Identification and characterization of a second isogene encoding γ-terpinene synthase in Thymus caespititius

Journal of Plant Physiology

Volumn 171, Issue 12, 2014, Pages 1017-1027

  Mendes, Marta D ^a   Barroso, José G ^a   Oliveira, M Margarida ^b   Trindade, Helena ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Chemotypes; In vitro culture; Lamiaceae; Monoterpene; Terpene synthases

Indexed keywords

ESSENTIAL OIL; GAMMA-TERPINENE; MESSENGER RNA; TERPENE; TERPENE SYNTHASE; TRANSFERASE;

AMINO ACID SEQUENCE; CHEMISTRY; ENZYMOLOGY; GAS CHROMATOGRAPHY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLANT; PLANT GENE; SEQUENCE ALIGNMENT; THYMUS (PLANT);

ALKYL AND ARYL TRANSFERASES; AMINO ACID SEQUENCE; CHROMATOGRAPHY, GAS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MOLECULAR SEQUENCE DATA; MONOTERPENES; OILS, VOLATILE; PHYLOGENY; PLANT SHOOTS; RNA, MESSENGER; SEQUENCE ALIGNMENT; THYMUS PLANT; TRANSCRIPTION, GENETIC;

EID: 84901981667     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2014.04.001     Document Type: Article

References (59)

