Plant Cell Reports

, Volume 29, Issue 6, pp 629–641 | Cite as

Stress and developmental responses of terpenoid biosynthetic genes in Cistus creticus subsp. creticus

Original Paper

Abstract

Plants, and specially species adapted in non-friendly environments, produce secondary metabolites that help them to cope with biotic or abiotic stresses. These metabolites could be of great pharmaceutical interest because several of those show cytotoxic, antibacterial or antioxidant activities. Leaves’ trichomes of Cistus creticus ssp. creticus, a Mediterranean xerophytic shrub, excrete a resin rich in several labdane-type diterpenes with verified in vitro and in vivo cytotoxic and cytostatic activity against human cancer cell lines. Bearing in mind the properties and possible future exploitation of these natural products, it seemed interesting to study their biosynthesis and its regulation, initially at the molecular level. For this purpose, genes encoding enzymes participating in the early steps of the terpenoids biosynthetic pathways were isolated and their gene expression patterns were investigated in different organs and in response to various stresses and defence signals. The genes studied were the CcHMGR from the mevalonate pathway, CcDXS and CcDXR from the methylerythritol 4-phosphate pathway and the two geranylgeranyl diphosphate synthases (CcGGDPS1 and 2) previously characterized from this species. The present work indicates that the leaf trichomes are very active biosynthetically as far as it concerns terpenoids biosynthesis, and the terpenoid production from this tissue seems to be transcriptionally regulated. Moreover, the CcHMGR and CcDXS genes (the rate-limiting steps of the isoprenoids’ pathways) showed an increase during mechanical wounding and application of defence signals (like meJA and SA), which is possible to reflect an increased need of the plant tissues for the corresponding metabolites.

Keywords

Cistus creticus subsp. creticus Secondary metabolism Terpenoid biosynthesis Hydroxymethylglutaryl coenzyme A reductase (HMGR) 1-deoxy-d-xylulose-5-phosphate (DXP) synthase (DXS) DXP reductoisomerase (DXR) Geranylgeranyl diphosphate synthase (GGDPS) Gene expression 

Notes

Acknowledgments

This research was partially supported from a grant (PENED 99ΕΔ 637) implemented within the framework of the “Reinforcement Programme of Human Research Manpower” and co-financed by National and Community Funds (25% from the Greek Ministry of Development-General Secretariat of Research and Technology and 75% from E.U.-European Social Fund).

