Induced systemic resistance by beneficial microbes

Annual Review of Phytopathology

Volumn 52, Issue , 2014, Pages 347-375

  Pieterse, Corné M J ^a   Zamioudis, Christos ^a   Berendsen, Roeland L ^a   Weller, David M ^a,b   Van Wees, Saskia C M ^a   Bakker, Peter A H M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b US Dept Agric Agric Res Serv   (United States)

Author keywords

Defense priming; Plant growth promoting microbes; Plant immunity; Rhizosphere microbiome; Root signaling

Indexed keywords

PHYTOHORMONE;

BACTERIAL PHENOMENA AND FUNCTIONS; FUNGUS; MICROBIOLOGY; PHYSIOLOGY; PLANT;

BACTERIAL PHYSIOLOGICAL PHENOMENA; FUNGI; PLANT GROWTH REGULATORS; PLANTS;

EID: 84905500401     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-082712-102340     Document Type: Article

References (191)

1. Ahn I-P, Lee S-W, Suh S-C. 2007. Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol. Plant-Microbe Interact. 20:759-68
2. Alabouvette C, Olivain C, Migheli Q, Steinberg C. 2009. Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. New Phytol. 184:529-44
3. Alfano G, Ivey MLL, Cakir C, Bos JIB, Miller SA, et al. 2007. Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97:429-37
4. Alizadeh H, Behboudi K, Amadzadeh M, Javan-Nikkhah M, Zamioudis C, et al. 2013. Induced systemic resistance in cucumber and Arabidopsis thaliana by the combination of Trichoderma harzianum Tr6 and Pseudomonas sp. Ps14. Biol. Control 65:14-23
5. Alstr om S. 1991. Induction of disease resistance in common bean susceptible to halo blight bacterial pathogen after seed bacterization with rhizosphere pseudomonads. J. Gen. Appl. Microbiol. 37:495-501
6. Audenaert K, Pattery T, Cornelis P, H ofte M. 2002. Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol. Plant- Microbe Interact. 15:1147-56
7. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM. 2006. The role of root exudates in rhizosphere interations with plants and other organisms. Annu. Rev. Plant Biol. 57:233-66
8. Bakker PAHM, Berendsen RL, Doornbos RF, Wintermans PCA, Pieterse CMJ. 2013. The rhizospere revisited: root microbiomics. Front. Plant Sci. 4:165
9. Bakker PAHM, Ran LX, Mercado-Blanco J. 2014. Rhizobacterial salicylate production provokes headaches! Plant Soil. doi: 10.1007/s11104-014-2102-0
10. Bakker PAHM, Ran LX, Pieterse CMJ, Van Loon LC. 2003. Understanding the involvement of rhizobacteria-mediated induction of systemic resistance in biocontrol of plant diseases. Can. J. Plant Pathol. 25:5-9
11. Bardoel BW, Van der Ent S, Pel MJC, Tommassen J, Pieterse CMJ, et al. 2011. Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog. 7:e1002206
12. Beauregard PB, Chai YR, Vlamakis H, Losick R, Kolter R. 2013. Bacillus subtilis biofilm induction by plant polysaccharides. Proc. Natl. Acad. Sci. USA 110:E1621-30
13. Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, et al. 2009. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944-53
14. Benhamou N, Belanger RR, Paulitz TC. 1996. Pre-inoculation of Ri T-DNA-transformed pea roots with Pseudomonas fluorescens inhibits colonization by Pythium ultimum Trow: an ultrastructural and cytochemical study. Planta 199:105-17
15. Berendsen RL, Pieterse CMJ, Bakker PAHM. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17:478-86
16. Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379-406
17. Brotman Y, Landau U, Cuadros-Inostroza A, Takayuki T, Fernie AR, et al. 2013. Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog. 9:e1003221
18. Browse J. 2009. Jasmonate passes muster: a receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60:183-205
19. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, et al. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91-95
20. Cameron DD, Neal AL, Van Wees SCM, Ton J. 2013. Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci. 18:539-45
21. Cao H, Bowling SA, Gordon AS, Dong X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583-92
22. Cartieaux F, Contesto C, Gallou A, Desbrosses G, Kopka J, et al. 2008. Simultaneous interaction of Arabidopsis thaliana with Bradyrhizobium sp. strain ORS278 and Pseudomonas syringae pv. tomato DC3000 leads to complex transcriptome changes. Mol. Plant-Microbe Interact. 21:244-59
23. Carvalhais L, Dennis P, Badri D, Tyson G, Vivanco J, Schenk P. 2013. Activation of the jasmonic acid plant defence pathway alters the composition of rhizosphere bacterial communities. PLoS ONE 8:e56457
24. Champigny M, Shearer H, Mohammad A, Haines K, Neumann M, et al. 2011. Localization ofDIR1at the tissue, cellular and subcellular levels during systemic acquired resistance in Arabidopsis using DIR1:GUS and DIR1:EGFP reporters. BMC Plant Biol. 11:125
