Herbivore-induced terpenoid emission in Medicago truncatula: Concerted action of jasmonate, ethylene and calcium signaling

Planta

Volumn 227, Issue 2, 2008, Pages 453-464

  Arimura, Gen Ichiro ^a   Garms, Stefan ^a   Maffei, Massimo ^b   Bossi, Simone ^b   Schulze, Birgit ^a   Leitner, Margit ^a   Mithöfer, Axel ^a   Boland, Wilhelm ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Calcium; Ethylene; Jasmonic acid; Medicago truncatula; Terpenoid

Indexed keywords

CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; JASMONIC ACID; OXYLIPIN; TERPENE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; BARREL MEDIC; CALCIUM SIGNALING; DRUG EFFECT; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; LARVA; METABOLISM; MOTH; PHYSIOLOGY;

ANIMALS; CALCIUM SIGNALING; CYCLOPENTANES; ETHYLENES; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION, PLANT; LARVA; MEDICAGO TRUNCATULA; MOTHS; OXYLIPINS; PLANT PROTEINS; TERPENES;

MEDICAGO TRUNCATULA; SPODOPTERA EXIGUA;

EID: 40949096452     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-007-0631-y     Document Type: Article

References (47)

1. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FWA, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866-2884
2. Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594-602
3. Ament K, Van Schie CC, Bouwmeester HJ, Haring MA, Schuurink RC (2006) Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways. Planta 224:1197-1208
4. Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512-515
5. Arimura G, Huber DPW, Bohlmann J (2004a) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa × deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (-)-germacrene D synthase, PtdTPS1. Plant J 37:603-616
6. Arimura G, Ozawa R, Kugimiya S, Takabayashi J, Bohlmann J (2004b) Herbivore-induced defense response in a model legume. Two-spotted spider mites induce emission of (E)-β-ocimene and transcript accumulation of (E)-β-ocimene synthase in Lotus japonicus. Plant Physiol 135:1976-1983
7. Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta 1734:91-111
8. Bach TJ, Lichtenthaler HK (1982) Mevinolin: a highly specific inhibitor of microsomal 3-hydroxy-3-methylglutaryl-coenzyme A reductase of radish plants. Z Naturforsch [C] 37:46-50
9. Bartram S, Jux A, Gleixner G, Boland W (2006) Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry 67:1661-1672
10. Bergomaz R, Boppré M (1986) A simple instant diet for rearing Arctiidae and other moths. J Lepidopt Soc 40:131-137
11. Bick JA, Lange M (2003) Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys 415:146-154
12. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:1907-1922
13. Degenhardt J, Gershenzon J (2000) 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 210:815-822
14. Donath J, Boland W (1994) Biosynthesis of acyclic homoterpenes in higher plants parallels steroid hormone metabolism. J Plant Physiol 143:473-478
15. Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Fäldt J, Miller B, Bohlmann J (2003) (E)-β-Ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell 15:1227-1241
16. Edelmann HG, Gudi G, Kühnemann F (2002) The gravitropic setpoint angle of dark-grown rye seedlings and the role of ethylene. J Exp Bot 53:1627-1634
17. Eisenreich W, Bacher A, Arigoni D, Rohdich F (2004) Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell Mol Life Sci 61:1401-1426
18. Engelberth J, Koch T, Schüler G, Bachmann N, Rechtenbach J, Boland W (2001) Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol 125:369-377
19. Gomez SK, Cox MM, Bede JC, Inoue K, Alborn HT, Tumlinson JH, Korth KL (2005) Lepidopteran herbivory and oral factors induce transcripts encoding novel terpene synthases in Medicago truncatula. Arch Insect Biochem Physiol 58:114-127
20. Horiuchi J, Arimura G, Ozawa R, Shimoda T, Takabayashi J, Nishioka T (2001) Exogenous ACC enhances volatiles production mediated by jasmonic acid in lima bean leaves. FEBS Lett 509:332-336
21. Jez JM, Ferrer JL, Bowman ME, Dixon RA, Noel JP (2000) Dissection of malonyl-coenzyme A decarboxylation from polyketide formation in the reaction mechanism of a plant polyketide synthase. Biochemistry 39:890-902
