Jasmonic acid and its precursor 12-Oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in tomato

Plant Physiology

Volumn 166, Issue 1, 2014, Pages 396-410

  Bosch, Marko ^a   Wright, Louwrance P ^b   Gershenzon, Jonathan ^b   Wasternack, Claus ^c   Hause, Bettina ^c   Schaller, Andreas ^a   Stintzi, Annick ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

12-OXOPHYTODIENOIC ACID; 3-HEXENAL; ALDEHYDE; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; TERPENE; UNSATURATED FATTY ACID;

ANIMAL; EGG LAYING; FOOD PREFERENCE; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HERBIVORY; IMMUNOLOGY; LARVA; MANDUCA; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE; SECONDARY METABOLISM; TOMATO; TRICHOME;

ALDEHYDES; ANIMALS; CYCLOPENTANES; FATTY ACIDS, UNSATURATED; FOOD PREFERENCES; GENE EXPRESSION REGULATION, PLANT; HERBIVORY; LARVA; LYCOPERSICON ESCULENTUM; MANDUCA; OVIPOSITION; OXYLIPINS; RNA INTERFERENCE; SECONDARY METABOLISM; TERPENES; TRICHOMES;

EID: 84907060517     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.237388     Document Type: Article

References (133)

1. Allmann S, Baldwin IT (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329: 1075-1078.
2. Allmann S, Späthe A, Bisch-Knaden S, Kallenbach M, Reinecke A, Sachse S, Baldwin IT, Hansson BS (2013) Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition. Elife (Cambridge) 2: e00421.
3. Alméras E, Stolz S, Vollenweider S, Reymond P, Mène-Saffrané L, Farmer EE (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J 34: 205-216.
4. Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135: 2025-2037.
5. Avdiushko SA, Brown GC, Dahlman DL, Hildebrand DF (1997) Methyl jasmonate exposure induces insect resistance in cabbage and tobacco. Environ Entomol 26: 642-654.
6. Balcke GU, Handrick V, Bergau N, Fichtner M, Henning A, Stellmach H, Tissier A, Hause B, Frolov A (2012) An UPLC-MS/MS method for highly sensitive high-throughput analysis of phytohormones in plant tissues. Plant Methods 8: 47.
7. Blakeney AB, Matheson NK (1984) Some properties of the stem and pollen starches of rice. Starch/Stärke 36: 265-269.
8. Blakeney AB, Mutton LL (1980) A simple colorimetric method for the determination of sugars in fruit and vegetables. J Sci Food Agric 31: 889-897.
9. Blechert S, Bockelmann C, Füßlein M, Von Schrader T, Stelmach B, Niesel U, Weiler EW (1999) Structure-activity analyses reveal the existence of two separate groups of active octadecanoids in elicitation of the tendril-coiling response of Bryonia dioica Jacq. Planta 207: 470-479.
10. Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR, Prins M, de Vos M, Haring MA, Schuurink RC (2012) Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proc Natl Acad Sci USA 109: 20124-20129.
11. Boughton AJ, Hoover K, Felton GW (2005) Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J Chem Ecol 31: 2211-2216.
12. Breithaupt C, Kurzbauer R, Lilie H, Schaller A, Strassner J, Huber R, Macheroux P, Clausen T (2006) Crystal structure of 12-oxophytodienoate reductase 3 from tomato: self-inhibition by dimerization. Proc Natl Acad Sci USA 103: 14337-14342.
13. Breithaupt C, Kurzbauer R, Schaller F, Stintzi A, Schaller A, Huber R, Macheroux P, Clausen T (2009) Structural basis of substrate specificity of plant 12-oxophytodienoate reductases. J Mol Biol 392: 1266-1277.
14. Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60: 183-205.
15. Brüx A, Liu TY, Krebs M, Stierhof YD, Lohmann JU, Miersch O, Wasternack C, Schumacher K (2008) Reduced V-ATPase activity in the trans-Golgi network causes oxylipin-dependent hypocotyl growth inhibition in Arabidopsis. Plant Cell 20: 1088-1100.
16. Carter CD, Gianfagna TJ, Sacalis JN (1989) Sesquiterpenes in glandular trichomes of a wild tomato species and toxicity to the Colorado potato beetle. J Agric Food Chem 37: 1425-1428.
17. Chehab EW, Kaspi R, Savchenko T, Rowe H, Negre-Zakharov F, Kliebenstein D, Dehesh K (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS ONE 3: e1904.
18. Chehab EW, Kim S, Savchenko T, Kliebenstein D, Dehesh K, Braam J (2011) Intronic T-DNA insertion renders Arabidopsis opr3 a conditional jasmonic acid-producing mutant. Plant Physiol 156: 770-778.
