Identification and Characterization of Terpene Synthases Potentially Involved in the Formation of Volatile Terpenes in Carrot (Daucus carota L.) Roots

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 19, 2015, Pages 4870-4878

  Yahyaa, Mosaab ^a   Tholl, Dorothea ^b   Cormier, Guy ^b   Jensen, Roderick ^b   Simon, Philipp W ^c   Ibdah, Mwafaq ^a  

^a VOLCANI CENTER   (Israel)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

(E) caryophyllene; Daucus carota; geraniol; terpene synthase; terpenes

Indexed keywords

BIOCHEMISTRY; GENES; MONOTERPENES; ODORS; PLANTS (BOTANY); RECOMBINANT PROTEINS; VOLATILE ORGANIC COMPOUNDS;

CARYOPHYLLENE; DAUCUS CAROTA; FUNCTIONAL CHARACTERIZATION; GERANIOL; NUTRACEUTICALS; SESQUITERPENE SYNTHASE; SYNTHASES; TRANSCRIPTOMES;

TERPENES;

DAUCUS CAROTA;

TERPENE; TERPENE SYNTHASE; TRANSFERASE; VEGETABLE PROTEIN; VOLATILE ORGANIC COMPOUND;

CARROT; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PLANT ROOT;

ALKYL AND ARYL TRANSFERASES; DAUCUS CAROTA; PLANT PROTEINS; PLANT ROOTS; TERPENES; VOLATILE ORGANIC COMPOUNDS;

EID: 84929994055     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b00546     Document Type: Article

References (52)

