Skip to main content

Advertisement

SpringerLink
Log in

Sequestration of the plant secondary metabolite, colchicine, by the noctuid moth Polytela gloriosae (Fab.)

  • Original Article
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

Colchicine, a well-known alkaloid, is a potent inhibitor of polymerization of tubulin leading to mitotic arrest. It is highly toxic to eukaryotic cells but also widely used in the field of medicine and plant breeding. Gloriosa superba (family: Colchicaceae) is an important natural source of colchicine. The seeds, tubers and leaves of this plant contain about 0.8, 1.2 and 0.014% colchicine by dry weight respectively. A noctuid moth, Polytela gloriosae (family: Noctuidae), feeds voraciously on leaves of G. superba without any adverse effect. However, the fate of colchicine and the mechanisms by which the insect is able to overcome the toxicity of the metabolite is not known. Here, we trace the fate of colchicine in both, the larva and moth of P. gloriosae. Colchicine was quantified in different body parts of the larvae and moth by high performance liquid chromatography, liquid chromatography mass spectrophotometry and nuclear magnetic resonance methods. Of the total colchicine taken in by the larva, a larger portion was excreted, while the rest was sequestered in its cuticle. In the moths however, the wings, legs and antennae were found to accumulate high amount of colchicine. The sequestered colchicine, in both the larva and adult, were chemically identical to that found in the plant. Negligible amounts of demethyl-(−)-colchicine, a less toxic derivative of colchicine was also detected. We discuss the probable adaptive significance of sequestration of colchicine by the insect.

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
Fig. 5

Similar content being viewed by others

References

  • Ade R, Rai MK (2010) Colchicine, current advances and future prospects. Nusant Biosci 2(2):90–96

    Google Scholar 

  • Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10(12):594–602

    Article  CAS  PubMed  Google Scholar 

  • Allegra E, Titball RW, Carter J, Champion OL (2018) Galleria  mellonella larvae allow the discrimination of toxic and non-toxic chemicals. Chemosphere 198:469–472

    Article  CAS  PubMed  Google Scholar 

  • Bowers MD (1993) Aposematic caterpillars: life-styles of the warningly colored and unpalatable. In: Stamp NE, Casey TM (eds) Caterpillar. Chapman & Hall, New York, pp 331–371

    Google Scholar 

  • Brown KS Jr (1988) Mimicry, aposematism and crypsis in neotropical Lepidoptera: the importance of dual signals. Bull Soc Zool France 113:83–101

    Google Scholar 

  • Buskila D, Zaks N, Neumann L, Livneh A, Greenberg S, Pras M, Langevitz P (1997) Quality of life of patients with familial Mediterranean fever. Clin Exp Rheumatol 15:355–360

    CAS  PubMed  Google Scholar 

  • Caperta AD, Delgado M, Ressurreição F, Meister A, Jones RN, Viegas W, Houben A (2006) Colchicine-induced polyploidization depends on tubulin polymerization in c-metaphase cells. Protoplasma 227(2–4):147–153

    Article  CAS  PubMed  Google Scholar 

  • Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22(6):298–307

    Article  PubMed  Google Scholar 

  • Dussourd DE (2003) Chemical stimulants of leaf-trenching by cabbage loopers: natural products, neurotransmitters, insecticides, and drugs. J Chem Ecol 29(9):2023–2047

    Article  CAS  PubMed  Google Scholar 

  • Finnie JF, Van Staden J (1989) In vitro propagation of Sandersonia and Gloriosa plant. Cell Tissue Organ Cult 19(2):151–158

    Article  Google Scholar 

  • Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14(5):10242–10297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh S, Jha S (2008) Colchicine—an overview for plant biotechnologists. In: Springer (eds) Bioactive molecules and medicinal plants. Springer, Berlin, pp 215–232

  • Gökel Y, Canataroglu A, Satar S, Koseoglu Z (2000) Colchicine toxicity: a patient with pneumopericardium. Turk J Med Sci 30(4):401–403

    Google Scholar 

  • Hanumanthaswamy BC, Rajgopal D (1995) Insect pests of Gloriosa superba Linn. an Indian medicinal plant. Indian J For 1/8(2):101–103

    Google Scholar 

  • Hari M, Wang Y, Veeraraghavan S, Cabral F (2003) Mutations in α-and β-tubulin that stabilize microtubules and confer resistance to colcemid and vinblastine1. Mol Cancer Ther 2(7):597–605

