Airborne induction and priming of plant defenses against a bacterial pathogen

Plant Physiology

Volumn 151, Issue 4, 2009, Pages 2152-2161

  Yi, Hwe Su ^a,b   Heil, Martin ^c   Adame Álvarez, Rosa M ^c   Ballhorn, Daniel J ^d   Ryu, Choong Min ^a,e  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Kyungpook National University   (South Korea)

^c Departamento de Ingenieríán y de Estudios Avanzados Irapuato   (Mexico)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e University of Science and Technology (UST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); PHASEOLUS LUNATUS; PSEUDOMONAS SYRINGAE;

EID: 71049139323     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.109.144782     Document Type: Article

References (70)

1. Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221: 277-279
2. Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol 96: 971-980
3. Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hasch R, Polle A, Bohlmann J, Schnitzler JP (2007) Transgenic, non-isoprene emitting poplars don't like it hot. Plant J 51: 485-499
4. Birkett MA, Campbell CA, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Pettersson J, Pickett JA, et al (2000) New roles for cisjasmone as an insect semiochemical and in plant defense. Proc Natl Acad Sci USA 97: 9329-9334
5. Birkett MA, Chamberlain K, Guerrieri E, Pickett JA, Wadhams LJ, Yasuda T (2003) Volatiles from whitefly-infested plants elicit a host-locating response in the parasitoid, Encarsia formosa. J Chem Ecol 29: 1589-1600
6. Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful "memories" of plants: evidence and possible mechanisms. Plant Sci 173: 603-608
7. Cools HJ, Ishii H (2002) Pre-treatment of cucumber plants with acibenzolar-S-methyl systemically primes a phenylalanine ammonia lyase gene (PAL1) for enhanced expression upon attack with a pathogenic fungus. Physiol Mol Plant Pathol 61: 273-280
8. de Lacy Costello BPJ, Evans P, Ewen RJ, Gunson HE, Jones PRH, Ratcliffe NM, Spencer-Phillips PTN (2001) Gas chromatography-mass spec-trometry analyses of volatile organic compounds from potato tubers inoculated with Phytophthora infestans or Fusarium coeruleum. Plant Pathol 50: 489-496
9. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbi-vore-infested plants selectively attract parasitoids. Nature 393: 570-573
10. De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410: 577-580
11. Dilantha Fernando WG, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37: 955-964
12. Donath J, Boland W (1995) Biosynthesis of acyclic homoterpenes: enzyme selectivity and absolute configuration of the nerolidol precursor. Phy-tochemistry 39: 785-790
13. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185-209
14. Edington B, Lamb C, Dixon R (1991) cDNA cloning and characterization of a putative 1,3-beta-D-glucanase transcript induced by fungal elicitor in bean cell suspension cultures. Plant Mol Biol 16: 81-94
15. 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
16. Farag MA, Fokar M, Zhang HA, Allen RD, Paré PW (2005) (Z)-3-Hexenol induces defense genes and downstream metabolites in maize. Planta 220: 900-909
17. Farmer EE, Alméras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6: 372-378
18. Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, et al (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci USA 102: 1773-1778
19. Francia D, Demaria D, Calderini O, Ferraris L, Valentino D, Arcioni S, Tamietti G, Cardinale F (2007) Wounding induces resistance to pathogens with different lifestyles in tomato: role of ethylene in cross-protection. Plant Cell Environ 30: 1357-1365
20. Frost C, Appel H, Carlson J, De Moraes C, Mescher M, Schultz J (2007) Within-plant signalling by volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10: 490-498
21. Godard KA, White R, Bohlmann J (2008) Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69: 1838-1849
22. Hammerschmidt R, Smith-Becker JA (1999) The role of salicylic acid in disease resistance. In AA Agrawal, S Tuzun, E Bent, eds, Induced Plant Defenses against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture. American Phytopathological Society Press, St. Paul, pp 37-53
23. Heil M (2004) Induction of two indirect defences benefits lima bean (Phaseolus lunatus, Fabaceae) in nature. J Ecol 92: 527-536 Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178: 41-61
24. Heil M, Baldwin IT (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7: 61-67
25. Heil M, Kost C (2006) Priming of indirect defences. Ecol Lett 9: 813-817
26. Heil M, Lion U, Boland W (2008) Defence-inducing volatiles: in search for the active motif. J Chem Ecol 34: 601-604
27. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104: 5467-5472
28. Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13: 264-272
