Advertisement

Planta

pp 1–6 | Cite as

A lavender ABC transporter confers resistance to monoterpene toxicity in yeast

  • Zerihun A. Demissie
  • Mike Tarnowycz
  • Ayelign M. Adal
  • Lukman S. Sarker
  • Soheil S. Mahmoud
Original Article
  • 63 Downloads
Part of the following topical collections:
  1. Terpenes and Isoprenoids

Abstract

Main conclusion

Functional expression of a multidrug resistance-type ABC transporter from Lavandula angustifolia improved yeast resistance to geraniol, a monoterpene constituent of lavender essential oil.

Plant ATP-binding cassette (ABC) transporters are a large family of membrane proteins involved in active and selective transport of structurally diverse compounds. In this study, we functionally evaluated LaABCB1, a multidrug resistance (MDR)-type ABC transporter strongly expressed in the secretory cells of lavender glandular trichomes, where monoterpene essential oil constituents are synthesized and secreted. We used LaABCB1 to complement a yeast knockout mutant in which 16 ABC transporters were deleted. Expression of LaABCB1 enhanced tolerance of yeast mutants to geraniol, a key constituent of essential oils in lavenders and numerous other plants. Our findings suggest a role for the MDR-type ABC transporters in the toxicity tolerance of at least certain essential oil constituents in lavender oil glands.

Keywords

ATP-binding cassette Lavandula Multidrug resistance Monoterpene trafficking Transmembrane protein 

Notes

Acknowledgements

This work was supported through grants or in-kind contributions by the Investment Agriculture Foundation of British Columbia, National Research Council Plant Biotechnology Institute through the NAPGEN program, Genome British Columbia, The University of British Columbia, the Natural Sciences and Engineering Research Council of Canada (RGPIN-2015-04858), and the Canadian Foundation for Innovation to S.S.M. We are also grateful to Dr. Fritz Roth and Harvard University for providing the yeast strains for this study.

Supplementary material

425_2018_3064_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 19 kb)
425_2018_3064_MOESM2_ESM.tif (188 kb)
The transcriptional activity of LaABCB1 and the reference gene (β-actin) in L. angustifolia and L. latifolia leaf and floral tissues, and L. x intermedia leaf, floral and secretory cells of glandular trichomes after 30 cycles of PCR. (TIFF 187 kb) (TIFF 187 kb)