    CAS  PubMed  Google Scholar 

  • Hartung EF (1954) History of the use of colchicum and related medicaments in gout: with suggestions for further research. Ann Rheum Dis 13(3):190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey PH, Paxton RJ (1981) The evolution of aposematic coloration. Oikos 37:391–396

    Article  Google Scholar 

  • Heckel DG (2014) Insect detoxification and sequestration strategies. In: Voelckel C, Jander G (eds) Annual review of plant biology, vol 47. Wiley, New York, pp 77–114

    Chapter  Google Scholar 

  • Heidel-Fischer HM, Vogel H (2015) Molecular mechanisms of insect adaptation to plant secondary compounds. Curr Opin Insect Sci 8:8–14

    Article  Google Scholar 

  • Helmus MR, Dussourd DE (2005) Glues or poisons: which triggers vein cutting by monarch caterpillars? Chemoecology 15(1):45–49

    Article  CAS  Google Scholar 

  • Holzinger F, Wink M (1996) Mediation of cardiac glycoside insensitivity in the monarch butterfly (Danaus  plexippus): role of an amino acid substitution in the ouabain binding site of Na+, K+-ATPase. J Chem Ecol 22(10):1921–1937

    Article  CAS  PubMed  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  CAS  Google Scholar 

  • Inoue S (1981) Cell division and the mitotic spindle. J Cell Biol 91(3):131–147

    Article  PubMed Central  Google Scholar 

  • Kavina J, Gopi R, Panneerselvam R (2011) Gloriosa  superba Linn—a medicinally important plant. Drug Invent Today 3(6):69–71

    Google Scholar 

  • Larsson S, Ronsted N (2014) Reviewing Colchicaceae alkaloids—perspectives of evolution on medicinal chemistry. Curr Top Med Chem 14(2):274–289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levy M, Spino M, Read SE (1991) Colchicine: a state‐of‐the‐art review. Pharmacother J Hum Pharmacol Drug Ther 11(3):196–211

    CAS  Google Scholar 

  • Maddrell SH, Gardiner BO (1976) Excretion of alkaloids by Malpighian tubules of insects. J Exp Biol 64(2):267–281

    CAS  PubMed  Google Scholar 

  • Malcolm SB, Cockrell BJ, Brower LP (1989) Cardenolide fingerprint of monarch butterflies reared on common milkweed Asclepias syriaca L. J Chem Ecol 15(3):819–853

    Article  CAS  PubMed  Google Scholar 

  • Marty MA, Krieger RI (1984) Metabolism of uscharidin, a milkweed cardenolide, by tissue homogenates of monarch butterfly larvae Danaus plexippus L. J Chem Ecol 10(6):945–956

    Article  CAS  PubMed  Google Scholar 

  • Nautiyal OP (2011) Isolation of 3-demethylcolchicine from Gloriosa  superba sludge and coupling with α-acetobromoglucose to yield colchicoside and thiocolchicoside. J Nat Prod 4:87–93

    CAS  Google Scholar 

  • Nishida R (1994) Sequestration of plant secondary compounds by butterflies and moths. Chemoecology 5(3–4):127–138

    Article  Google Scholar 

  • Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47(1):57–92

    Article  CAS  PubMed  Google Scholar 

  • Opitz SE, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19(3):117–154

    Article  CAS  Google Scholar 

  • Rajagopal CV, Kandhasamy R (2009) Genetic variability of kazhappai kizhangu (Gloriosa  superba L.) in Tamil Nadu assessed using morphological and biochemical traits. J Trop Agric 47(1):77–79

    Google Scholar 

  • Ramesha BT, Zuehlke S, Vijaya RC, Priti V, Ravikanth G, Ganeshaiah KN, Spiteller M, Shaanker RU (2011) Sequestration of camptothecin, an anticancer alkaloid, by chrysomelid beetles. J Chem Ecol 37(5):533–536

    Article  CAS  PubMed  Google Scholar 

  • Ramesha BT, Suma HK, Senthilkumar U, Priti V, Ravikanth G, Vasudeva R, Kumar TS, Ganeshaiaha KN, Shaanker RU (2013) New plant sources of the anti-cancer alkaloid, camptothecine from the Icacinaceae taxa India. Phytomedicine 20(6):521–527

    Article  CAS  PubMed  Google Scholar 

  • Rosenthal GA, Berenbaum MR (2012) Herbivores: their interactions with secondary plant metabolites: ecological and evolutionary processes, vol 2. Academic Press, London

    Google Scholar 

  • Rothschild M (1985) British aposematic Lepidoptera. In: Heath J (ed) The moths and butterflies of Great Britain and Ireland, AM Emmet. Harley Books, Essex, pp 9–62