References

  1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42Google Scholar
  2. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel W-J, Verstappen FWA, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884CrossRefPubMedGoogle Scholar
  3. Ament K, Van Schie CC, Bouwmeester HJ, Haring MA, Schuurink RC (2006) Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of -4, 8, 12-trimethyltrideca-1, 3, 7, 11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways. Planta 224:1197–1208CrossRefPubMedGoogle Scholar
  4. Arimura G-i, Ozawa R, Kugimiya S, Takabayashi J, Bohlmann J (2004) Herbivore-induced defense response in a model legume. Two-spotted spider mites induce emission of (E)-b-ocimene and transcript accumulation of (E)-b-ocimene synthase in Lotus japonicus. Plant Physiol 135:1976–1983CrossRefPubMedGoogle Scholar
  5. Aronne G, De Micco V (2001) Seasonal dimorphism in the Mediterranean Cistus incanus L. subsp. incanus. Ann Bot 87:789–794CrossRefGoogle Scholar
  6. Campos N, Boronat A (1995) Targeting and topology in the membrane of plant 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Cell 7:2163–2174CrossRefPubMedGoogle Scholar
  7. Carretero-Paulet L, Ahumada I, Cunillera N, Rodriguez-Concepcion M, Ferrer A, Boronat A, Campos N (2002) Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-D-xylulose 5-phosphate reductoisomerase, the first committed enzyme of the 2-C-methyl-D-erythritol 4-phosphate pathway. Plant Physiol 129:1581–1591CrossRefPubMedGoogle Scholar
  8. 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 plants? Plant Physiol 109:1337–1343PubMedGoogle Scholar
  9. Chen F, Tholl D, D’Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:1–14CrossRefGoogle Scholar
  10. Dimas K, Papadaki A, Tsimplouli C, Hatziantoniou S, Alevizopoulos K, Pantazis P, Demetzos C (2006) Labd-14-ene-8, 13-diol (sclareol) induces cell cycle arrest and apoptosis in human breast cancer cells and enhances the activity of anticancer drugs. Biomed Pharmacother 60:127–133CrossRefPubMedGoogle Scholar
  11. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016CrossRefPubMedGoogle Scholar
  12. Enfissi EMA, Fraser PD, Lois L-M, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol J 3:17–27CrossRefPubMedGoogle Scholar
  13. Falara V, Fotopoulos V, Margaritis T, Anastasaki T, Pateraki I, Bosabalidis M, Artemios D, Kafetzopoulos D, Demetzos C, Pichersky E, Kanellis A (2008) Transcriptome analysis approaches for the isolation of trichome-specific genes from the medicinal plant Cistus creticus subsp. creticus. Plant Mol Biol 68:633–651CrossRefPubMedGoogle Scholar
  14. Gershenzon J, McCaskill D, Rajaonarivony JIM, Mihaliak C, Karp F, Croteau R (1992) Isolation of secretory cells from plant glandular trichomes and their use in biosynthetic studies of monoterpenes and other gland products. Anal Biochem 200:130–138CrossRefPubMedGoogle Scholar
  15. Gulz PG, Herrmann T, Hangst K (1996) Leaf trichomes in the genus Cistus. Flora 191:82–104Google Scholar
  16. Harker M, Holmberg N, Clayton JC, Gibbard CL, Wallace AD, Rawlins S, Hellyer SA, Lanot A, Safford R (2003) Enhancement of seed phytosterol levels by expression of an N-terminal truncated Hevea brasiliensis (rubber tree) 3-hydroxy-3-methylglutaryl-CoA reductase. Plant Biotechnol J 1:113–121CrossRefPubMedGoogle Scholar
  17. Hatziantoniou S, Dimas K, Georgopoulos A, Sotiriadou N, Demetzos C (2006) Cytotoxic and antitumor activity of liposome-incorporated sclareol against cancer cell lines and human colon cancer xenografts. Pharmacol Res 53:80–87CrossRefPubMedGoogle Scholar
  18. Heidel AJ, Baldwin IT (2004) Microarray analysis of salicylic acid and jasmonic acid signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ 27:1362–1373CrossRefGoogle Scholar
  19. Korth KL, Stermer BA, Bhattacharyya MK, Dixon RA (1997) HMG-CoA reductase gene families that differentially accumulate transcripts in potato tubers are developmentally expressed in floral tissues. Plant Mol Biol 33:545–551CrossRefPubMedGoogle Scholar
  20. Krushkal J, Pistilli M, Ferrell KM, Souret FF, Weathers PJ (2003) Computational analysis of the evolution of the structure and function of 1-deoxy–xylulose-5-phosphate synthase, a key regulator of the mevalonate-independent pathway in plants. Gene 313:127–138CrossRefPubMedGoogle Scholar
  21. Lange BM, Croteau R (1999) Isoprenoid biosynthesis via a mevalonate-independent pathway in plants: cloning and heterologous expression of 1-deoxy–xylulose-5-phosphate reductoisomerase from peppermint. Arch Biochem Biophys 365:170–174CrossRefPubMedGoogle Scholar
  22. Li L, Li C, Howe GA (2001) Genetic analysis of wound signaling in tomato. Evidence for a dual role of jasmonic acid in defense and female fertility. Plant Physiol 127:1414–1417CrossRefPubMedGoogle Scholar
  23. Lois LM, Rodriguez-Concepcion M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J 22:503–513CrossRefPubMedGoogle Scholar
  24. Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787CrossRefPubMedGoogle Scholar
  25. Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of norway spruce stems. Plant Physiol 129:1003–1018CrossRefPubMedGoogle Scholar
  26. Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol 132:1586–1599CrossRefPubMedGoogle Scholar
  27. Matsingou C, Dimas K, Demetzos C (2006) Design and development of liposomes incorporating a bioactive labdane-type diterpene. In vitro growth inhibiting and cytotoxic activity against human cancer cell lines. Biomed Pharmacother 60:191–199CrossRefPubMedGoogle Scholar