1. Barbosa P., Lima A.S., Vieira P., Tinoco M.T., Barroso J.G., Pedro L.G., et al. Nematicidal activity of essential oils and volatiles derived from Portuguese aromatic flora against the pinewood nematode, Bursaphelenchus xylophilus. J Nematol 2010, 42(1):8-16.
2. Bohlmann J., Meyer-Gauen G., Croteau R. Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 1998, 95:4126-4133.
3. Byun-Mckay S.A., Geeta R. Protein subcellular relocalization: a new perspective on the origin of novel genes. Trends Ecol Evol 2007, 22:338-344.
4. Chen F., Ro D.K., Petri J., Gershenzon J., Bohlmann J., Pichersky E., et al. Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiol 2004, 135:1956-1966.
5. Cheng A.X., Lou Y.G., Mao Y.B., Lu S., Wang L.J., Chen X.Y. Plant terpenoids: biosynthesis and ecological functions. J Integr Plant Biol 2007, 49:179-186.
6. Clegg M.T., Cummings M.P., Durbin M.L. The evolution of plant nuclear genes. Proc Natl Acad Sci USA 1997, 94:7791-7798.
7. Colby S.M., Alonso W.R., Katahira E.J., McGravey D.J., Croteau R. 4S-Limonene synthase from the oil glands of spearmint (Mentha spicata): cDNA isolation, characterization, and bacterial expression of the catalytically active monoterpene cyclase. J Biol Chem 1993, 268(3):23016-23024.
8. Crocoll C., Asbach J., Novak J., Gershenzon J., Degenhardt J. Terpene synthases of oregano (Origanum vulgare L.) and their roles in the pathway and regulation of terpene biosynthesis. Plant Mol Biol 2010, 73:587-593.
9. Crocoll C. Biosynthesis of the phenolic monoterpenes, thymol and carvacrol, by terpene synthases and cytochrome P450s in oregano and thyme 2011, Dissertation, Biologisch-Pharmazeutischen Fakultät der Friedrich-Schiller-Universität Jena, Germany.
10. Dandlen S.A., Lima A.S., Mendes M.D., Miguel M.G., Faleiro M.L., Sousa M.J., et al. Antimicrobial activity, cytotoxicity and intracellular growth inhibition of Portuguese Thymus essential oils. Braz J Pharmacogn 2011, 21(6):1012-1024.
11. Daviet L., Schalk M. Biotechnology in plant essential oil production: progress and perspectives in metabolic engineering of the terpene pathway. Flavour Fragr J 2010, 25(3):123-127.
12. Davis E.M., Croteau R. Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. Top Curr Chem 2000, 209:53-95.
13. Degenhardt J., Köllner T.G., Gershenzon J. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 2009, 70:1621-1637.
14. Demissie Z.A., Sarker L.S., Mahmoud S.S. Cloning and functional characterization of β-phellandrene synthase from Lavandula angustifolia. Planta 2011, 233:685-696.
15. Dewick P.M. Medicinal natural products - a biosynthetic approach 2002, John Wiley & Sons, Ltd, Chichester. 2nd ed.
16. Drummond A.J., Ashton B., Buxton S., Cheung M., Cooper A., Heled J., Kearse M., Moir R., Stones-Havas S., Sturrock S., Thierer T., Wilson A. Geneious v5.3 2010, Available from:. http://www.geneious.com/.
17. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000, 300:1005-1016.
18. Figueiredo A.C., Barroso J.G., Pedro L.G., Salgueiro L., Miguel M.G., Faleiro M.L. Portuguese Thymbra and Thymus species volatiles: chemical composition and biological activities. Curr Pharm Des 2008, 14:3120-3140.
19. Figueiredo A.C., Barroso J.G., Pedro L.G., Scheffer J.C. Factors affecting secondary metabolite production in plants: volatile components and essential oils. Flavour Fragr J 2008, 23:213-226.
20. Fischer M.J.C., Meyer S., Claudel P., Perrin M., Ginglinger J.F., Gertz C., et al. Specificity of Ocimum basilicum geraniol synthase modified by its expression in different heterologous systems. J Biotechnol 2013, 163:24-29.
21. Fryxell K.J. The coevolution of gene family trees. Trends Genet 1996, 12:356-369.
22. Gang D.R., Wang J., Dudareva N., Nam K.H., Simon J.E., Lewinsohn E., et al. An investigation of the storage and biosynthesis of phenylpropenes in sweet basil. Plant Physiol 2001, 125:539-555.
23. Gershenzon J., Maffei M., Croteau R. Biochemical and histochemical-localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata). Plant Physiol 1989, 89:1351-1357.
24. Haudenschild C., Schalk M., Karp F., Croteau R. Functional expression of regiospecific cytochrome P450 limonene hydroxylases from mint (Mentha spp.) in Escherichia coli and Saccharomyces cerevisiae. Arch Biochem Biophys 2000, 379:127-136.
25. Iijima Y., Davidovich-Rikanati R., Fridman E., Gang D.R., Bar E., Lewinsohn E., et al. The biochemical and molecular basis for the divergent patterns in the biossynthesis of terpenes and phenylpropenes in the peltade glands of three cultivars of basil. Plant Physiol 2004, 136:3724-3736.
26. Iijima Y., Gang D.R., Fridman E., Lewinsohn E., Pichersky E. Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiol 2004, 134:370-379.
27. Ito M., Honda G. Geraniol synthases from perilla and their taxonomical significance. Phytochemistry 2007, 68:446-453.
28. Johnson C.B., Kazantzis A., Skoula M., Mitteregger U., Novak J. Seasonal, populational and ontogenic variation in the volatile oil content and composition of individuals of Origanum vulgare subsp. hirtum, assessed by GC headspace analysis and by SPME sampling of individual oil glands. Phytochem Anal 2004, 15:286-292.
29. Kampranis S.C., Ioannidis D., Purvis A., Mahrez W., Ninga E., Katerelos N.A., et al. Rational conversion of substrate and product specificity in a Salvia monoterpene synthase: structural insights into the evolution of terpene synthase function. Plant Cell 2007, 19:1994-1995.
30. Keeling C.I., Bohlmann J. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 2006, 170:657-675.
31. Krause S.T., Köllner T.G., Asbach J., Degenhardt J. Stereochemical mechanism of two sabinene hydrate synthases forming antipodal monoterpenes in thyme (Thymus vulgaris). Arch Biochem Biophys 2013, 529:112-121.
32. Landmann C., Fink B., Festner M., Dregus M., Engel K.H., Schwab W. Cloning and functional characterization of three terpene synthases from lavender (Lavandula angustifolia). Arch Biochem Biophys 2007, 465:417-429.