22. Kahl J, Siemens DH, Aerts RJ, Gäbler R, Kühnemann F, Preston CA, Baldwin IT (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336-342
23. Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004) The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 16:1115-1131
24. Krumm T, Bandemer K, Boland W (1995) Induction of volatile biosynthesis in the Lima bean (Phaseolus lunatus) by leucine- and isoleucine conjugates of 1-oxo- and 1-hydroxyindan-4-carboxylic acid: evidence for amino acid conjugates of jasmonic acid intermediates in the octadecanoid signalling pathway. FEBS Lett 377:523-529
25. Kuzuyama T, Shimizu T, Takahashi S, Seto H (1998) Fosmidomycin, a specific inhibitor of 1-deoxy-D-xylulose 5-phosphate reductoisomerase in the nonmevalonate pathway for terpenoid biosynthesis. Tetrahedron Lett 39:7913-7916
26. Leitner M, Boland W, Mithöfer A (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol 167:597-606
27. Lücker J, Bouwmeester HJ, Schwab W, Blaas J, van der Plas LHW, Verhoeven HA (2001) Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of S-linalyl-β-D- glucopyranoside. Plant J 27:315-324
28. Maffei M, Bossi S, Spiteller D, Mithöfer A, Boland W (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol 134:1752-1762
29. Maffei ME, Mithöfer A, Arimura G, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS, Novero M, Volpe V, Quadro S, Boland W (2006) Effects of feeding Spodoptera littoralis on Lima Bean Leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 140:1022-1035
30. McKay SAB, Hunter WL, Godard KA, Wang SX, Martin DM, Bohlmann J, Plant AL (2003) Insect attack and wounding induce traumatic resin duct development and gene expression of (-)-pinene synthase in Sitka spruce. Plant Physiol 133:368-378
31. Meyer O, Hoeffler JF, Grosdemange-Billiard C, Rohmer M (2004) Practical synthesis of 1-deoxy-D-xylulose and 1-deoxy-D-xylulose 5-phosphate allowing deuterium labelling. Tetrahedron 60:12153-12162
32. Mithöfer A, Ebel J, Bhagwat AA, Boller T, Neuhaus-Url G (1999) Transgenic aequorin monitors cytosolic calcium transients in soybean cells challenged with β-glucan or chitin elicitors. Planta 207:566-574
33. Oldroyd GED, Engstrom EM, Long SR (2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13:1835-1849
34. Ozawa R, Arimura G, Takabayashi J, Shimoda T, Nishioka T (2000) Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol 41:391-398
35. Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275:527-530
36. Piel J, Donath J, Bandemer K, Boland W (1998) Mevalonate-independent biosynthesis of terpenoid volatiles in plants: induced and constitutive emission of volatiles. Angew Chem Int Ed 37:2478-2481
37. Rodríguez-Concepción 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 130:1079-1089
38. Ruther J, Kleier S (2005) Plant-plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol 31:2217-22
39. Sharon-Asa L, Shalit M, Frydman A, Bar E, Holland D, Or E, Lavi U, Lewinsohn E, Eyal Y (2003) Citrus fruit flavor and aroma biosynthesis: isolation, functional characterization, and developmental regulation of Cstps1, a key gene in the production of the sesquiterpene aroma compound valencene. Plant J 36:664-674
40. Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH (2003a) Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133:295-306
41. Schmelz EA, Alborn HT, Tumlinson JH (2003b) Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Physiol Plant 117:403-412
42. Schulze B, Lauchli R, Sonwa MM, Schmidt A, Boland W (2006) Profiling of structurally labile oxylipins in plants by in situ derivatization with pentafluorobenzyl hydroxylamine. Anal Biochem 348:269-283
43. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117-2127
44. Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E (2005) Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J 42:757-771
45. Veen H (1983) Silver thiosulfate: an experimental tool in plant science. Sci Hortic 20:211-224
46. Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-D-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31:243-54
47. Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):S131-S151