  28. McConkey ME, Gershenzon J, Croteau R (2000) Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint. Plant Physiol 122:215–224CrossRefPubMedGoogle Scholar
  29. McKay S, Godard K-A, Toudefallah M, Martin DM, Alfaro R, King J, Bohlmann J, Plant AL (2006) Wound-induced terpene synthase gene expression in Sitka spruce that exhibit resistance or susceptibility to attack by the white pine weevil. Plant Physiol 140:1009–1021CrossRefGoogle Scholar
  30. Munne-Bosch S, Alegre L (2003) Drought-induced changes in the redox state of α-tocopherol, ascorbate, and the diterpene carnosic acid in chloroplasts of Labiatae species differing in carnosic acid content. Plant Physiol 131:1816–1825CrossRefPubMedGoogle Scholar
  31. Munné-Bosch S, Falara V, Pateraki I, López-Carbonell M, Cela J, Kanellis AK (2008) Physiological and molecular responses of the isoprenoid biosynthetic pathway in a drought-resistant Mediterranean shrub, Cistus creticus exposed to water deficit. J Plant Physiol 166:136–145CrossRefPubMedGoogle Scholar
  32. Munoz-Bertomeu J, Arrillaga I, Ros R, Segura J (2006) Up-regulation of 1-deoxy-d-xylulose-5-phosphate synthase enhances production of essential oils in transgenic spike lavender. Plant Physiol 142:890–900CrossRefPubMedGoogle Scholar
  33. Okada K, Saito T, Nakagawa T, Kawamukai M, Kamiya Y (2000) Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol 122:1045–1056CrossRefPubMedGoogle Scholar
  34. Oudin A, Mahroug S, Courdavault V, Hervouet N, Zelwer C, Rodríguez-Concepción M, St-Pierre B, Burlat V (2007) Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus. Plant Mol Biol 65:13–30CrossRefPubMedGoogle Scholar
  35. Pateraki I, Kanellis AK (2008) Isolation and functional analysis of two Cistus creticus cDNAs encoding geranylgeranyl diphosphate synthase. Phytochemistry (in press)Google Scholar
  36. Penuelas J, Llusia J, Asensio D, Munne-Bosch S (2005) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ 28:278–286CrossRefGoogle Scholar
  37. Pichersky E, Gang DR (2000) Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends Plant Sci 5:439–445CrossRefPubMedGoogle Scholar
  38. Pieterse CMJ, Koornneef A, Leon Reyes A, Ritsema T, Verhage A, Joosten R, De Vos M, Van Oosten V, Dicke M (2007) Cross-talk between signaling pathways leading to defense against pathogens and insects. In: Lorito M, Woo SL, Scala F (eds) Biology of plant-microbe interactions. The American Phytopathological Society, APS Press, TXGoogle Scholar
  39. Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The Effect of α-Amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134:1598–1613CrossRefPubMedGoogle Scholar
  40. Rodriguez-Concepcion M, Boronat A (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol 130:1079–1089CrossRefPubMedGoogle Scholar
  41. Ryan CA, Moura DS (2002) Systemic wound signaling in plants: a new perception. Proc Natl Acad Sci USA 99:6519–6520CrossRefPubMedGoogle Scholar
  42. Schnee C, Kollner TG, Gershenzon J, Degenhardt J (2002) The Maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-beta -Farnesene, (E)-Nerolidol, and (E, E)-Farnesol after herbivore damage. Plant Physiol 130:2049–2060CrossRefPubMedGoogle Scholar
  43. Schwartz SH, Qin X, Zeevaart JAD (2003) Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol 131:1591–1601CrossRefPubMedGoogle Scholar
  44. Smith JL, Moraes CMD, Mescher MC (2009) Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manag Sci 65:497–503CrossRefPubMedGoogle Scholar
  45. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux J-P, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770CrossRefPubMedGoogle Scholar
  46. Steele CL, Katoh S, Bohlmann J, Croteau R (1998) Regulation of oleoresinosis in grand fir (Abies grandis): differential transcriptional control of monoterpene, sesquiterpene, and diterpene synthase genes in response to wounding. Plant Physiol 116:1497–1504CrossRefPubMedGoogle Scholar
  47. Takaya A, Zhang YW, Asawatreratanakul K, Wititsuwannakul D, Wititsuwannakul R, Takahashi S, Koyama T (2003) Cloning, expression and characterization of a functional cDNA clone encoding geranylgeranyl diphosphate synthase of Hevea brasiliensis. Biochim Biophys Acta 1625:214–220PubMedGoogle Scholar
  48. Yang Z, Park H, Lacy GH, Cramer CL (1991) Differential activation of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes by wounding and pathogen challenge. Plant Cell 3:397–405CrossRefPubMedGoogle Scholar
  49. Yerger EH, Grazzini RA, Hesk D, Cox-Foster DL, Craig R, Mumma R (1992) A rapid method for isolating glandular trichomes. Plant Physiol 99:1–7CrossRefPubMedGoogle Scholar
  50. Zavala JA, Baldwin IT (2006) Jasmonic acid signalling and herbivore resistance traits constrain regrowth after herbivore attack in Nicotiana attenuata. Plant Cell Environ 29:1751–1760CrossRefPubMedGoogle Scholar
  51. Zhao J, Zheng S-H, Fujita K, Sakai K (2004) Jasmonate and ethylene signalling and their interaction are integral parts of the elicitor signalling pathway leading to b-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J Exp Bot 55:1003–1012CrossRefPubMedGoogle Scholar
  52. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Group of Biotechnology of Pharmaceutical Plants, Laboratory of Pharmacognosy, Department of Pharmaceutical SciencesAristotle University of ThessalonikiThessalonikiGreece
  2. 2.Departament de Bioquímica i Biologia Molecular, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain

Personalised recommendations