefly: molecular evolution and structural/functional properties, Photochem. Photobiol. Sci., 2011, 10, 1879–1886.

    Article  CAS  Google Scholar 

  11. Y. Oba, M. Yoshida, T. Shintani, M. Furuhashi, S. Inouye, Firefly luciferase genes from the subfamilies Psilocladinae and Ototretinae (Lampyridae, Coleoptera), Comp. Biochem. Physiol., B: Biochem. Mol. Biol., 2012, 161, 110–116.

    Article  CAS  Google Scholar 

  12. F. R. Leach, L. Ye, H. J. Schaefferand L. M. Buck, Cloning and sequencing of a firefly luciferase from Photuris pennsylvanica, in Bioluminescence and Chemiluminescence, ed. J. W. Hastings, L. J. Kricka and P. E. Stanley, John Wiley & Sons, Chichester, 1997, pp. 240–243.

    Google Scholar 

  13. L. Ye, L. M. Buck, H. J. Schaeffer, F. R. Leach, Cloning and sequencing of a cDNA for firefly luciferase from Photuris pennsylvanica, Biochim. Biophys. Acta, 1997, 1339, 39–52.

    Article  CAS  Google Scholar 

  14. T. Masuda, H. Tatsumi, E. Nakano, Cloning and sequence analysis of cDNA for luciferase of a Japanese firefly, Luciola cruciata, Gene, 1989, 77, 265–270.

    Article  CAS  Google Scholar 

  15. H. Tatsumi, T. Masuda, N. Kajiyama, E. Nakano, Luciferase cDNA from Japanese firefly, Luciola cruciata: cloning, structure and expression in Escherichia coli, J. Biolumin. Chemilumin., 1989, 3, 75–78.

    Article  CAS  Google Scholar 

  16. Y. Oba, N. Mori, M. Yoshida, S. Inouye, Identification and characterization of a luciferase isotype in the Japanese firefly, Luciola cruciata, involving in the dim glow of firefly eggs, Biochemistry, 2010, 49, 10788–10795.

    Article  CAS  Google Scholar 

  17. Y. Oba, M. A. Branham, T. Fukatsu, The terrestrial bioluminescent animals in Japan, Zool. Sci., 2011, 28, 771–789.

    Article  CAS  Google Scholar 

  18. N. Ohba, Breeding and Study of Firefly (Hotaru no Kaikata to Kansatsu), Heart Shuppan, Tokyo, Japan, 2012, (in Japanese).

    Google Scholar 

  19. Y. Oba, M. Sato, Y. Ohta, S. Inouye, Identification of paralogous genes of firefly luciferase in the Japanese firefly, Luciola cruciata, Gene, 2006, 368, 53–60.

    Article  CAS  Google Scholar 

  20. K. Katoh, H. Toh, Recent developments in the MAFFT multiple sequence alignment program, Brief. Bioinform., 2008, 9, 286–298.

    Article  CAS  Google Scholar 

  21. F. Ronquist, J. P. Huelsenbeck, MrBayes 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 2003, 19, 1572–1574.

    Article  CAS  Google Scholar 

  22. S. Inouye, Y. Sahara, Soluble protein expression in E. coli cells using IgG-binding domain of protein A as a solubilizing partner in the cold induced system, Biochem. Biophys. Res. Commun., 2008, 376, 448–453.

    Article  CAS  Google Scholar 

  23. E. Eguchi, A. Nemoto, V. B. Meyer-Rochow, N. Ohba, A comparative study of spectral sensitivity curves in three diurnal and eight nocturnal species of Japanese fireflies, J. Insect Physiol., 1984, 30, 607–612.

    Article  Google Scholar 

  24. R. De Cock, Larval and adult emission spectra of bioluminescence in three European firefly species, Photochem. Photobiol., 2004, 79, 339–342.

    Article  Google Scholar 

  25. N. Ohba, Mystery of Fireflies (Hotaru Tenmetsu no Fushigi), Yokosuka City Mus., Yokosuka, Japan, 2004, (in Japanese).

    Google Scholar 

  26. S. J. Gould, G.-A. Keller, S. Subramani, Identification of a peroxisomal targeting signal at the carboxy terminus of firefly luciferase, J. Cell Biol., 1987, 105, 2923–2931.

    Article  CAS  Google Scholar 

  27. Y. Oba, M. Sato, M. Ojika, S. Inouye, Enzymatic and genetic characterization of firefly luciferase and Drosophila CG6178 as a fatty acyl-CoA synthetase, Biosci., Biotechnol., Biochem., 2005, 69, 819–828.