    Google Scholar 

  • Rothschild M, Moore BP, Brown WV (1984) Pyrazines as warning odour components in the monarch butterfly, Danaus  plexippus, and in moths of the genera Zygaena and Amata (Lepidoptera). Biol J Linn Soc Lond 23(4):375–380

    Article  Google Scholar 

  • Sajitha TP, Manjunatha BL, Siva R, Gogna N, Dorai K, Ravikanth G, Shaanker RU (2018) Mechanism of resistance to camptothecin, a cytotoxic plant secondary metabolite, by Lymantria sp. larvae. J Chem Ecol 44:1–10

    Article  CAS  Google Scholar 

  • Sarvalingam A, Rajendran A (2016) Rare, endangered and threatened (RET) climbers of Southern Western Ghats India. Rev Chil Hist Nat 89(1):9

    Article  Google Scholar 

  • Sathe TV (2015) Biology, intrinsic rate of increase and control of Indian lily moth Polytela  gloriosae (Fab.) (Lepidoptera: Noctuidae). Int J Pharm Biol Sci 6(1):940–950

    Google Scholar 

  • Schibler MJ, Barlow SB, Cabral FERNANDO (1989) Elimination of permeability mutants from selections for drug resistance in mammalian cells. FASEB J 3(2):163–168

    Article  CAS  PubMed  Google Scholar 

  • Sillen-Tullberg B, Leimar O (1988) The evolution of gregariousness in distasteful insects as a defense against predators. Am Nat 132(5):723–734

    Article  Google Scholar 

  • Slobodnick A, Shah B, Pillinger MH, Krasnokutsky S (2015) Colchicine: old and new. Am J Med 128(5):461–470

    Article  CAS  PubMed  Google Scholar 

  • Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Tullberg BS, Hunter AF (1996) Evolution of larval gregariousness in relation to repellent defences and warning coloration in tree-feeding Macrolepidoptera: a phylogenetic analysis based on independent contrasts. Biol J Linn Soc Lon 57(3):253–276

    Article  Google Scholar 

  • Vinnersten A, Larsson S (2010) Colchicine is still a chemical marker for the expanded Colchicaceae. Biochem Syst Ecol 38(6):1193–1198

    Article  CAS  Google Scholar 

  • Von Nickisch-Rosenegk E, Wink M (1993) Sequestration of pyrrolizidine alkaloids in several arctiid moths (Lepidoptera: Arctiidae). J Chem Ecol 19(9):1889–1903

    Article  Google Scholar 

Download references

Acknowledgements

The work was supported by Grants from SERB/EMR/2016/005481 New Delhi, India to R. Uma Shaanker. Dr. Senthil Kumar Umapathy and Mrs. Hima Bindu, School of Ecology and Conservation, University of Agricultural Sciences, GKVK, Bengaluru assisted in locating and collecting the insect samples. Prof. C A Viraktamath and Dr. Yeshwanth H M, Department of Entomology, University of Agricultural Sciences, GKVK, Bengaluru confirmed the identity of the insect.

Author information

Authors and Affiliations

  1. Department of Biotechnology, School of Biosciences and Technology, Vellore Institute of Technology, Vellore, Tamilnadu, 632014, India

    T. P. Sajitha & R. Siva

  2. Department of Crop Physiology and School of Ecology and Conservation, University of Agricultural Sciences, GKVK, Bengaluru, Karnataka, 560065, India

    T. P. Sajitha, B. L. Manjunatha, P. Rajani & R. Uma Shaanker

  3. Department of Physical Sciences, Indian Institute of Science Education and Research, Mohali, Sector 8, SAS Nagar, Punjab, 160062, India

    Gogna Navdeep & Dorai Kavita

  4. Ashoka Trust for Research in Ecology and the Environment, Royal Enclave, Srirampura, Jakkur Post, Bengaluru, Karnataka, 560064, India

    G. Ravikanth & R. Uma Shaanker

Authors
  1. T. P. Sajitha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Siva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. L. Manjunatha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Rajani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gogna Navdeep
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dorai Kavita
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Ravikanth
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. R. Uma Shaanker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Uma Shaanker.

Additional information

Communicated by Günther Raspotnig.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 243 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sajitha, T.P., Siva, R., Manjunatha, B.L. et al. Sequestration of the plant secondary metabolite, colchicine, by the noctuid moth Polytela gloriosae (Fab.). Chemoecology 29, 135–142 (2019). https://doi.org/10.1007/s00049-019-00283-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-019-00283-3

Keywords

Search

Navigation