1. Fukuda, T.; Okazaki, K.; Shinano, T. Aroma characteristic and volatile profiling of carrot varieties and quantitative role of terpenoid compounds for carrot sensory attributes J. Food Sci. 2013, 78, S1800 - S1806 10.1111/1750-3841.12292
2. Yahyaa, M.; Bar, E.; Dubey, N. K.; Meir, A.; Davidovich-Rikanati, R.; Hirschberg, J.; Aly, R.; Tholl, D.; Simon, P. W.; Tadmor, Y.; Lewinsohn, E.; Ibdah, M. Formation of norisoprenoid flavor compounds in carrot (Daucus carota L.) roots: Characterization of a cyclic-specific carotenoid cleavage dioxygenase 1 gene J. Agric. Food Chem. 2013, 61, 12244 - 12252 10.1021/jf404085k
3. Simon, P. W.; Peterson, C. E.; Lindsay, R. C. Genotype, soil, and climate effects on sensory and objective components of carrot flavor J. Am. Soc. Hortic. Sci. 1982, 107, 644 - 648
4. Dudareva, N.; Pichersky, E.; Gershenzon, J. Biochemistry of plant volatiles Plant Physiol. 2004, 135, 1893 - 1902 10.1104/pp.104.049981
5. Matarese, F.; Cuzzola, A.; Scalabrelli, G.; D'Onofrio, C. Expression of terpene synthase genes associated with the formation of volatiles in different organs of Vitis vinifera Phytochemistry 2014, 105, 12 - 24 10.1016/j.phytochem.2014.06.007
6. Portnoy, V.; Benyamini, Y.; Bar, E.; Harel-Beja, R.; Gepstein, S.; Giovannoni, J. J.; Schaffer, A. A.; Burger, J.; Tadmor, Y.; Lewinsohn, E.; Katzir, N. The molecular and biochemical basis for varietal variation in sesquiterpene content in melon (Cucumis melo L.) rinds Plant Mol. Biol. 2008, 66, 647 - 661 10.1007/s11103-008-9296-6
7. Tholl, D.; Lee, S. Terpene specialized metabolism in Arabidopsis thaliana Arabidopsis Book 2011, 9, e0143 10.1199/tab.0143
8. Hasegawa, M.; Mitsuhara, I.; Seo, S.; Imai, T.; Koga, J.; Okada, K.; Yamane, H.; Ohashi, Y. Phytoalexin accumulation in the interaction between rice and the blast fungus Mol. Plant-Microbe Interact. 2010, 23, 1000 - 1011 10.1094/MPMI-23-8-1000
9. Heiling, S.; Schuman, M. C.; Schoettner, M.; Mukerjee, P.; Berger, B.; Schneider, B.; Jassbi, A. R.; Baldwin, I. T. Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata Plant Cell 2010, 22, 273 - 292 10.1105/tpc.109.071449
10. Walling, L. L. The myriad plant responses to herbivores J. Plant Growth Regul. 2000, 19, 195 - 216 10.1007/s003440000026
11. Tholl, D. Terpene synthases and the regulation, diversity and biological roles of terpene metabolism Curr. Opin. Plant Biol. 2006, 9, 297 - 304 10.1016/j.pbi.2006.03.014
12. Cunningham, F. X. J.; Gantt, E. Genes and enzymes of carotenoid biosynthesis in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49, 557 - 583 10.1146/annurev.arplant.49.1.557
13. Chen, F.; Tholl, D.; Bohlmann, J.; Pichersky, E. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom Plant J. 2011, 66, 212 - 229 10.1111/j.1365-313X.2011.04520.x
14. Degenhardt, J.; Kollner, T. G.; Gershenzon, J. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants Phytochemistry 2009, 70, 1621 - 1637 10.1016/j.phytochem.2009.07.030
15. Tholl, D.; Chen, F.; Petri, J.; Gershenzon, J.; Pichersky, E. Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers Plant J. 2005, 42, 757 - 771 10.1111/j.1365-313X.2005.02417.x
16. Huang, X.; Xiao, Y.; Kollner, T.; Zhang, W.; Wu, J.; Wu, J.; Guo, Y.; Zhang, Y. Identification and characterization of (E)-β-caryophyllene synthase and α/β-pinene synthase potentially involved in constitutive and herbivore-induced terpene formation in cotton Plant Physiol. Biochem. 2013, 73, 302 - 308 10.1016/j.plaphy.2013.10.017
17. Falara, V.; Akhtar, T. A.; Nguyen, T. T. H.; Spyropoulou, E. A.; Bleeker, P. M.; Schauvinhold, I.; Matsuba, Y.; Bonini, M. E.; Schilmiller, A. L.; Last, R. L.; Schuurink, R. C.; Pichersky, E. The tomato terpene synthase gene family Plant Physiol. 2011, 157, 770 - 789 10.1104/pp.111.179648
18. Martin, D. M.; Aubourg, S.; Schouwey, M. B.; Daviet, L.; Schalk, M.; Toub, O.; Lund, S. T.; Bohlmann, J. Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays BMC Plant Biol. 2010, 10, 226 10.1186/1471-2229-10-226