25. Cho I, Blaser MJ. 2012. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13:260-70
26. Chung HS, Niu Y, Browse J, Howe GA. 2009. Top hits in contemporary JAZ: an update on jasmonate signaling. Phytochemistry 70:1547-59
27. Conrath U. 2011. Molecular aspects of defence priming. Trends Plant Sci. 16:524-31
28. Conrath U, Beckers GJM, Flors V, Garca-Agustn P, Jakab G, et al. 2006. Priming: getting ready for battle. Mol. Plant-Microbe Interact. 19:1062-71
29. Contreras-CornejoHA, Macas-Rodrguez L, Beltran-Pena E, Herrera-Estrella A, L opez-Bucio J. 2011. Trichoderma-induced plant immunity likely involves both hormonal- and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal. Behav. 6:1554-63
30. Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez-Bucio J. 2009. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 149:1579-92
31. De Jonge R, Van Esse HP, Kombrink A, Shinya T, Desaki Y, et al. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953-55
32. De La Fuente L, Mavrodi D, Landa B, Thomashow L, Weller D. 2006. phlD-based genetic diversity and detection of genotypes of 2, 4-diacetylphloroglucinol-producing Pseudomonas fluorescens. FEMS Microbiol. Ecol. 56:64-78
33. De Meyer G, Capieau K, Audenaert K, Buchala A, Metraux J-P, H ofte M. 1999. Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. Mol. Plant-Microbe Interact. 12:450-58
34. DeMortel JEV, Schat H, Moerland PD, Ver Loren vanThemaat E, Van derEnt S, et al. 2008. Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 31:301-24
35. Dempsey DA, Klessig DF. 2012. SOS: too many signals for systemic acquired resistance? Trends Plant Sci. 17:538-45
36. De Vleesschauwer D, Djavaheri M, Bakker PAHM, H ofte M. 2008. Pseudomonas fluorescens WCS374r- induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiol. 148:1996-2012
37. De Vleesschauwer D, H ofte M. 2009. Rhizobacteria-induced systemic resistance. Adv. Bot. Res. 51:223-81
38. Dicke M, Baldwin IT. 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the "cry for help." Trends Plant Sci. 15:167-75
39. Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, et al. 2008. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320:942-45
40. Djavaheri M, Mercado-Blanco J, Versluis C, Meyer J-M, Van Loon LC, Bakker PAHM. 2012. Ironregulated metabolites produced by Pseudomonas fluorescensWCS374rare not required for eliciting induced systemic resistance (ISR) against Pseudomonas syringae pv. tomato in Arabidopsis. MicrobiologyOpen 1:311-25
41. Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM. 2007. A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol. 145:875-89
42. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-48
43. Dong X. 2004. NPR1, all things considered. Curr. Opin. Plant Biol. 7:547-52
44. Fan B, Carvalhais L, Becker A, Fedoseyenko D, VonWiren N, Borriss R. 2012. Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol. 12:116
45. Flors HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-96
46. Franken P. 2012. The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl. Microbiol. Biotechnol. 96:1455-64
47. Frost CJ, Mescher MC, Carlson JE, De Moraes CM. 2008. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol. 146:818-24
48. Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, et al. 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228-32
49. Green TR, Ryan CA. 1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776-77
50. Haichar F, Marol C, Berge O, Rangel-Castro J, Prosser J, et al. 2008. Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2:1221-30
51. Hammerschmidt R, Metraux J-P, Van Loon LC. 2001. Inducing resistance: a summary of papers presented at the First International Symposium on Induced Resistance to Plant Diseases, Corfu, May 2000. Eur. J. Plant Pathol. 107:1-6
52. Hase S, Takahashi S, Takenaka S, Nakaho K, Arie T, et al. 2008. Involvement of jasmonic acid signalling in bacterial wilt disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathol. 57:870-76
53. Heil M. 2009. Damaged-self recognition in plant herbivore defence. Trends Plant Sci. 14:356-63
54. Hoffland E, Pieterse CMJ, Bik L, Van Pelt JA. 1995. Induced systemic resistance in radish is not associated with accumulation of pathogenesis-related proteins. Physiol. Mol. Plant Pathol. 46:309-20
55. Hogenhout SA, Bos JIB. 2011. Effector proteins that modulate plant-insect interactions. Curr. Opin. Plant Biol. 14:422-28
56. Hossain MM, Sultana F, Kubota M, Hyakumachi M. 2008. Differential inducible defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana by plant-growth-promoting-fungus Penicillium sp. GP16-2 and its cell free filtrate. Plant Soil 304:227-39
57. Howe GA, Jander G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41-66
