Skip to main content
SpringerLink
Log in

Effects of ABA on primary terpenoids and Δ9-tetrahydrocannabinol in Cannabis sativa L. at flowering stage

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

This work examined the effects of exogenously applied abscisic acid (ABA) on the content of chlorophyll, carotenoids, α-tocopherol, squalene, phytosterols, Δ9-tetrahydrocannabinol (THC) concentration, 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) and 1-deoxy-d-xylulose 5-phosphate synthase (DXS) activity in Cannabis sativa L. at flowering stage. Treatment with 1 and 10 mg l−1 ABA significantly decreased the contents of chlorophyll, carotenoids, squalene, stigmasterol, sitosterol, and HMGR activity in female cannabis plants. ABA caused an increase in α-tocopherol content and DXS activity in leaves and THC concentration in leaves and flowers of female plants. Chlorophyll content decreased with 10 mg l−1 ABA in male plants. Treatment with 1 and 10 mg l−1 ABA showed a decrease in HMGR activity, squalene, stigmasterol, and sitosterol contents in leaves but an increase in THC content of leaves and flowers in male plants. The results suggest that ABA can induce biosynthesis of 2-methyl-d-erythritol-4-phosphate (MEP) pathway secondary metabolites accumulation (α-tocopherol and THC) and down regulated biosynthesis of terpenoid primary metabolites from MEP and mevalonate (MVA) pathways (chlorophyll, carotenoids, and phytosterols) in Cannabis sativa.

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
Fig. 6

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

THC:

Δ9-Tetrahydrocannabinol

CBD:

Cannabidiol

HMGR:

3-Hydroxy-3-methylglutaryl coenzyme A reductase

DXS:

1-Deoxy-d-xylulose 5-phosphate synthase

MEP:

2-Methyl-d-erythritol-4-phosphate

MVA:

Mevalonate

References

  • Agarwal S, Sairam RK, Srivastava GC, Meena RC (2005) Changes in antioxidant enzymes activity and oxidative stress by abscisic acid and salicylic acid in wheat genotypes. Biol Plant 49(4):541–550. doi:10.1007/s10535-005-0048-z

    Article  CAS  Google Scholar 

  • Ahmed S, Nawata E, Sakuratani T (2006) Changes of endogenous ABA and ACC, and their correlations to photosynthesis and water relations in mungbean (Vigna radiata L. Wilczak cv. KPS1) during waterlogging. Environ Exp Bot 57:278–284. doi:10.1016/j.envexpbot.2005.06.006

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Chem 72:248–254

    CAS  Google Scholar 

  • Chappell J, Wolf’ F, Proulx J, Cuellar R, Saunders C (1995) Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase a rate-limiting step for isoprenoid biosynthesis in plans? Plant Physiol 109:1337–1343

    PubMed  CAS  Google Scholar 

  • Cowan AK, Moore-Cordon CS, Bertling L, Wolstenholme BN (1997) Metabolic control of avocado fruit growth: isoprenoid growth regulators and the reaction catalyzed by 3-hydroxy-3-methylglutaryl catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Physiol 114:511–518

    PubMed  CAS  Google Scholar 

  • Cuello J, Quiles MJ, Rosauro J, Sabate B (1995) Effects of growth regulators and light on chloroplasts NAD(P)H dehydrogenase activities of senescent barley leaves. Plant Growth Regul 17:225–232. doi:10.1007/BF00024730

    Article  CAS  Google Scholar 

  • Devarenne TP, Ghosh A, Chappell J (2002) Regulation of squalene synthase, a key enzyme of sterol biosynthesis, in tobacco. Plant Physiol 129:1095–1106. doi:10.1104/pp.001438

    Article  PubMed  CAS  Google Scholar 

  • Dewick PM (2002) The biosynthesis of C5–C25 terpenoid compounds. Nat Prod Rep 19:181–222. doi:10.1039/b002685i

    Article  PubMed  CAS  Google Scholar 

  • Estévez JM, Cantero A, Reindl A, Reichler S, León P (2001) 1-Deoxy-d-xylulose 5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276:22901–22909. doi:10.1074/jbc.M100854200

    Article  PubMed  Google Scholar 

  • Fellermeier M, Eisenreich W, Bacher A, Zenk MH (2001) Biosynthesis of cannabinoids: incorporation experiments with 13C-labeled glucoses. Eur J Biochem 268:1596–1604. doi:10.1046/j.1432-1327.2001.02030.x