33. Lane A., Boecklemann A., Woronuk G.N., Sarker L., Mahmoud S.S. A genomic resource for investigating regulation of essential oil production in Lavandula angustifolia. Planta 2010, 231:835-845.
34. Lima A.S., Schimmel J., Lukas B., Novak J., Barroso J.G., Figueiredo A.C., et al. Genomic characterization, molecular cloning and expression analysis of two terpene synthases from Thymus caespititius. Planta 2013, 238:191-204.
35. Lukas B., Samuel R., Novak J. Oregano or marjoram? The enzyme γ-terpinene synthase affects chemotype formation in the genus Origanum. Isr J Plant Sci 2010, 58:211-220.
36. Lupien S., Karp F., Wildung M., Croteau R. Regiospecific cytochrome P450 limonene hydroxylases from mint (Mentha) species: cDNA isolation, characterization, and functional expression of (-)-4S-limonene-3-hydroxylase and (-)-4S-limonene-6-hydroxylase. Arch Biochem Biophys 1999, 368:181-192.
37. Mendes M.D., Figueiredo A.C., Oliveira M.M., Trindade H. Essential oil production in shoot cultures versus field-grown plants of Thymus caespititius. Plant Cell Tissue Organ Cult 2013, 113:341-351.
38. Mendes M.D., Trindade H., Figueiredo A.C., Pedro L.G., Barroso J.G. Trichomes morphology and essential oils composition in micropropagated versus field grown Thymus caespititius plants. Acta Hort 2010, 860:215-218.
39. Miguel G., Simões M., Figueiredo A.C., Barroso J.G., Pedro L.G., Carvalho L. Composition and antioxidant activities of the essential oils of Thymus caespititius, Thymus camphoratus and Thymus mastichina. Food Chem 2004, 86:183-188.
40. Miguel M.G., Figueiredo A.C., Costa M.M., Martins D., Duarte J., Barroso J.G., et al. Effect of the volatile constituents isolated from Thymus albicans, Th. mastichina, Th. carnosus and Thymbra capitata in sunflower oil. Nahrung 2003, 47:397-401.
41. Muñoz-Bertomeu J., Ros R., Arrillaga I., Segura J. Expression of spearmint limonene synthase in transgenic spike lavender results in an altered monoterpene composition in developing leaves. Metab Eng 2008, 10:166-177.
42. Murashige T., Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 1962, 15:473-497.
43. Nagegowda D.A. Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and suncellular compartimentation. FEBS Lett 2010, 284:2965-2973.
44. Pereira S.I., Santos P.A.G., Barroso J.G., Figueiredo A.C., Pedro L.G., Salgueiro L.R., et al. Chemical polymorphism of the essential oils from populations of Thymus caespititius grown on the island S. Jorge (Azores). Phytochemistry 2000, 55:241-246.
45. Poulose A.J., Croteau R. Biosynthesis of aromatic monoterpenes: conversion of γ-terpinene to p-cymene and thymol in Thymus vulgaris L. Arch Biochem Biophys 1978, 187:307-314.
46. Ro D.K., Ehlting J., Keeling C.I., Lin R., Mattheus N., Bohlmann J. Microarray expression profiling and functional characterization of AtTPS genes: duplicated Arabidopsis thaliana sesquiterpene synthase genes At4g13280 and At4g13300 encode root-specific and wound-inducible (Z)-γ-bisabolene synthases. Arch Biochem Biophys 2006, 448(1-2):104-116.
47. Roeder S., Hartmann A.M., Effermert U., Piechulla B. Regulation of simultaneous synthesis of floral scent terpenoids by the 1,8-cineole synthase of Nicotiana suaveolens. Plant Mol Biol 2007, 65:107-124.
48. Rout G.R., Samantaray S., Das P. In vitro manipulation and propagation of medicinal plants. Biotechnol Adv 2000, 18:20-91.
49. Salgueiro L. Potencialidades e aplicações das plantas aromáticas e medicinais. Curso teórico-prático 2006, 48-54. Edições da Faculdade de Ciências da Universidade de Lisboa - Centro de Biotecnologia Vegetal Lisboa. 1st ed. P. Os tomilhos de, A.C. Figueiredo, J.G. Barroso, L.G. Pedro (Eds.).
50. Schmiderer C., Grausgruber-Gröger S., Grassi P., Steinborn R., Novak J. Influence of gibberellins and daminozide on the expression of terpene synthases and on monoterpenes in common sage (Salvia officinalis). J Plant Physiol 2010, 167:779-786.
51. Schuler M.A., Werck-Reichhart D. Functional genomics of P450s. Annu Rev Plant Biol 2003, 54:629-667.
52. Steele C.L., Crock J., Bohlmann J., Croteau R. Sesquiterpene synthases from grand fir (Abies grandis) - comparison of constitutive and wound-induced activities, and cDNA isolation, characterization and bacterial expression of delta-selinene synthase and gamma-humulene synthase. J Biol Chem 1998, 273:2078-2089.
53. Tholl D. Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 2006, 9:297-304.
54. Trapp S.C., Croteau R.B. Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics 2001, 158:811-832.
55. Trindade H., Costa M.M., Lima A.S., Pedro L.G., Figueiredo A.C., Barroso J.G. Genetic diversity and chemical polymorphism of Thymus caespititius from Pico, São Jorge and Terceira islands (Azores). Biochem Syst Ecol 2008, 36:790-797.
56. Turner G., Gershenzon J., Nielson E.E., Froehlich J.E., Croteau R. Limonene synthase, the enzyme responsible for monoterpene biosynthesis in peppermint, is localized to leucoplasts of oil gland secretory cells. Plant Physiol 1999, 120:879-886.
57. Turner G.W., Croteau R. Organization of monoterpene biosynthesis in Mentha - immunocytochemical localizations of geranyl diphosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase and pulegone reductase. Plant Physiol 2004, 136:4215-4227.
58. Wise M.L., Savage T.J., Katahira E., Croteau R. Monoterpene synthases from common sage (Salvia officinalis): cDNA isolation, characterization, and functional expression of (+)-sabinene synthase, 1,8-cineole synthase, and (+)-bornyl diphosphate synthase. J Biol Chem 1998, 273(24):14891-14899.
59. Zarzuelo A., Crespo E. The medicinal and non-medicinal uses of thyme. Thyme: the genus Thymus, medicinal and aromatic plants - industrial profiles 2002, 263-292. Taylor & Francis, London. E. Stahl-Biskup, F. Sáez (Eds.).