19. Chen QF, Dai LY, Xiao S, Wang YS, Liu XL, Wang GL (2007) The COI1 and DFR genes are essential for regulation of jasmonate-induced anthocyanin accumulation in Arabidopsis. J Integr Plant Biol 9: 1370-1377.
20. Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García- Casado G, López-Vidriero I, Lozano FM, Ponce MR, et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671.
21. Dalin P, Agren J, Björkman C, Huttunen P, Kärkkäinen K (2008) Leaf trichome formation and plant resistance to herbivory. In Schaller A, ed, Induced Plant Resistance to Herbivory. Springer, Heidelberg, pp 89-105.
22. Dave A, Graham IA (2012) Oxylipin signalling: a distinct role for the jasmonic acid precursor 12-Oxo-Phytodienoic Acid (cisOPDA). Front Plant Sci 3: 42.
23. Dave A, Hernández ML, He Z, Andriotis VME, Vaistij FE, Larson TR, Graham IA (2011) 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23: 583-599.
24. De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17: 349-359.
25. De Marcos Lousa C, van Roermund CWT, Postis VLG, Dietrich D, Kerr ID, Wanders RJA, Baldwin SA, Baker A, Theodoulou FL (2013) Intrinsic acyl-CoA thioesterase activity of a peroxisomal ATP binding cassette transporter is required for transport and metabolism of fatty acids. Proc Natl Acad Sci USA 110: 1279-1284.
26. Degenhardt DC, Refi-Hind S, Stratmann JW, Lincoln DE (2010) Systemin and jasmonic acid regulate constitutive and herbivore-induced systemic volatile emissions in tomato, Solanum lycopersicum. Phytochemistry 71: 2024-2037
27. Del Campo ML, Miles CI, Schroeder FC, Mueller C, Booker R, Renwick JA (2001) Host recognition by the tobacco hornworm is mediated by a host plant compound. Nature 411: 186-189.
28. Eigenbrode SD, Trumble JT, Millar JG, White KK (1994) Topical toxicity of tomato sesquiterpenes to the beet armyworm and the role of these compounds in resistance derived from an accession of Lycopersicon hirsutum f. typicum. J Agric Food Chem 42: 807-810.
29. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101: 1781-1785.
30. Escalante-Pérez M, Krol E, Stange A, Geiger D, Al-Rasheid KAS, Hause B, Neher E, Hedrich R (2011) A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap. Proc Natl Acad Sci USA 108: 15492-15497.
31. Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RESactivated signaling. Annu Rev Plant Biol 64: 429-450.
32. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87: 7713-7716.
33. Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4: 129-134.
34. Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Nat Biotechnol 5: 726-730.
35. Fliegmann J, Schüler G, Boland W, Ebel J, Mithöfer A (2003) The role of octadecanoids and functional mimics in soybean defense responses. Biol Chem 384: 437-446.
36. Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5: 344-350.
37. Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180: 722-734.
38. Fulda M, Schnurr J, Abbadi A, Heinz E, Browse J (2004) Peroxisomal Acyl- CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell 16: 394-405.
39. Goetz S, Hellwege A, Stenzel I, Kutter C, Hauptmann V, Forner S, McCaig B, Hause G, Miersch O, Wasternack C, et al (2012) Role of cis- 12-oxo-phytodienoic acid in tomato embryo development. Plant Physiol 158: 1715-1727.
40. Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175: 776-777.
41. Halitschke R, Ziegler J, Keinänen M, Baldwin IT (2004) Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in Nicotiana attenuata. Plant J 40: 35-46.
42. Haribal M, Renwick JAA, Attygalle AB, Kiemle D (2006) A feeding stimulant for Manduca sexta from Solanum surattenses. J Chem Ecol 32: 2687-2694.
43. Hause B, Stenzel I, Miersch O, Maucher H, Kramell R, Ziegler J, Wasternack C (2000) Tissue-specific oxylipin signature of tomato flowers: allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J 24: 113-126.
44. Heiling S, Schuman MC, Schoettner M, Mukerjee P, Berger B, Schneider B, Jassbi AR, Baldwin IT (2010) 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 22: 273-292.
45. Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Holder E, Grausem B, Kandel S, Miesch M, et al (2012) Cytochromes P450. CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone Jasmonoyl-isoleucine for catabolic turnover. J Biol Chem 287: 6296-6306.
46. Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8: 2067-2077.
47. Howe GA, Schaller A (2008) Direct defenses in plants and their induction by wounding and insect herbivores. In Schaller A, ed, Induced Plant Resistance to Herbivory. Springer, Heidelberg, pp 7-29.
48. Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13: 2191-2209.
49. Kang JH, Liu G, Shi F, Jones AD, Beaudry RM, Howe GA (2010) The tomato odorless-2 mutant is defective in trichome-based production of diverse specialized metabolites and broad-spectrum resistance to insect herbivores. Plant Physiol 154: 262-272.
50. Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucinemediated defenses against Manduca sexta. Plant Cell 18: 3303-3320.
51. Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17: 22-31.
52. Kennedy GG (2003) Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu Rev Entomol 48: 51-72.
53. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141-2144.
54. Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305: 665-668.
55. Koch T, Krumm T, Jung V, Engelberth J, Boland W (1999) Differential induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway. Plant Physiol 121: 153-162.
56. Koo AJK, Chung HS, Kobayashi Y, Howe GA (2006) Identification of a peroxisomal acyl-activating enzyme involved in the biosynthesis of jasmonic acid in Arabidopsis. J Biol Chem 281: 33511-33520.
57. Koo AJK, Gao X, Jones AD, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59: 974-986.
58. Koo AJK, Howe GA (2009) The wound hormone jasmonate. Phytochemistry 70: 1571-1580.
59. Koo AJK, Howe GA (2012) Catabolism and deactivation of the lipidderived hormone jasmonoyl-isoleucine. Front Plant Sci 3: 19.
60. Li C, Liu G, Xu C, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA (2003) The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15: 1646-1661.
61. Li C, Schilmiller AL, Liu G, Lee GI, Jayanty S, Sageman C, Vrebalov J, Giovannoni JJ, Yagi K, Kobayashi Y, et al (2005) Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17: 971-986.
62. Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99: 6416-6421.
63. Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143.
64. Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P (2008) Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol 179: 1004-1016.
65. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9: 274-280.
66. Matsuura H, Takeishi S, Kiatoka N, Sato C, Sueda K, Masuta C, Nabeta K (2012) Transportation of de novo synthesized jasmonoyl isoleucine in tomato. Phytochemistry 83: 25-33.
67. Matthes MC, Bruce TJ, Ton J, Verrier PJ, Pickett JA, Napier JA (2010) The transcriptome of cis-jasmone-induced resistance in Arabidopsis thaliana and its role in indirect defence. Planta 232: 1163-1180.
68. McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8: 403-416.
69. Miersch O, Neumerkel J, Dippe M, Stenzel I, Wasternack C (2008) Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling. New Phytol 177: 114-127.
70. Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem 47: 511-517.
71. Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500: 422-426.
72. Mueller S, Hilbert B, Dueckershoff K, Roitsch T, Krischke M, Mueller MJ, Berger S (2008) General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. Plant Cell 20: 768-785.
73. Nakamura Y, Mithöfer A, Kombrink E, Boland W, Hamamoto S, Uozumi N, Tohma K, Ueda M (2011) 12-hydroxyjasmonic acid glucoside is a COI1-JAZ-independent activator of leaf-closing movement in Samanea saman. Plant Physiol 155: 1226-1236.
74. Noir S, Bömer M, Takahashi N, Ishida T, Tsui T-L, Balbi V, Shanahan H, Sugimoto K, Devoto A (2013) Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol 161: 1930-1951.
75. Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H Jr, Kangasjärvi J (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12: 1849-1862.
76. Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31: 1-12.