    Article  PubMed  CAS  Google Scholar 

  • Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343:425–430. doi:10.1038/343425a0

    Article  PubMed  CAS  Google Scholar 

  • Gondet I, Weber T, Maillot-Vernier P, Benveniste P, Bach TJ (1992) Regulatory role of microsomal 3-hydroxy-3-methylglutaryl coenzyme A reductase in a tobacco mutant that overproduces sterols. Biochem Biophys Res Commun 186:888–893. doi:10.1016/0006-291X(92)90829-A

    Article  PubMed  CAS  Google Scholar 

  • Guzman M (2003) Cannabinoids: potential anticancer agents. Natl Rev 3:745–755

    CAS  Google Scholar 

  • Herbinger K, Tausz M, Wonisch A, Soja G, Sorger A, Grill D (2002) Complex interactive effects of drought and ozone stress on the antioxidant defence systems of two wheat cultivars. Plant Physiol Biochem 40:691–696. doi:10.1016/S0981-9428(02)01410-9

    Article  CAS  Google Scholar 

  • Hilling KW (2004) A chemotaxonomic analysis of terpenoid variation in cannabis. Biochem Syst Ecol 32:875–891. doi:10.1016/j.bse.2004.04.004

    Article  CAS  Google Scholar 

  • Howlett AC, Breivogel CS, Childers SR, Deadwyler SA, Hampson RE, Porrino LY (2004) Cannabinoid physiology and pharmacology: 30 years of progress. Neuropharmacol 47:345–358. doi:10.1016/j.neuropharm.2004.07.030

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of Abscisic acid on active oxygen species, antioxidative defence system, and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42(11):1265–1273. doi:10.1093/pcp/pce162

    Article  PubMed  CAS  Google Scholar 

  • Kang SM, Min JY, Kim YD, Park DJ, Jung HN, Karigar C et al (2006) Effect of supplementing terpenoid biosynthetic precursors on the accumulation of bilobalide and ginkgolides in Ginkgo biloba cell cultures. J Biotechnol 123:85–92

    Article  PubMed  CAS  Google Scholar 

  • Kefu Z, Munns R, King RW (1991) Abscisic acid levels in NaCl treated barley, cotton, and saltbush. Aust J Plant Physiol 18:17–24

    Article  CAS  Google Scholar 

  • Keleo Y, Ünyayar S (2004) Responses of antioxidant defense system of Helianthus annuus to abscisic acid treatment under drought and water logging. Acta Physiol Plant 26(2):149–156. doi:10.1007/s11738-004-0004-0

    Article  Google Scholar 

  • Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB et al (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Plant Biol 100:6866–6871

    CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and caretenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. doi:10.1016/0076-6879(87)48036-1

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1999) The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47–65. doi:10.1146/annurev.arplant.50.1.47

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK, Schwender J, Disch A, Rohmer M (2002) Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. Planta 216:271–274

    Google Scholar 

  • Massei G, Watkins R, Hartley SE (2006) Sex-related growth and secondary compounds in Juniperus oxycedrus macrocarpa. Acta Oecologica 29:135–140

    Article  Google Scholar 

  • Mitchell DI, Cowan AK (2003) Mevastatin-induced inhibition of cell growth in avocado suspension cultures and reversal by isoprenoid compounds. Afr J Biotechnol 2(9):264–270

    CAS  Google Scholar 

  • Moore KB, Oishi KK (1993) Characterization of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity during maize seed development, germination, and seedling emergence. Plant Physiol 101:485–491

    PubMed  CAS  Google Scholar 

  • Moore KB, Oishi KK (1994) 3-Hydroxy-3-methylglutaryl coenzyme A reductase activity in the endosperm of maize vivipary Mutants. Plant Physiol 105:119–125

    PubMed  CAS  Google Scholar 

  • Munné-Bosch S, Falara V, Pateraki I, López-Carbonell M, Jana CJ, Kanellis AK (2009) Physiological and molecular responses of the isoprenoid biosynthetic pathway in a drought-resistant Mediterranean shrub, Cistus creticus exposed to water deficit. J Plant Physiol 166:136–145. doi:10.1016/j.jplph.2008.02.011

