Three-step pathway engineering results in more incidence rate and higher emission of nerolidol and improved attraction of Diadegma semiclausum

Metabolic Engineering

Volumn 15, Issue 1, 2013, Pages 88-97

  Houshyani, Benyamin ^a   Assareh, Maryam ^a   Busquets, Antoni ^b   Ferrer, Albert ^c,d   Bouwmeester, Harro J ^a   Kappers, Iris F ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^c CENTRE FOR RESEARCH IN AGRICULTURAL GENOMICS CRAG   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Arabidopsis thaliana; Diadegma semiclausum; Indirect insect defence; Linalool; Metabolic engineering; Nerolidol; Terpenoids

Indexed keywords

ARABIDOPSIS THALIANA; DIADEGMA SEMICLAUSUM; INDIRECT INSECT DEFENCE; LINALOOL; NEROLIDOL; TERPENOIDS;

ALCOHOLS; BIOSYNTHESIS; LIPIDS; METABOLIC ENGINEERING; PLANTS (BOTANY);

BIOCHEMISTRY;

LINALOOL; NEROLIDOL;

ARTICLE; CONTROLLED STUDY; CYTOSOL; DIADEGMA SEMICLAUSUM; DRUG SYNTHESIS; INCIDENCE; METABOLIC ENGINEERING; NONHUMAN; PARASITOID; PRIORITY JOURNAL;

ANIMALS; GENETIC ENHANCEMENT; HOST-PARASITE INTERACTIONS; LEPIDOPTERA; METABOLIC ENGINEERING; MULTIENZYME COMPLEXES; PLANTS, GENETICALLY MODIFIED; SESQUITERPENES; WASPS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; DIADEGMA SEMICLAUSUM; HEXAPODA;

EID: 84871451005     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2012.10.002     Document Type: Article

References (53)