58. Iavicoli A, Boutet E, Buchala A, Metraux J-P. 2003. Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 16:851-58
59. Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, et al. 2011. Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol. 156:726-40
60. Jaskiewicz M, Conrath U, Peterhansel C. 2011. Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12:50-55
61. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323-29
62. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ. 2012. Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol. 38:651-64
63. Kachroo A, Robin GP. 2013. Systemic signaling during plant defense. Curr. Opin. Plant Biol. 16:527-33
64. Kloepper JW, Ryu C-M, Zhang SA. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259-66
65. Kloppholz S, Kuhn H, Requena N. 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21:1204-9
66. Knoester M, Pieterse CMJ, Bol JF, Van Loon LC. 1999. Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signaling at the site of application. Mol. Plant-Microbe Interact. 12:720-27
67. Korolev N, David DR, Elad Y. 2008. The role of phytohormones in basal resistance and Trichodermainduced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. Biocontrol 53:667-83
68. Kuc J. 1982. Induced immunity to plant disease. Bioscience 32:854-60
69. Kumar AS, Lakshmanan V, Caplan JL, Powell D, Czymmek KJ, et al. 2012. Rhizobacteria Bacillus subtilis restricts foliar pathogen entry through stomata. Plant J. 72:694-706
70. Lahrmann U, Ding Y, Banhara A, Rath M, Hajirezaei MR, et al. 2013. Host-related metabolic cues affect colonization strategies of a root endophyte. Proc. Natl. Acad. Sci. USA 110:13965-70
71. Lakshmanan V, Castaneda R, Rudrappa T, Bais HP. 2013. Root transcriptome analysis of Arabidopsis thaliana exposed to beneficial Bacillus subtilis FB17 rhizobacteria revealed genes for bacterial recruitment and plant defense independent of malate efflux. Planta 238:657-68
72. Landa BB, Mavrodi OV, Schroeder KL, Allende-Molar R, Weller DM. 2006. Enrichment and genotypic diversity of phlD-containing fluorescent Pseudomonas spp. in two soils after a century of wheat and flax monoculture. FEMS Microbiol. Ecol. 55:351-68
73. Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu CM. 2012. Induced resistance by a longchain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS ONE 7:e48744
74. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ. 2007. Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J. 50:529-44
75. Loper JE, Hassan KA, Mavrodi DV, Davis EW, Lim CK, et al. 2012. Comparative genomics of plantassociated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet. 8:e1002784
76. Lorito M, Woo SL, Harman GE, Monte E. 2010. Translational research on Trichoderma: from 'omics to the field. Annu. Rev. Phytopathol. 48:395-417
77. Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541-56
78. Luna E, Bruce TJA, Roberts MR, Flors V, Ton J. 2012. Next-generation systemic acquired resistance. Plant Physiol. 158:844-53
79. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, et al. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-90
80. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK. 2002. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399-403
81. Mark GL, Dow JM, Kiely PD, Higgins H, Haynes J, et al. 2005. Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc. Natl. Acad. Sci. USA 102:17454-59
82. Martnez-Medina A, Fernandez I, Sanchez-Guzman MJ, Jung SC, Pascual JA, Pozo MJ. 2013. Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front. Plant Sci. 4:206
83. Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B, et al. 2012. Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front. Plant Sci. 3:108
84. Matilla M, Espinosa-Urgel M, Rodriguez-Herva J, Ramos J, Ramos-Gonzalez M. 2007. Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol. 8:R179
85. Maurhofer M, Reimmann C, Schmidli-Sacherer P, Heeb SD, Defago G. 1998. Salicylic acid biosynthesis genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology 88:678-84
86. Mavrodi DV, Joe A, Mavrodi OV, Hassan KA, Weller DM, et al. 2011. Structural and functional analysis of the type III secretion system from Pseudomonas fluorescens Q8r1-96. J. Bacteriol. 193:177-89
87. Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM. 2009. Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J. 3:977-91
88. Memelink J. 2009. Regulation of gene expression by jasmonate hormones. Phytochemistry 70:1560-70
89. Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van der VoortM, et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097-100
90. Meziane H, Van der Sluis I, Van Loon LC, Hofte M, Bakker PAHM. 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Pathol. 6:177-85
91. Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, et al. 2010. Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973-90
92. Mishina TE, Zeier J. 2006. The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol. 141:1666-75
93. Mishina TE, Zeier J. 2007. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50:500-13
94. Mith ofer A, Boland W. 2008. Recognition of herbivory-associated molecular patterns. Plant Physiol. 146:825-31
95. Mortier V, Holsters M, Goormachtig S. 2012. Never too many? How legumes control nodule numbers. Plant Cell Environ. 35:245-58
96. Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. 2013. GLUTAMATE RECEPTORLIKE genes mediate leaf-to-leaf wound signalling. Nature 500:422-26
97. Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM. 2013. Trichoderma research in the genome era. Annu. Rev. Phytopathol. 51:105-29
98. Neal AL, Ahmad S, Gordon-Weeks R, Ton J. 2012. Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS ONE 7:e35498
99. Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M. 2013. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 4:2191
100. Oldroyd GED, Harrison MJ, Paszkowski U. 2009. Reprogramming plant cells for endosymbiosis. Science 324:753-54
101. Ortiz-Castro R, Diaz-Perez C, Martinez-Trujillo M, del Rio RE, Campos-Garcia J, Lopez-Bucio J. 2011. Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc. Natl. Acad. Sci. USA 108:7253-58
102. Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS. 2013. Tell me more: roles of NPRs in plant immunity. Trends Plant Sci. 18:402-11
103. Palmer CM, Hindt MN, Schmidt H, Clemens S, Guerinot ML. 2013. MYB10 and MYB72 are required for growth under iron-limiting conditions. PLoS Genet. 9:e1003953
104. Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V. 2013. Primed plants do not forget. Environ. Exp. Bot. 94:46-56
105. Pauwels L, Goossens A. 2011. The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089-100
106. Pearce G, Strydom D, Johnson S, Ryan CA. 1991. A polypeptide from tomato leaves induces woundinducible proteinase inhibitor proteins. Science 253:895-97
107. Pedrotti L, Mueller MJ, Waller F. 2013. Piriformospora indica root colonization triggers local and systemic root responses and inhibits secondary colonization of distal roots. PLoS ONE 8:e69352
108. Peiffer J, Spor A, Koren O, Jin Z, Tringe S, et al. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci. USA 110:6548-53
109. Pel MJC, Pieterse CMJ. 2013. Microbial recognition and evasion of host immunity. J. Exp. Bot. 64:1237-48
110. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. 2013. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11:789-99
111. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. 2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489-521
112. Pieterse CMJ, Van Pelt JA, Ton J, Parchmann S, Mueller MJ, et al. 2000. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiol. Mol. Plant Pathol. 57:123-34
113. Pieterse CMJ, Van Wees SCM, Hoffland E, Van Pelt JA, Van Loon LC. 1996. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesisrelated gene expression. Plant Cell 8:1225-37
114. Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, et al. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-80
115. Pineda A, Dicke M, Pieterse CMJ, Pozo MJ. 2013. Beneficial microbes in a changing environment: Are they always helping plants to deal with insects? Funct. Ecol. 27:574-86
116. Pineda A, Zheng S-J, Van Loon JJA, Pieterse CMJ, Dicke M. 2010. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci. 15:507-14
117. Plett JM, Kemppainen M, Kale SD, Kohler A, Legue V, et al. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr. Biol. 21:1197-203
118. Pozo MJ, Azcon-Aguilar C. 2007. Unraveling mycorrhiza-induced resistance. Curr. Opion Plant Biol. 10:393-98
119. Pozo MJ, Van der Ent S, Van Loon LC, Pieterse CMJ. 2008. Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol. 180:511-23
120. Press CM, Wilson M, Tuzun S, Kloepper JW. 1997. Salicylic acid produced by Serratiamarcescens 91-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol. Plant-Microbe Interact. 10:761-68
121. Raaijmakers JM, Leeman M, Van Oorschot MMP, Van der Sluis I, Schippers B, Bakker PAHM. 1995. Dose-response relationships in biological control of Fusarium wilt of radish by Pseudomonas spp. Phytopathology 85:1075-81
122. Ramirez V, Van der Ent S, Garcia-Andrade J, Coego A, Pieterse CMJ, Vera P. 2010. OCP3 is an important modulator of NPR1-mediated jasmonic acid-dependent induced defenses in Arabidopsis. BMC Plant Biol. 10:199
123. Ran LX, Van Loon LC, Bakker PAHM. 2005. No role for bacterially produced salicylic acid in rhizobacterial induction of systemic resistance in Arabidopsis. Phytopathology 95:1349-55
124. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, et al. 2012. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol. 158:854-63
125. Reinhold-Hurek B, Hurek T. 2011. Living inside plants: bacterial endophytes. Curr. Opin. Plant Biol. 14:435-43
126. Ross AF. 1961. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340-58
127. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA 95:9750-54
128. Rudrappa T, Czymmek KJ, Pare PW, Bais HP. 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol. 148:1547-56
129. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner H-Y, Hunt MD. 1996. Systemic acquired resistance. Plant Cell 8:1808-19
130. Ryu C-M, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134:1017-26
131. RyuC-M, HuC-H, Reddy MS, Kloepper JW. 2003. Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytol. 160:413-20
132. Ryu C-M, Murphy JF, Mysore KS, Kloepper JW. 2004. Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J. 39:381-92
133. Segarra G, Van der Ent S, Trillas I, Pieterse CMJ. 2009. MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol. 11:90-96
134. Shah J, Zeier J. 2013. Long-distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci. 4:30
135. Shoresh M, Gal-On A, Leibman D, Chet I. 2006. Characterization of a mitogen-activated protein kinase gene from cucumber required for Trichoderma-conferred plant resistance. Plant Physiol. 142:1169-79
136. Shoresh M, Harman GE, Mastouri F. 2010. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 48:21-43
137. Shoresh M, Yedidia I, Chet I. 2005. Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76-84
138. Slaughter A, Daniel X, Flors V, Luna E, Hohn B, Mauch-Mani B. 2012. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158:835-43
139. Spoel SH, Dong X. 2012. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12:89-100
140. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, et al. 2003. NPR1 modulates crosstalk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760-70
141. Spoel SH, Mou ZL, Tada Y, Spivey NW, Genschik P, Dong X. 2009. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860-72
142. Staehelin C, Xie ZP, Illana A, Vierheilig H. 2011. Long-distance transport of signals during symbiosis: Are nodule formation and mycorrhization autoregulated in a similar way? Plant Signal. Behav. 6:372-77
143. Stein E, Molitor A, Kogel KH, Waller F. 2008. Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol. 49:1747-51
144. Sun JQ, Jiang HL, Li CY. 2011. Systemin/jasmonate-mediated systemic defense signaling in tomato. Mol. Plant 4:607-15
145. Thomma BPHJ, Penninckx IAMA, Broekaert WF, Cammue BPA. 2001. The complexity of disease signaling in Arabidopsis. Curr. Opin. Immunol. 13:63-68
146. Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, et al. 2013. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc. Natl. Acad. Sci. USA 110:20117-22
147. Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P. 2005. Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol. Plant-Microbe Interact. 18:555-61
148. Ton J, Davison S, Van Wees SCM, Van Loon LC, Pieterse CMJ. 2001. The Arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signaling. Plant Physiol. 125:652-61
149. Ton J, Jakab G, Toquin V, Flors V, Iavicoli A, et al. 2005. Dissecting the-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:987-99
150. Ton J, Pieterse CMJ, Van Loon LC. 1999. Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Mol. Plant-Microbe Interact. 12:911-18
151. Ton J, Van Pelt JA, Van Loon LC, Pieterse CMJ. 2002. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol. Plant-Microbe Interact. 15:27-34
152. Van de Mortel JE, De Vos RCH, Dekkers E, Pineda A, Guillod L, et al. 2012. Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160:2173-88
153. Van der Ent S, Van Hulten MHA, Pozo MJ, Czechowski T, Udvardi MK, et al. 2009. Priming of plant innate immunity by rhizobacteria and-aminobutyric acid: differences and similarities in regulation. New Phytol. 183:419-31
154. Van der Ent S, Van Wees SCM, Pieterse CMJ. 2009. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581-88
155. Van der Ent S, Verhagen BWM, Van Doorn R, Bakker D, Verlaan MG, et al. 2008. MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol. 146:1293-304
156. 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 103:5602-7
157. Van Loon LC, Bakker PAHM. 2005. Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In PGPR: Biocontrol and Biofertilization, ed. ZA Siddiqui, pp. 39-66. Dordrecht, Neth.: Springer
158. Van Loon LC, Bakker PAHM. 2006. Root-associated bacteria inducing systemic resistance. In Plant- Associated Bacteria, ed. SS Gnanamanickam, pp. 269-316. Dordrecht, Neth.: Springer
