Diverse transcription factors control monoterpene synthase expression in lavender (Lavandula)

Abstract

Main conclusion

We cloned eight transcription factors that activate lavender monoterpene synthase promoters.

Abstract

In this study, we employed the Yeast One-Hybrid (Y1H) assay system to identify transcription factors that control promoters for two Lavandula × intermedia monoterpene synthase genes, linalool synthase (LiLINS) and 1,8-cineole synthase (LiCINS). The bait sequences used in the assay were either a 768-bp LiLINS, or a 1087-bp LiCINS promoter. The prey included proteins expressed in L. × intermedia floral tissue. The assay identified 96 sequences encoding proteins that interacted with one or both promoters. To explore the nature of this interaction, the LiLINS and LiCINS promoter fragments were each fused to the E. coli gusA (GUS) reporter gene. The constructs were separately transformed into tobacco (Nicotiana benthamiana) leaves co-expressing individually a subset of ten representative transcription factors (TFs) predicted to control these promoters. Six TFs induced expression from both promoters, two activated LiCINS promoter alone, and two did not induce expression from either promoter. The TFs identified in this study belong to various groups including those containing conserved domains typical of MYB, bZIP, NAC, GeBP and SBP-related proteins.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

References

  1. Adal AM, Sarker LS, Lemke AD, Mahmoud SS (2017) Isolation and functional characterization of a methyl jasmonate-responsive 3-carene synthase from Lavandula × intermedia. Plant Mol Biol. https://doi.org/10.1007/s11103-017-0588-6

    Article  PubMed  Google Scholar 

  2. Adal AM, Sarker LS, Malli RPN, Liang P, Mahmoud SS (2019) RNA-Seq in the discovery of a sparsely expressed scent-determining monoterpene synthase in lavender (Lavandula). Planta 249:271–290. https://doi.org/10.1007/s00425-018-2935-5

    CAS  Article  PubMed  Google Scholar 

  3. Alfieri M, Vaccaro MC, Cappetta E, Ambrosone A, Tommasi D, Leone A (2018) Coactivation of MEP-biosynthetic genes and accumulation of abietane diterpenes in Salvia sclarea by heterologous expression of WRKY and MYC2 transcription factors. Sci Rep 8:1–13. https://doi.org/10.1038/s41598-018-29389-4

    CAS  Article  Google Scholar 

  4. An G (1986) Development of plant promoter expression vectors and their use for analysis of differential activity of nopaline synthase promoter in transformed tobacco cells. Plant Physiol 81:86–91. https://doi.org/10.1104/pp.81.1.86

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Aprotosoaie AC, Hǎncianu M, Costache II, Miron A (2014) Linalool: a review on a key odorant molecule with valuable biological properties. Flavour Fragr J 29:193–219. https://doi.org/10.1002/ffj.3197

    CAS  Article  Google Scholar 

  6. Aprotosoaie AC, Gille E, Trifan A, Luca VS, Miron A (2017) Essential oils of Lavandula genus: a systematic review of their chemistry. Phytochem Rev 16:761–799. https://doi.org/10.1007/s11101-017-9517-1

    CAS  Article  Google Scholar 

  7. Chevalier F, Perazza D, Laporte F, Le Henanff G, Hornitschek P, Bonneville JM, Herzog M, Vachon G (2008) GeBP and GeBP-like proteins are noncanonical leucine-zipper transcription factors that regulate cytokinin response in arabidopsis. Plant Physiol 146:1142–1154. https://doi.org/10.1104/pp.107.110270

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Chuang YC, Hung YC, Tsai WC, Chen WH, Chen HH (2018) PbbHLH4 regulates floral monoterpene biosynthesis in Phalaenopsis orchids. J Exp Bot 69:4363–4377. https://doi.org/10.1093/jxb/ery246

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Demissie ZA, Sarker LS, Mahmoud SS (2011) Cloning and functional characterization of β-phellandrene synthase from Lavandula angustifolia. Planta. https://doi.org/10.1007/s00425-010-1332-5

    Article  PubMed  Google Scholar 

  10. Demissie ZA, Cella MA, Sarker LS, Thompson TJ, Rheault MR, Mahmoud SS (2012) Cloning, functional characterization and genomic organization of 1,8-cineole synthases from Lavandula. Plant Mol Biol 79:393–411. https://doi.org/10.1007/s11103-012-9920-3

    CAS  Article  PubMed  Google Scholar 

  11. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:2901–3907

    Article  Google Scholar 

  12. Ouwerkerk PBF, Meijer AH (2011) Plant reverse genetics. Methods 678:211–227. https://doi.org/10.1007/978-1-60761-682-5