References

  1. Bienert MD, Siegmund SE, Drozak A, Trombik T, Bultreys A, Baldwin IT, Boutry M (2012) A pleiotropic drug resistance transporter in Nicotiana tabacum is involved in defense against the herbivore Manduca sexta. Plant J 72:745–757CrossRefGoogle Scholar
  2. Buda GJ, Barnes WJ, Fich EA, Park S, Yeats TH, Zhao L, Domozych DS, Rose JK (2013) An ATP binding cassette transporter is required for cuticular wax deposition and desiccation tolerance in the Moss Physcomitrella patens. Plant Cell 25:4000–4013CrossRefGoogle Scholar
  3. Crouzet J, Roland J, Peeters E, Trombik T, Ducos E, Nader J, Boutry M (2013) NtPDR1, a plasma membrane ABC transporter from Nicotiana tabacum, is involved in diterpene transport. Plant Mol Biol 82:181–192CrossRefGoogle Scholar
  4. Demissie ZA (2014) Cloning and functional characterization of genes involved in the biosynthesis and secretion of essential oil constituents of Lavandula. Ph.D. Thesis, The University of British ColumbiaGoogle Scholar
  5. Demissie Z, Cella M, Sarker L, Thompson T, Rheault M, Mahmoud S (2012) Cloning, functional characterization and genomic organization of 1,8-cineole synthases from Lavandula. Plant Mol Biol 79:393–411CrossRefGoogle Scholar
  6. Demissie ZA, Erland LA, Rheault MR, Mahmoud SS (2013) The biosynthetic origin of irregular monoterpenes in Lavandula: isolation and biochemical characterization of a novel cis-prenyl diphosphate synthase gene, lavandulyl diphosphate synthase. J Biol Chem 288:6333–6341CrossRefGoogle Scholar
  7. Gietz RD (2014) Yeast transformation by the LiAc/SS carrier DNA/PEG method. Methods Mol Biol 1205:1–12.  https://doi.org/10.1007/978-1-4939-1363-3_1 CrossRefPubMedGoogle Scholar
  8. Gietz RD, Schiestl RH (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2(1):31–34CrossRefGoogle Scholar
  9. Kaneda M, Schuetz M, Lin BS, Chanis C, Hamberger B, Western TL, Ehlting J, Samuels AL (2011) ABC transporters coordinately expressed during lignification of Arabidopsis stems include a set of ABCBs associated with auxin transport. J Exp Bot 62:2063–2077CrossRefGoogle Scholar
  10. Lane A, Boecklemann A, Woronuk GN, Sarker S, Mahmoud SS (2010) A genomics resource for investigating regulation of essential oil production in Lavandula angustifolia. Planta 231:835–845.  https://doi.org/10.1007/s00425-009-1090-4 CrossRefPubMedGoogle Scholar
  11. Lee M, Choi Y, Burla B, Kim YY, Jeon B, Maeshima M, Yoo JY, Martinoia E, Lee Y (2008) The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat Cell Biol 10:1217CrossRefGoogle Scholar
  12. Lefevre F, Boutry M (2018) Towards identification of the substrates of ATP-binding cassette transporters. Plant Physiol 178:18–39PubMedPubMedCentralGoogle Scholar
  13. Lis-Balchin M (2002) Lavender essential oil Standardisation, ISO: adulteration and its detection using GC, enantiomeric columns and bioactivity. In: Lis-Balchin (ed) Lavender; The Genus Lavandula: Medicinal and Aromatic Plants–Industrial Profiles, Taylor & Francis, London, pp 117–123Google Scholar
  14. McCaskill D, Gershenzon J, Croteau R (1992) Morphology and monoterpene biosynthetic capabilities of secretory cell clusters isolated from glandular trichomes of peppermint (Mentha piperita L.). Planta 187(4):445–454CrossRefGoogle Scholar
  15. McConkey ME, Gershenzon J, Croteau RB (2000) Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint. Plant Physiol 122:215–224CrossRefGoogle Scholar
  16. Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375CrossRefGoogle Scholar
  17. Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K (2003) Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proc Natl Acad Sci USA 100:751–756CrossRefGoogle Scholar
  18. Smigielski K, Raj A, Krosowiak K, Gruska R (2009) Chemical composition of the essential oil of Lavandula angustifolia cultivated in Poland. J Essent Bear Plants 12(3):338–347CrossRefGoogle Scholar
  19. Suzuki Y, Onge RPS, Mani R, King OD, Heilbut A, Labunskyy VM, Chen W, Pham L, Zhang LV, Tong AHY, Nislow C, Giaever G, Gladyshev VN, Vidal M, Schow P, Lehár J, Roth FP (2011) Knocking out multi-gene redundancies via cycles of sexual assortment and fluorescence selection. Nat Methods 8(2):159–164CrossRefGoogle Scholar
  20. Turner GW, Croteau R (2004) Organization of monoterpene biosynthesis in Mentha. Immunocytochemical localizations of geranyl diphosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Plant Physiol 136(4):4215–4227CrossRefGoogle Scholar
  21. Ushigome F, Koyabu N, Satoh S, Tsukimori K, Nakano H, Nakamura T, Uchiumi T, Kuwano M, Ohtani H, Sawada Y (2003) Kinetic analysis of P-glycoprotein-mediated transport by using normal human placental brush-border membrane vesicles. Pharm Res 20:38–44CrossRefGoogle Scholar
  22. Wang Y, Lim L, DiGuistini S, Robertson G, Bohlmann J, Breuil C (2013) A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytol 197:886–898CrossRefGoogle Scholar
  23. Yoshida N, Takagi A, Kitazawa H, Kawakami J, Adachi I (2005) Inhibition of P-glycoprotein-mediated transport by extracts of and monoterpenoids contained in Zanthoxyli fructus. Toxicol Appl Pharmacol 209:167–173CrossRefGoogle Scholar
  24. Yoshida N, Koizumi M, Adachi I, Kawakami J (2006) Inhibition of P-glycoprotein-mediated transport by terpenoids contained in herbal medicines and natural products. Food Chem Toxicol 44:2033–2039CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Zerihun A. Demissie
    • 1
    • 2
  • Mike Tarnowycz
    • 1
  • Ayelign M. Adal
    • 1
  • Lukman S. Sarker
    • 1
  • Soheil S. Mahmoud
    • 1
  1. 1.Department of BiologyUniversity of British ColumbiaKelownaCanada
  2. 2.National Research Council of CanadaOttawaCanada

Personalised recommendations