    Article  PubMed  CAS  Google Scholar 

  • Munne-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162(7):743–748. doi:10.1016/j.jplph.2005.04.022

    Article  PubMed  CAS  Google Scholar 

  • Munne-Bosch S, Alegre L (2000) Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta 210:925–931. doi:10.1007/s004250050699

    Article  PubMed  CAS  Google Scholar 

  • Panfili G, Fratianni A, Irano M (2003) Normal phase high-performance liquid method for the determination of tocopherols and tocotrienols in cereals. J Agric Food Chem 51:3940–3944. doi:10.1021/jf030009v

    Article  PubMed  CAS  Google Scholar 

  • Querol J, Besumbes O, Lois LM, Boronat A, Imperial S (2001) A fluorometric assay for the determination of 1-deoxy-d-xylulose 5-phosphate synthase activity. Anal Biochem 296:101–105. doi:10.1006/abio.2001.5234

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Concepcion M (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoids biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol 130:1079–1089. doi:10.1104/pp.007138

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Concepcion M (2006) Early steps in isoprenoid biosynthesis: multilevel regulation of the supply of common precursors in plant cells. Phytochem Rev 5:1–15. doi:10.1007/s11101-005-3130-4

    Article  CAS  Google Scholar 

  • Samet JS, Thomas R, Sinclair TR (1980) Leaf senescence and abscisic acid in leaves of field-grown soybean. Plant Physiol 66:1164–1168. doi:10.1104/pp.66.6.1164

    Article  PubMed  CAS  Google Scholar 

  • Simontacchi M, Caro A, Fraga CG, Puntarulo S (1993) Oxidative stress affects α-tocopherol content in soybean embryonic axes upon imbibition and following germination. Plant Physiol 103:949–953

    PubMed  CAS  Google Scholar 

  • Sirikantaramas S, Morimoto S, Shoyama Y, Ishikawa Y, Yoshiko Y, Shoyama Y et al (2004) The gene controlling marijuana psychoactivity molecular cloning and heterologous expression of tetrahydrocannabinolic acid synthase frome Cannabis sativa L. J Biol Chem 279:39767–39774. doi:10.1074/jbc.M403693200

    Article  PubMed  CAS  Google Scholar 

  • Toroser D, Huber SC (1998) 3-Hydroxy-3-methylglutaryl-coenzyme A reductase kinase and sucrose–phosphate synthase kinase activities in cauliflower florets: Ca2+ dependence and substrate specificities. Arch Biochem Biophys 355:291–300. doi:10.1006/abbi.1998.0740

    Article  PubMed  CAS  Google Scholar 

  • Tsai FY, Chi C, HueiKao C (1997) A comparative study of the effects of abscisic acid and methyl jasmonate on seedling growth of rice. Plant Growth Regul 21:37–42. doi:10.1023/A:1005761804191

    Article  CAS  Google Scholar 

  • Xie Z, Jiang D, Dai T, Jing Q, Cao W (2004) Effects of exogenous ABA and cytokinin on leaf photosynthesis and grain protein accumulation in wheat ears cultured in vitro. Plant Growth Regul 44:25–32. doi:10.1007/s10725-004-1880-4

    Article  CAS  Google Scholar 

  • Zhou B, Guo Z, Liu Z (2005) Effects of abscisic acid on antioxidant systems of Stylosanthes guianensis (Aublet) Sw. under chilling stress. Crop Sci 45:599–605

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to express our sincere gratitude to Dr. Anna Kulma for her outstanding contributions and her help with UPLC analysis.

Author information

Authors and Affiliations

  1. Department of Biology, Bahonar University, Kerman, Iran

    Hakimeh Mansouri & Zahra Asrar

  2. International Center for Science, High Technology, and Environmental Science (ICST), Kerman, Iran

    Hakimeh Mansouri

  3. Department of Biotechnology, Wroclaw University, Wroclaw, Poland

    Jan Szopa

Authors
  1. Hakimeh Mansouri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zahra Asrar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jan Szopa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hakimeh Mansouri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mansouri, H., Asrar, Z. & Szopa, J. Effects of ABA on primary terpenoids and Δ9-tetrahydrocannabinol in Cannabis sativa L. at flowering stage. Plant Growth Regul 58, 269–277 (2009). https://doi.org/10.1007/s10725-009-9375-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-009-9375-y

Keywords

Search

Navigation