77. Park SW, Li W, Viehhauser A, He B, Kim S, Nilsson AK, Andersson MX, Kittle JD, Ambavaram MMR, Luan S, et al (2013) Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proc Natl Acad Sci USA 110: 9559-9564.
78. Paschold A, Halitschke R, Baldwin IT (2007) Co(i)-ordinating defenses: NaCOI1 mediates herbivore- induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant J 51: 79-91.
79. Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23: 3089-3100.
80. Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184: 644-656.
81. Quintana A, Reinhard J, Faure R, Uva P, Bagnères AG, Massiot G, Clément JL (2003) Interspecific variation in terpenoid composition of defensive secretions of European Reticulitermes termites. J Chem Ecol 29: 639-652.
82. Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12: 1633-1646.
83. Restrepo MA, Freed DD, Carrington JC (1990) Nuclear transport of plant potyviral proteins. Plant Cell 2: 987-998.
84. Ribot C, Zimmerli C, Farmer EE, Reymond P, Poirier Y (2008) Induction of the Arabidopsis PHO1;H10 gene by 12-oxo-phytodienoic acid but not jasmonic acid via a CORONATINE INSENSITIVE1-dependent pathway. Plant Physiol 147: 696-706.
85. Ryu CM, Murphy JF, Mysore KS, Kloepper JW (2004) Plant growthpromoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J 39: 381-392.
86. Sánchez-Hernández C, López MG, Délano-Frier JP (2006) Reduced levels of volatile emissions in jasmonate-deficient spr2 tomato mutants favour oviposition by insect herbivores. Plant Cell Environ 29: 546-557.
87. Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12: 1041-1061.
88. Sato C, Aikawa K, Sugiyama S, Nabeta K, Masuta C, Matsuura H (2011) Distal transport of exogenously applied jasmonoyl-isoleucine with wounding stress. Plant Cell Physiol 52: 509-517.
89. Schaller A, Frasson D (2001) Induction of wound response gene expression in tomato leaves by ionophores. Planta 212: 431-435.
90. Schaller A, Ryan CA (1996) Systemin—a polypeptide defense signal in plants. BioEssays 18: 27-33.
91. Schaller A, Stintzi A (2008) Jasmonate biosynthesis and signaling for induced plant defense against herbivory. In Schaller A, ed, Induced Plant Resistance to Herbivory. Springer, Heidelberg, pp 349-365.
92. Schaller A, Stintzi A (2009) Enzymes in jasmonate biosynthesis - structure, function, regulation. Phytochemistry 70: 1532-1538.
93. Schaller F, Biesgen C, Müssig C, Altmann T, Weiler EW (2000) 12- Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210: 979-984.
94. Schuman MC, Barthel K, Baldwin IT (2012) Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature. Elife (Cambridge) 1: e00007.
95. Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, et al (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468: 400-405.
96. Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci USA 103: 16672-16676.
97. Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89: 6837-6840.
98. 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.
99. Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14: 1405-1415.
100. Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J 15: 747-754.
101. Stelmach BA, Müller A, Hennig P, Laudert D, Andert L, Weiler EW (1998) Quantitation of the octadecanoid 12-oxo-phytodienoic acid, a signalling compound in plant mechanotransduction. Phytochemistry 47: 539-546.
102. Stenzel I, Hause B, Maucher H, Pitzschke A, Miersch O, Ziegler J, Ryan CA, Wasternack C (2003) Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato - amplification in wound signalling. Plant J 33: 577-589.
103. Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97: 10625-10630.
104. Stintzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci USA 98: 12837-12842.
105. Stotz HU, Jikumaru Y, Shimada Y, Sasaki E, Stingl N, Mueller MJ, Kamiya Y (2011) Jasmonate-dependent and COI1-independent defense responses against Sclerotinia sclerotiorum in Arabidopsis thaliana: auxin is part of COI1-independent defense signaling. Plant Cell Physiol 52: 1941-1956.
106. Stotz HU, Mueller S, Zoeller M, Mueller MJ, Berger S (2013) TGA transcription factors and jasmonate-independent COI1 signalling regulate specific plant responses to reactive oxylipins. J Exp Bot 64: 963-975.