1. Adam K.P., Zapp J. Biosynthesis of the isoprene units of chamomile sesquiterpenes. Phytochemistry 1998, 48:953-959.
2. Adams, R.P., 1995. Identification of Essential Oil Components by Gas Chromatography/Mass Spectroscopy.
3. Aharoni A., Giri A.P., Deuerlein S., Griepink F., De Kogel W.J., Verstappen F.W.A., Verhoeven H.A., Jongsma M.A., Schwab W., Bouwmeester H.J. Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 2003, 15:2866-2884.
4. Aharoni A., Giri A.P., Verstappen F.W.A., Bertea C.M., Sevenier R., Sun Z., Jongsma M.A., Schwab W., Bouwmeester H.J. Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 2004, 16:3110-3131.
5. Aharoni A., Jongsma M.A., Bouwmeester H.J. Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci. 2005, 10:594-602.
6. Ament K., Kant M.R., Sabelis M.W., Haring M.A., Schuurink R.C. Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol. 2004, 135:2025-2037.
7. Bouwmeester H.J., Matusova R., Zhongkui S., Beale M.H. Secondary metabolite signaling in host-parasitic plant interactions. Curr. Opin. Plant Biol. 2003, 6:358-364.
8. Bouwmeester H.J., Verstappen F.W.A., Posthumus M.A., Dicke M. Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima bean. The first dedicated step in acyclic C11-homoterpene biosynthesis. Plant Physiol. 1999, 121:173-180.
9. Bukovinszky T., Gols R., Posthumus M.A., Vet L.E.M., Van Lenteren J.C. Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Helle̕n). J. Chem. Ecol. 2005, 31:461-480.
10. Chappell J., VonLanken C., Vögeli U. Elicitor-inducible 3-hydroxy-3-methylglutaryl coenzyme a reductase activity is required for sesquiterpene accumulation in tobacco cell suspension cultures. Plant Physiol. 1991, 97:693-698.
11. Chen D.H., Ye H.C., Li G.F. Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant Sci. 2000, 155:179-185.
12. Cunillera N., Arro M., Delourme D., Karst F., Boronat A., Ferrer A. Arabidopsis thaliana contains two differentially expressed farnesyl-diphosphate synthase genes. J. Biol. Chem. 1996, 271:7774-7780.
13. Cunillera N., Boronat A., Ferrer A. The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J. Biol. Chem. 1997, 272:15381-15388.
14. Degenhardt J., Gershenzon J. Demonstration and characterization of (E)-nerolidol synthase from maize: a herbivore-inducible terpene synthase participating in (3E)-4,8-dimethyl-1,3,7-nonatriene biosynthesis. Planta 2000, 210:815-822.
15. Degenhardt J., Gershenzon J., Baldwin I.T., Kessler A. Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr. Opin. Biotechnol. 2003, 14:169-176.
16. Degenhardt J., Hiltpold I., Kollner T.G., Frey M., Gierl A., Gershenzon J., Hibbard B.E., Ellersieck M.R., Turlings T.C.J. Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc. Nat. Acad. Sci. U.S.A. 2009, 106:13213-13218.
17. Delourme D., Lacroute F., Karst F. Cloning of an Arabidopsis thaliana cDNA coding for farnesyl diphosphate synthase by functional complementation in yeast. Plant Mol. Biol. 1994, 26:1867-1873.
18. Dicke M., Baldwin I.T. The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends Plant Sci. 2010, 15:167-175.
19. Dicke M., Van Beek T.A., Posthumus M.A., Ben Dom N., Van Bokhoven H., De Groot A. Isolation and identification of volatile kairomone that affects acarine predatorprey interactions Involvement of host plant in its production. J. Chem. Ecol. 1990, 16:381-396.
20. Gatehouse J.A. Plant resistance towards insect herbivores: a dynamic interaction. New Phytol. 2002, 156:145-169.
21. Halbert S.E., Corsini D., Wiebe M., Vaughn S.F. Plant-derived compounds and extracts with potential as aphid repellents. Ann. Appl. Biol. 2009, 154:303-307.
22. Halitschke R., Baldwin I.T. Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J. 2003, 36:794-807.
23. Houshyani B., Kabouw P., Muth D., Vos R.C.H.d., Bino R.J., Bouwmeester H.J. Characterization of the natural variation in Arabidopsis thaliana metabolome by the analysis of metabolic distance. Metabolomics 2011, 8:131-145.
24. James D.G. Further field evaluation of synthetic herbivore-induced plan volatiles as attractants for beneficial insects. J. Chem. Ecol. 2005, 31:481-495.
25. Kappers I.F., Aharoni A., Van Herpen T.W.J.M., Luckerhoff L.L.P., Dicke M., Bouwmeester H.J. Plant science: genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 2005, 309:2070-2072.
26. Kessler A., Baldwin I.T. Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J. 2004, 38:639-649.
27. Kind T., Fiehn O. Seven Golden Rules for heuristic filtering of molecular formulas obtained by accurate mass spectrometry. BMC Bioinf. 2007, 8:105.