    CAS  Article  Google Scholar 

  13. Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    CAS  Article  Google Scholar 

  14. Romanel EAC, Schrago CG, Couñago RM et al (2009) Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification. PLoS One. https://doi.org/10.1371/journal.pone.0005791

    Article  PubMed  PubMed Central  Google Scholar 

  15. Sarker LS, Mahmoud SS (2015) Cloning and functional characterization of two monoterpene acetyltransferases from glandular trichomes of L. × intermedia. Planta 242:709–719. https://doi.org/10.1007/s00425-015-2325-1

    CAS  Article  PubMed  Google Scholar 

  16. Sarker LS, Galata M, Demissie ZA, Mahmoud SS (2012) Molecular cloning and functional characterization of borneol dehydrogenase from the glandular trichomes of Lavandula × intermedia. Arch Biochem Biophys 528:163–170. https://doi.org/10.1016/j.abb.2012.09.013

    CAS  Article  PubMed  Google Scholar 

  17. Schöb H, Kunz C, Meins F (1997) Silencing of transgenes introduced into leaves by agroinfiltration: a simple, rapid method for investigating sequence requirements for gene silencing. Mol Gen Genet 256:581–585. https://doi.org/10.1007/s004380050604

    Article  PubMed  Google Scholar 

  18. Spyropoulou EA, Haring MA, Schuurink RC (2014) Expression of Terpenoids 1, a glandular trichome-specific transcription factor from tomato that activates the terpene synthase 5 promoter. Plant Mol Biol 84:345–357. https://doi.org/10.1007/s11103-013-0142-0

    CAS  Article  PubMed  Google Scholar 

  19. Xu Y-H, Wang J-W, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-delta-cadinene synthase-A. Plant Physiol 135:507–515. https://doi.org/10.1104/pp.104.038612

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Xu J, Van Herwijnen ZO, Dräger DB, Sui C, Haring MA, Schuurink RC (2018) SlMYC1 regulates type VI glandular trichome formation and terpene biosynthesis in tomato glandular cells. Plant Cell 30:2988–3005. https://doi.org/10.1105/tpc.18.00571

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Yoshida K, Oyama-Okubo N, Yamagishi M (2018) An R2R3-MYB transcription factor ODORANT1 regulates fragrance biosynthesis in lilies (Lilium spp.). Mol Breed. https://doi.org/10.1007/s11032-018-0902-2

    Article  Google Scholar 

  22. Yu ZX, Li JX, Yang CQ, Hu WL, Wang LJ, Chen XY (2012) The jasmonate-responsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Mol Plant. https://doi.org/10.1093/mp/ssr087

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported through grants and/or in-kind contributions to SSM by UBC, and the Natural Sciences and Engineering Research Council of Canada (NSERC).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Soheil S. Mahmoud.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1.

Biosynthesis of linalool and 1,8-cineole in L. × intermedia. IPP: isopentenyl diphosphate, DMAPP: dimethylallyl diphosphate and GPP: geranyl diphosphate (DOCX 47 kb)

Fig. S2.

a) Schematic representation of promoter–GUS fusion constructs used in this study. LiCINS promoter (LiCINSp) and LiLINS promoter (LiLINSp) were cloned upstream of the gusA gene (encoding GUS) within the T-DNA of the pCambia1391z plant transformation vector. LB: left T-DNA border and RB: right T-DNA border. HygR: Hygromycin resistance gene. KanR: Kanamycin resistance gene (Neomycin phosphotransferase II, NPTII). b) Schematic representation of the CaMV353-TF constructs used in this study. In these constructs individual TFs were cloned downstream of a tandem CaMV 35S promoter in pGA482 plant expression vector. KanR: Kanamycin resistance gene (Neomycin phosphotransferase II, NPTII) (DOCX 25 kb)

Table S1

. List of primers used for cloning of promoters and transcription factors from L. × intermedia (DOCX 14 kb)

Table S2

. Spectrophotometric readings (OD595) corresponding to GUS activity in N. benthamiana plants harboring either LiLINSp:GUS or LiCINSp:GUS construct, co-expressing L. × intermedia TFs from the pGA482 vector (See Fig S2b). Results correspond to data reported in Table 1 and Fig. 2 (DOCX 15 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sarker, L.S., Adal, A.M. & Mahmoud, S.S. Diverse transcription factors control monoterpene synthase expression in lavender (Lavandula). Planta 251, 5 (2020). https://doi.org/10.1007/s00425-019-03298-w

Download citation