107. Stoutjesdijk PA, Singh SP, Liu Q, Hurlstone CJ, Waterhouse PA, Green AG (2002) hpRNA-mediated targeting of the Arabidopsis FAD2 gene gives highly efficient and stable silencing. Plant Physiol 129: 1723-1731.
108. Strassner J, Schaller F, Frick UB, Howe GA, Weiler EW, Amrhein N, Macheroux P, Schaller A (2002) Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound response. Plant J 32: 585-601.
109. Stumpe M, Göbel C, Faltin B, Beike AK, Hause B, Himmelsbach K, Bode J, Kramell R, Wasternack C, Frank W, et al (2010) The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. New Phytol 188: 740-749.
110. Suza WP, Staswick PE (2008) The role of JAR1 in Jasmonoyl-L: -isoleucine production during Arabidopsis wound response. Planta 227: 1221-1232.
111. Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T, et al (2005) 12-oxophytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol 139: 1268-1283.
112. Thaler JS, Farag MA, Paré PW, Dicke M (2002) Jasmonate-deficient plants have reduced direct and indirect defences against herbivores. Ecol Lett 5: 764-774.
113. Theodoulou FL, Job K, Slocombe SP, Footitt S, Holdsworth M, Baker A, Larson TR, Graham IA (2005) Jasmonic acid levels are reduced in COMATOSE ATP-binding cassette transporter mutants: implications for transport of jasmonate precursors into peroxisomes. Plant Physiol 137: 835-840.
114. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448: 661-665.
115. Tian D, Tooker J, Peiffer M, Chung SH, Felton GW (2012) Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 236: 1053-1066.
116. Tong X, Qi J, Zhu X, Mao B, Zeng L, Wang B, Li Q, Zhou G, Xu X, Lou Y, et al (2012) The rice hydroperoxide lyase OsHPL3 functions in defense responses by modulating the oxylipin pathway. Plant J 71: 763-775
117. Van Loon LC, Bakker PA, Pieterse CM (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36: 453-483
118. Van Schie CC, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64: 251-263.
119. Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castañera P, Sánchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc Natl Acad Sci USA 98: 8139-8144.
120. Vandoorn A, Bonaventure G, Rogachev I, Aharoni A, Baldwin IT (2011) JA-Ile signalling in Solanum nigrum is not required for defence responses in nature. Plant Cell Environ 34: 2159-2171.
121. Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51: 227-237.
122. Wang L, Allmann S, Wu J, Baldwin IT (2008) Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiol 146: 904-915.
123. Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot (Lond) 111: 1021-1058.
124. Wasternack C, Kombrink E (2010) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 5: 63-77.
125. Wei J, Wang L, Zhu J, Zhang S, Nandi OI, Kang L (2007) Plants attract parasitic wasps to defend themselves against insect pests by releasing hexenol. PLoS ONE 2: e852.
126. Wei J, Yan L, Ren Q, Li C, Ge F, Kang LE (2013) Antagonism between herbivore-induced plant volatiles and trichomes affects tritrophic interactions. Plant Cell Environ 36: 315-327.
127. Westfall CS, Zubieta C, Herrmann J, Kapp U, Nanao MH, Jez JM (2012) Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336: 1708-1711.
128. Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, O’Donnell PJ, Bowles DJ (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360: 62-65.
129. Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, et al (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21: 2220-2236.
130. Yerger EH, Grazzini RA, Hesk D, Cox-Foster DL, Craig R, Mumma RO (1992) A rapid method for isolating glandular trichomes. Plant Physiol 99: 1-7.
131. Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K (2009) Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development 136: 1039-1048.
132. Yoshihara T, Omer ESA, Koshino H, Sakamura S, Kikuta Y, Koda Y (1989) Structure of a tuber-inducing stimulus from potato leaves (Solanum tuberosum L.). Agric Biol Chem 53: 2835-2837.
133. Zhang Y, Turner JG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS ONE 3: e3699