19. Galata, M.; Sarker, L. S.; Mahmoud, S. S. Transcriptome profiling, and cloning and characterization of the main monoterpene synthases of Coriandrum sativum L Phytochemistry 2014, 102, 64 - 73 10.1016/j.phytochem.2014.02.016
20. Hemmerlin, A.; Harwood, J. L.; Bach, T. J. A raison d'etre for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog. Lipid Res. 2012, 51, 95 - 148 10.1016/j.plipres.2011.12.001
21. Yu, Z.-X.; Wang, L.-J.; Zhao, B.; Shan, C.-M.; Zhang, Y.-H.; Chen, D.-F.; Chen, X.-Y. Progressive regulation of sesquiterpene biosynthesis in Arabidopsis and Patchouli (Pogostemon cablin) by the miR156-targeted SPL transcription factors Mol. Plant 2015, 8, 98 - 110 10.1016/j.molp.2014.11.002
22. Habegger, R.; Schnitzler, W. H. Aroma compounds in essential oils of carrots (Daucus carota L. ssp. sativus) leaves in comparison with roots J. Appl. Bot. 2000, 74, 220 - 223
23. Senalik, D. A.; Simon, P. W. Relationship between oil ducts and volatile terpenoid content in carrot roots Am. J. Bot. 1986, 73, 60 - 63 10.2307/2444277
24. Hampel, D.; Mosandl, A.; Wust, M. Biosynthesis of mono- and sesquiterpenes in carrot roots and leaves (Daucus carota L.): Metabolic cross talk of cytosolic mevalonate and plastidial methylerythritol phosphate pathways Phytochemistry 2005, 66, 305 - 311 10.1016/j.phytochem.2004.12.010
25. Rand, K.; Bar, E.; Ben-Ari, M.; Lewinsohn, E.; Inbar, M. The mono- and sesquiterpene content of aphid-induced galls on Pistacia palaestina is not a simple reflection of their composition in intact leaves J. Chem. Ecol. 2014, 40, 632 - 642 10.1007/s10886-014-0462-9
26. Iorizzo, M.; Senalik, D. A.; Grzebelus, D.; Bowman, M.; Cavagnaro, P. F.; Matvienko, M.; Ashrafi, H.; Van Deynze, A.; P.W, S. De novo assembly and characterization of the carrot transcriptome reveals novel genes, new markers, and genetic diversity BMC Genomics 2011, 12, 389 10.1186/1471-2164-12-389
27. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248 - 254 10.1016/0003-2697(76)90527-3
28. Alasalvar, C.; Grigor, J. M.; Quantick, P. C. Method for the static headspace analysis of carrot volatiles Food Chem. 1999, 65, 391 - 397 10.1016/S0308-8146(98)00202-7
29. Kjeldsen, F.; Christensen, L. P.; Edelenbos, M. Quantitative analysis of aroma compounds in carrot (Daucus carota L.) cultivars by capillary gas chromatography using large-volume injection technique J. Agric. Food Chem. 2001, 49, 4342 - 4348 10.1021/jf010213n
30. Kjeldsen, F.; Christensen, L. P.; Edelenbos, M. Changes in volatile compounds of carrots (Daucus carota L.) during refrigerated and frozen storage J. Agric. Food Chem. 2003, 51, 5400 - 5407 10.1021/jf030212q
31. Kreutzmann, S.; Thybo, A. K.; Edelenbos, M.; Christensen, L. P. The role of volatile compounds on aroma and flavour perception in coloured raw carrot genotypes Int. J. Food Sci. Technol. 2008, 43, 1619 - 1627 10.1111/j.1365-2621.2007.01662.x
32. Rosenfeld, H. J.; Knut S. Dalen, K. S.; Haffner, K. The growth and development of carrot roots Gartenbauwissenschaft 2002, 67, 11 - 16
33. Nicolle, C.; Simon, G.; Rock, E.; Amouroux, P.; Remesy, C. Genetic variability influences carotenoid, vitamin, phenolic, and mineral content in white, yellow, purple, orange, and dark-orange carrot cultivars J. Am. Soc. Hortic. Sci. 2004, 129, 523 - 529
34. Cai, Y.; Jia, J.-W.; Crock, J.; Lin, Z.-X.; Chen, X.-Y.; Croteau, R. A cDNA clone for β-caryophyllene synthase from Artemisia annua Phytochemistry 2002, 61, 523 - 529 10.1016/S0031-9422(02)00265-0
35. Sarker, L.; Demissie, Z.; Mahmoud, S. Cloning of a sesquiterpene synthase from Lavandula × intermedia glandular trichomes Planta 2013, 238, 983 - 989 10.1007/s00425-013-1937-6
36. 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 10.1016/j.abb.2007.06.011