159. Van Loon LC, Bakker PAHM, Pieterse CMJ. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-83
160. Van Loon LC, Rep M, Pieterse CMJ. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135-62
161. Van Oosten VR, Bodenhausen N, Reymond P, Van Pelt JA, Van Loon LC, et al. 2008. Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol. Plant- Microbe Interact. 21:919-30
162. Van Peer R, Niemann GJ, Schippers B. 1991. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728-34
163. Van Wees SCM, De Swart EAM, Van Pelt JA, Van Loon LC, Pieterse CMJ. 2000. Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97:8711-16
164. Van Wees SCM, Luijendijk M, Smoorenburg I, Van Loon LC, Pieterse CMJ. 1999. Rhizobacteriamediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol. Biol. 41:537-49
165. Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van 't Westende YAM, Hartog F, Van Loon LC. 1997. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol. Plant-Microbe Interact. 10:716-24
166. Van Wees SCM, Van der Ent S, Pieterse CMJ. 2008. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11:443-48
167. Vargas WA, Crutcher FK, Kenerley CM. 2011. Functional characterization of a plant-like sucrose transporter from the beneficial fungus Trichoderma virens. Regulation of the symbiotic association with plants by sucrose metabolism inside the fungal cells. New Phytol. 189:777-89
168. Vargas WA, Mandawe JC, Kenerley CM. 2009. Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol. 151:792-808
169. Verhagen BWM, Glazebrook J, Zhu T, Chang H-S, Van Loon LC, Pieterse CMJ. 2004. The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol. Plant-Microbe Interact. 17:895-908
170. Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar R, et al. 1994. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959-65
171. Vlot AC, Dempsey DA, Klessig DF. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177-206
172. Vos IA, Pieterse CMJ, Van Wees SCM. 2013. Costs and benefits of hormone-regulated plant defences. Plant Pathol. 62:43-55
173. Vos IA, Verhage A, Schuurink RC, Watt LG, Pieterse CMJ, Van Wees SCM. 2013. Onset of herbivoreinduced resistance in systemic tissue primed for jasmonate-dependent defenses is activated by abscisic acid. Front. Plant Sci. 4:539
174. Walters DR, Paterson L, Walsh DJ, Havis ND. 2008. Priming for plant defense in barley provides benefits only under high disease pressure. Physiol. Mol. Plant Pathol. 73:95-100
175. Walters DR, Ratsep J, Havis ND. 2013. Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64:1263-80
176. Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, et al. 2012. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22:2242-46
177. Wang YQ, Ohara Y, Nakayashiki H, Tosa Y, Mayama S. 2005. Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol. Plant-Microbe Interact. 18:385-96
178. 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. 111:1021-58
179. Wei G, Kloepper JW, Tuzun S. 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant-growth promoting rhizobacteria. Phytopathology 81:1508-12
180. Weller DM, Landa BB, Mavrodi OV, Schroeder KL, De La Fuente L, et al. 2007. Role of 2, 4- diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biol. 9:4-20
181. Weller DM, Mavrodi DV, Van Pelt JA, Pieterse CMJ, Van Loon LC, Bakker PAHM. 2012. Induced systemic resistance (ISR) in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2, 4- diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102:403-12
182. Weller DM, Raaijmakers JM, McSpadden Gardener BB, Thomashow LS. 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40:309-48
183. Wu J, Baldwin IT. 2010. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44:1-24
184. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, et al. 2012. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 1:639-47
185. Yan Z, Reddy MS, Ryu C-M, McInroy JA, Wilson M, Kloepper JW. 2002. Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92:1329-33
186. Yang S, Tang F, Gao MQ, Krishnan HB, Zhu HY. 2010. R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc. Natl. Acad. Sci. USA 107:18735-40
187. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ. 2013. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol. 162:304-18
188. Zamioudis C, Pieterse CMJ. 2012. Modulation of host immunity by beneficial microbes. Mol. Plant- Microbe Interact. 25:139-50
189. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, et al. 2007. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839-51
190. Zipfel C. 2009. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12:414-20
191. Zuccaro A, Lahrmann U, Guldener U, Langen G, Pfiffi S, et al. 2011. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. 7:e1002290