29. Huang HC, Schuurink R, Denny TP, Atkinson MM, Baker CJ, Yucel I, Hutcheson SW, Collmer A (1988) Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonas fluorescens to elicit the hypersensitive response in tobacco plants. J Bacteriol 170: 4748-4756
30. Hunt MD, Ryals JA (1996) Systemic acquired resistance signal transduc-tion. Crit Rev Plant Sci 15: 583-606
31. Chicago Karban R, Shiojiri K, Huntzinger M, McCall AC (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87: 922-930
32. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141-2144
33. Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148: 280-292
34. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46: 1093-1102
35. Kohler A, Schwindling S, Conrath U (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128: 1046-1056
36. Korneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146: 839-844
37. Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94: 619-628
38. Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci USA 100: 16101-16106
39. Maffei ME, Mithofer A, Arimura G, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS, Novero M, Volpe V, Quadro S, et al (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 140: 1022-1035
40. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403-410
41. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9: 274-280
42. Meier B, Shaw N, Slusarenko A (1993) Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell death. Mol Plant Microbe Interact 6: 453-466
43. Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylides C, Haring MA, Schuurink RC (2008) The Arabidopsis her1 mutant impli-cates GABA in E-2-hexenal responsiveness. Plant J 53: 197-213
44. Nakamura S, Hatanaka A (2002) Green-leaf-derived C6-aroma compounds with potent antibacterial action that act on both gram-negative and gram-positive bacteria. J Agric Food Chem 50: 7639-7644
45. Ongena M, Duby F, Rossignol F, Fauconnier ML, Dommes J, Thonart P (2004) Stimulation of the lipoxygenase pathway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Mol Plant Microbe Interact 17: 1009-1018
46. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resis-tance. Science 318: 113-116
47. Paschold A, Halitschke R, Baldwin IT (2006) Using 'mute' plants to translate volatile signals. Plant J 45: 275-291
48. Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12: 564-569
49. Pieterse CMJ, van Wees SCM, van Pelt JA, Knoester M, Laan R, Gerrits N, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10: 1571-1580
50. Rhoades DF (1983) Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. In PA Hedin, ed, Plant Resistance to Insects. American Chem-ical Society, Washington, DC, pp 55-68
51. RostÁs M, Turlings TCJ (2008) Induction of systemic acquired resistance in Zea mays also enhances the plant's attractiveness to parasitoids. Biol Control 46: 178-186
52. 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: 2217-2222
53. Ryu CM, Anand A, Kang L, Mysore KS (2004a) Agrodrench: a novel and effective agroinoculation method for virus-induced gene silencing in roots and diverse solanaceous species. Plant J 40: 322-331
54. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004b) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134: 1017-1026
55. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100: 4927-4932
56. Schilmiller AL, Howe GA (2005) Systemic signaling in the wound re-sponse. Curr Opin Plant Biol 8: 369-377
57. 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
58. Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385: 718-721
59. Thaler JS (1999) Jasmonate-inducible plant defences cause increased par-asitism of herbivores. Nature 399: 686-688
60. Ton J, D'Allesandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49: 16-26
61. Truman W, Bennettt MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 104: 1075-1080
62. Tscharntke T, Thiessen S, Dolch R, Boland W (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Syst Ecol 29: 1025-1047
63. Turlings TCJ, Loughrin JH, McCall PJ, Rose USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 92: 4169-4174
64. van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103: 5602-5607
65. van Loon LC (1997) Induced resistance in plants and the role of pathogen-esis-related proteins. Eur J Plant Pathol 103: 753-765
66. Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71: 3-17
67. Walters DR, Boyle C (2005) Induced resistance and allocation costs: what is the impact of pathogen challenge? Physiol Mol Plant Pathol 66: 40-44
68. Walters DR, Cowley T, Weber H (2006) Rapid accumulation of trihydroxy oxylipins and resistance to the bean rust pathogen Uromyces fabae following wounding in Vicia faba. Ann Bot (Lond) 97: 779-784
69. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal trans-duction and action in plant stress response, growth and development. Ann Bot (Lond) 100: 681-697
70. Wasternack C, Parthier B (1997) Jasmonate-signalled plant gene expres-sion. Trends Plant Sci 2: 302-307