28. Kohler R.H., Zipfel W.R., Webb W.W., Hanson M.R. The green fluorescent protein as a marker to visualize plant mitochondria in vivo. Plant J. 1997, 11:613-621.
29. Lee S., Badieyan S., Bevan D.R., Herde M., Gatz C., Tholl D. Herbivore-induced and floral homoterpene volatiles are biosynthesized by a single P450 enzyme (CYP82G1) in Arabidopsis. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:21205-21210.
30. Lichtenthaler H.K. Non-mevalonate isoprenoid biosynthesis: enzymes, genes and inhibitors. Biochem. Soc. Trans. 2000, 28:785-789.
31. Loivamaki M., Mumm R., Dicke M., Schnitzler J.P. Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:17430-17435.
32. Lommen A. Metalign: interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. Anal. Chem. 2009, 81:3079-3086.
33. Manzano D., Busquets A., Closa M., Hoyerova K., Schaller H., Kaminek M., Arro M., Ferrer A. Overexpression of farnesyl diphosphate synthase in Arabidopsis mitochondria triggers light-dependent lesion formation and alters cytokinin homeostasis. Plant Mol. Biol. 2006, 61:195-213.
34. Manzano D., Fernández-Busquets X., Schaller H., Gonzalez V., Boronat A., Arro M., Ferrer A. The metabolic imbalance underlying lesion formation in Arabidopsis thaliana overexpressing farnesyl diphosphate synthase [isoform 1S] leads to oxidative stress and is triggered by the developmental decline of endogenous HMGR activity. Planta 2004, 219:982-992.
35. Mumm R., Dicke M. Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can. J. Zool. 2010, 88:628-667.
36. Pompella A., Visvikis A., Paolicchi A., De Tata V., Casini A.F. The changing faces of glutathione, a cellular protagonist. Biochem. Pharmacol. 2003, 66:1499-1503.
37. Rohloff J., Bones A.M. Volatile profiling of Arabidopsis thaliana-putative olfactory compounds in plant communication. Phytochemistry 2005, 66:1941-1955.
38. Schnee C., Kollner T.G., Held M., Turlings T.C.J., Gershenzon J., Degenhardt J. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Nat. Acad. Sci. U.S.A. 2006, 103:1129-1134.
39. Smilauer J.L.a.P. Multivariate Analysis of Ecological Data using CANOCO 2003, Cambridge University Press, Cambridge.
40. Snoeren T.A.L., Kappers I.F., Broekgaarden C., Mumm R., Dicke M., Bouwmeester H.J. Natural variation in herbivore-induced volatiles in Arabidopsis thaliana. J. Exp. Bot. 2010, 61:3041-3056.
41. Snoeren T.A.L., van Poecke R.M.P., Dicke M. Multidisciplinary approach to unravelling the relative contribution of different oxylipins in indirect defense of Arabidopsis thaliana. J. Chem. Ecol. 2009, 35:1021-1031.
42. 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.
43. Usta J., Kreydiyyeh S., Knio K., Barnabe P., Bou-Moughlabay Y., Dagher S. Linalool decreases HepG2 viability by inhibiting mitochondrial complexes I and II, increasing reactive oxygen species and decreasing ATP and GSH levels. Chem. Biol. Interact. 2009, 180:39-46.
44. van Herpen T.W.J.M., Cankar K., Nogueira M., Bosch D., Bouwmeester H.J., Beekwilder J. Nicotiana benthamiana as a production platform for artemisinin precursors. PLoS One 2010, 5.
45. Van Poecke R.M.P., Dicke M. Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant. Plant Biol. 2004, 6:387-401.
46. Vasconcelos I.M., Oliveira J.T.A. Antinutritional properties of plant lectins. Toxicon 2004, 44:385-403.
47. Von Rad U., Huttl R., Lottspeich F., Gierl A., Frey M. Two glucosyltransferases are involved in detoxification of benzoxazinoids in maize. Plant J. 2001, 28:633-642.
48. Wei S., Reuveny H., Bravdo B.A., Shoseyov O. Hydrolysis of glycosidically bound volatiles from apple leaves (cv. Anna) by Aspergillus niger Β-glucosidase affects the behavior of codling moth (Cydia pomonella L.). J. Agric. Food Chem. 2004, 52:6212-6216.
49. Wittstock U., Gershenzon J. Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr. Opin. Plant Biol. 2002, 5:300-307.
50. Wu S., Schalk M., Clark A., Miles R.B., Coates R., Chappell J. Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat. Biotechnol. 2006, 24:1441-1447.
51. Yang T., Stoopen G., Yalpani N., Vervoort J., de Vos R., Voster A., Verstappen F.W.A., Bouwmeester H.J., Jongsma M.A. Metabolic engineering of geranic acid in maize to achieve fungal resistance is compromised by novel glycosylation patterns. Metab. Eng. 2011, 13:414-425.
52. Yu F., Utsumi R. Diversity, regulation, and genetic manipulation of plant mono- and sesquiterpenoid biosynthesis. Cell. Mol. Life Sci. 2009, 66:3043-3052.
53. Zhang Y., Nowak G., Reed D.W., Covello P.S. The production of artemisinin precursors in tobacco. Plant Biotechnol. J. 2011, 9:445-454.