    Article  CAS  Google Scholar 

  28. J. C. Day, T. I. Goodall, M. J. Bailey, The evolution of the adenylate-forming protein family in beetles: multiple luciferase gene paralogues in fireflies and glow-worms, Mol. Phylogenet. Evol., 2009, 50, 93–101.

    Article  CAS  Google Scholar 

  29. U. Stolz, S. Velez, K. V. Wood, M. Wood, J. L. Feder, Darwinian natural selection for orange bioluminescent color in a Jamaican click beetle, Proc. Natl. Acad. Sci. U. S. A., 2003, 100, 14955–14959.

    Article  CAS  Google Scholar 

  30. Y. Oba, M. Kumazaki, S. Inouye, Characterization of luciferases and its paralogue in the Panamanian luminous click beetle Pyrophorus angustus: a click beetle luciferase lacks the fatty acyl-CoA synthetic activity, Gene, 2010, 452, 1–6.

    Article  CAS  Google Scholar 

  31. L. G. Strause, M. DeLuca, J. F. Case, Biochemical and morphological changes accompanying light organ development in the firefly, Photuris pennsylvanica, J. Insect Physiol., 1979, 25, 339–347.

    Article  CAS  Google Scholar 

  32. N. Hattori, N. Kajiyama, M. Maeda, S. Murakami, Mutant luciferase enzymes from fireflies with increased resistance to benzalkonium chloride, Biosci., Biotechnol., Biochem., 2002, 66, 2587–2593.

    Article  CAS  Google Scholar 

  33. G. D. Kutuzova, R. R. Hannahand K. V. Wood, Bioluminescence color variation and kinetic behavior relationships among beetle luciferases, in Bioluminescence and Chemiluminescence, ed. J. W. Hastings, L. J. Kricka and P. E. Stanley, John Wiley & Sons, Chichester, 1997, pp. 248–252.

    Google Scholar 

  34. B. R. Branchini, R. A. Magyar, M. H. Murtiashaw, S. M. Anderson, L. C. Helgerson, M. Zimmer, Site-directed mutagenesis of firefly luciferase active site amino acids: a proposed model for bioluminescence color, Biochemistry, 1999, 38, 13223–13230.

    Article  CAS  Google Scholar 

  35. B. R. Branchini, T. L. Southworth, J. P. DeAngelis, A. Roda, E. Michelini, Luciferase from the Italian firefly Luciola italica: molecular cloning and expression, Comp. Biochem. Physiol., B: Biochem. Mol. Biol., 2006, 145, 159–167.

    Article  Google Scholar 

  36. S. Kuribayashi, Hotaru, LUCIOLA CRUCIATA, Gakken Co., Tokyo, 2003, (in Japanese).

    Google Scholar 

  37. K. Minami, Studies on Fireflies (Hotaru no Kenkyu), Ohta Shoten, Hikone, Japan, 1961, (in Japanese).

    Google Scholar 

  38. Y. Haneda, On the Luminous Organisms (Hakkou Seibutsu no Hanashi), Hokuryukan, Tokyo, Japan, 1972, (in Japanese).

    Google Scholar 

  39. N. Ohba, Genji-Botaru, Bun-ichi Co., Tokyo, Japan, 1988, (in Japanese).

    Google Scholar 

  40. F. X. Williams, Photogenic organs and embryology of lampyrids, J. Morphol., 1916, 28, 145–207.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa-ku, Nagoya, 464-8601, Japan

    Yuichi Oba, Mana Furuhashi, Manabu Bessho & Shingo Sagawa

  2. Toin Gakuen High School, Kurogane-cho, Aoba-ku, Yokohama, 225-8502, Japan

    Haruyoshi Ikeya

  3. Yokohama Research Center, JNC Co., Kanazawa-ku, Yokohama, 236-8605, Japan

    Satoshi Inouye

Authors
  1. Yuichi Oba
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mana Furuhashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manabu Bessho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shingo Sagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haruyoshi Ikeya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Satoshi Inouye
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuichi Oba.

Additional information

Electronic supplementary information (ESI) available. See DOI: 10.1039/c3pp25363e

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oba, Y., Furuhashi, M., Bessho, M. et al. Bioluminescence of a firefly pupa: involvement of a luciferase isotype in the dim glow of pupae and eggs in the Japanese firefly, Luciola lateralis. Photochem Photobiol Sci 12, 854–863 (2013). https://doi.org/10.1039/c3pp25363e

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c3pp25363e

Search

Navigation