37. Bleeker, P. M.; Spyropoulou, E. A.; Diergaarde, P. J.; Volpin, H.; Both, M. J.; Zerbe, P.; Bohlmann, J.; Falara, V.; Matsuba, Y.; Pichersky, E.; Haring, M. A.; Schuurink, R. C. RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes Plant Mol. Biol. 2011, 77, 323 - 336 10.1007/s11103-011-9813-x
38. Huang, M.; Abel, C.; Sohrabi, R.; Petri, J.; Haupt, I.; Cosimano, J.; Gershenzon, J.; Tholl, D. Variation of herbivore-induced volatile terpenes among Arabidopsis ecotypes depends on allelic differences and subcellular targeting of two terpene synthases, TPS02 and TPS03 Plant Physiol. 2010, 153, 1293 - 1310 10.1104/pp.110.154864
39. Koellner, T. G.; Held, M.; Lenk, C.; Hiltpold, I.; Turlings, T. C. J.; Gershenzon, J.; Degenhardt, J. A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties Plant Cell 2008, 20, 482 - 494 10.1105/tpc.107.051672
40. Bos, R.; Koulman, A.; Woerdenbag, H. J.; Quax, W. J.; Pras, N. Volatile components from Anthriscus sylvestris (L.) Hoffm J. Chromatogr. A 2002, 966, 233 - 238 10.1016/S0021-9673(02)00704-5
41. Chen, F.; Ro, D. K.; Petri, J.; Gershenzon, J.; Bohlmann, J.; Pichersky, E.; Tholl, D. 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 10.1104/pp.104.044388
42. Kessler, A.; Baldwin, I. T. Defensive function of herbivore-induced plant volatile emissions in nature Science 2001, 291, 2141 - 2144 10.1126/science.291.5511.2141
43. Rasmann, S.; Köllner, T. G.; Degenhardt, J.; Hiltpold, I.; Toepfer, S.; Kuhlmann, U.; Gershenzon, J.; Turlings, T. C. J. Recruitment of entomopathogenic nematodes by insect-damaged maize roots Nature 2005, 434, 732 - 737 10.1038/nature03451
44. Schnee, C.; Kollner, T. G.; Gershenzon, J.; Degenhardt, J. The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-β-farnesene, (E)-nerolidol, and (E, E)-farnesol after herbivore damage Plant Physiol. 2002, 130, 2049 - 2060 10.1104/pp.008326
45. Arimura, G. I.; Koepke, S.; Kunert, M.; Volpe, V.; David, A.; Brand, P.; Dabrowska, P.; Maffei, M. E.; Boland, W. Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission Plant Physiol. 2008, 146, 965 - 973 10.1104/pp.107.111088
46. Davis, E. M.; Croteau, R. Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes Biosynthesis 2000, 209, 53 - 95 10.1007/3-540-48146-X-2
47. Williams, D. C.; McGarvey, D. J.; Katahira, E. J.; Croteau, R. Truncation of limonene synthase preprotein provides a fully active 'pseudomature' form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair Biochemistry 1998, 37, 12213 - 12220 10.1021/bi980854k
48. Martin, D. M.; Bohlmann, J. Identification of Vitis vinifera (-)-α-terpineol synthase by in silico screening of full-length cDNA ESTs and functional characterization of recombinant terpene synthase Phytochemistry 2004, 65, 1223 - 1229 10.1016/j.phytochem.2004.03.018
49. Bohlmann, J.; Meyer-Gauen, G.; Croteau, R. Plant terpenoid synthases: Molecular biology and phylogenetic analysis Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 4126 - 4133 10.1073/pnas.95.8.4126
50. Pickel, B.; Drew, D. P.; Manczak, T.; Weitzel, C.; Simonsen, H. T.; Ro, D. K. Identification and characterization of a kunzeaol synthase from Thapsia garganica: Implications for the biosynthesis of the pharmaceutical thapsigargin Biochem. J. 2012, 448, 261 - 271 10.1042/BJ20120654
51. Nieuwenhuizenm, N. J.; Green, S. A.; Chen, X.; Bailleul, E. J.; Matich, A. J.; Wang, M. Y.; Atkinson, R. G. Functional genomics reveals that a compact terpene synthase gene family can account for terpene volatile production in apple Plant Physiol. 2013, 161, 787 - 804 10.1104/pp.112.208249
52. Lucker, J.; El Tamer, M. K.; Schwab, W.; Verstappen, F. W. A.; van der Plas, L. H. W.; Bouwmeester, H. J.; Verhoeven, H. A. Monoterpene biosynthesis in lemon (Citrus limon)-cDNA isolation and functional analysis of four monoterpene synthases Eur. J. Biochem. 2002, 269, 3160 - 3171 10.1046/j.1432-1033.2002.02985.x