Skip to main content
SpringerLink
Log in

Plant Growth-Promoting Microbial-Mediated Induced Systemic Resistance in Plants: Induction, Mechanism, and Expression

  • Chapter
  • First Online:
Microbial-mediated Induced Systemic Resistance in Plants

Abstract

In the agroecosystem, plants are an attractive source of nutrients and life environment for many microbes. Pathogenic as well as nonpathogenic microbes get colonized to the plants resulting in various diseases and beneficial effects on plant growth or stress resistance, respectively. Plants are generally resistant to the majority of phytopathogens due to the presence of an efficient and complex immune system which is able to deal with most microbial invaders ubiquitously present in the environment. Plant growth-promoting microbes (PGPMs) elicit a higher level of resistance in addition to an indigenous immune system in the form of induced systemic resistance in plants and provide a heightened level of protection. Induced systemic resistance is a pre-activated induced resistance in plants leading to defense-related protein activation which is independent of salicylic acid and dependent on jasmonic acid and ethylene. Nonexpressor of pathogenesis-related protein 1 (NPR1) works as a master regulator of hormonal defense signaling pathway leading to activation of pathogenesis-related and defense-related protein that depends on the preceding signals. This chapter focuses on recent research study concerning interaction between PGPMs and plants under biotic stress condition.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  • Agrios GN (1988) Plant pathology, 3rd edn. Academic, San Diego

    Google Scholar 

  • Ahl Goy P, Felix G, Metraux JP, Meins JR (1992) Resistance to disease in the hybrid Nicotiana glutinosa × Nicotiana debneyi is associated with high constitutive levels of β-1,3-glucanase, chitinase, peroxidase and polyphenol oxidase. Physiol Mol Plant Pathol 41:11–21

    Google Scholar 

  • 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 20:759–768

    CAS  PubMed  Google Scholar 

  • Attaran E, Zeier TE, Griebel T, Zeier J (2009) Systemic acquired resistance in Arabidopsis is independent of methyl salicylate production and jasmonate signaling. Plant Cell 21:954–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    CAS  PubMed  Google Scholar 

  • Berger S, Bell E, Sadka A, Mullet JE (1995) Arabidopsis thaliana AtVsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol Biol 27:933–942

    CAS  PubMed  Google Scholar 

  • Bezemer TM, van Dam NM (2005) Linking above-ground and below ground interactions via induced plant defenses. Trends Ecol Evol 20:617–624

    PubMed  Google Scholar 

  • Boller T (1991) Ethylene in pathogenesis and disease resistance. In: Mattoo AK, Suttle JC (eds) The plant hormone ethylene. CRC Press, Boca Raton, pp 293–314

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Borges AA, Sandalio LM (2015) Induced resistance for plant defense. Front Plant Sci 6:109. doi:10.3389/fpls.2015.00109

    Article  PubMed  PubMed Central  Google Scholar 

  • Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P et al (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464:418–422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren Van The maat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    CAS  PubMed  Google Scholar 

  • Burketová L, Trdá L, Ott P, Valentova O (2015) Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnol Adv. doi:10.1016/j.biotechadv.2015.01.004

    Article  PubMed  Google Scholar 

  • Cavalcanti FR, Oliveira JTA, Martins-Miranda AS, Vie’gas RA, Silveira JAG (2004) Superoxide dismutase, catalase and peroxidase activities do not confer protection against oxidative damage in salt stressed cowpea leaves. New Phytol 163:563–571

    CAS  PubMed  Google Scholar 

  • Chen C, Bélanger RR, Benhamou N, Paulitz T (2000) Defense enzymes induced in cucumber roots by treatment with plant growth promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiol Mol Plant Pathol 56:13–23

    CAS  Google Scholar 

  • Chen YC, Kidd BN, Carvalhais LC, Schenk PM (2014) Molecular defense responses in roots and the rhizosphere against Fusarium oxysporum. Plant Signal Behav 9(12):e977710. doi:10.4161/15592324.2014.977710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chunhua S, Ya D, Bingle X, Xiao L, Yonshu X, Qinguang L (2001) The purification and spectral properties of PPO I from Nicotianan tababcum. Plant Mol Biol 19:301–314

    Google Scholar 

  • Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531

    CAS  PubMed  Google Scholar 

  • Constabel CP, Ryan CA (1998) A survey of wound- and methyl jasmonate-induced polyphenol oxidase in crop plants. Phytochemistry 47:507–511

    CAS  Google Scholar 

  • Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381

    CAS  PubMed  Google Scholar 

  • Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE, Ausubel FM (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci U S A 102:1791–1796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daayf F, Bel–Rhlid R, Bélanger RR (1997) Methyl ester of p-coumaric acid: a phytoalexin-like compound from long English cucumber leaves. J Chem Ecol 23:1517–1526

    CAS  Google Scholar 

  • 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 329:953–955

    PubMed  Google Scholar 

  • De Meyer G, Capieau K, Audenaert K, Buchala A, Metraux JP, Höfte 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 12:450–458

    PubMed  Google Scholar 

  • De Vleesschauwer D, Djavaheri M, Bakker PAHM, Höfte 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

    PubMed  PubMed Central  Google Scholar 

  • Dempsey DA, Klessig DF (2012) SOS: too many signals for systemic acquired resistance? Trends Plant Sci 17:538–545

    CAS  PubMed  Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the cry for help. Trends Plant Sci 15:167–175

    CAS  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548

    CAS  PubMed  Google Scholar 

  • Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552

    CAS  PubMed  Google Scholar 

  • Duijff BJ, Pouhair D, Olivain C, Alabouvette C, Lemanceau P (1998) Implication of systemic induced resistance in the suppression of fusarium wilt of tomato by Pseudomonas fluorescens WCS417r and by nonpathogenic Fusarium oxysporum Fo47. Eur J Plant Pathol 104:903–910

    Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    CAS  PubMed  Google Scholar 

  • Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol 109:813–820

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    CAS  PubMed  Google Scholar 

  • Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134

    CAS  PubMed  PubMed Central  Google Scholar 

  • Farmer EE, Johnson RR, Ryan CA (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol 98:995–1002

    CAS  PubMed  PubMed Central  Google Scholar 

  • Felton GW, Korth KL (2000) Trade-offs between pathogen and herbivore resistance. Curr Opin Plant Biol 3:309–314

    CAS  PubMed  Google Scholar 

  • Feys BJ, Parker JE (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet 16:449–455

    CAS  PubMed  Google Scholar 

  • Flors HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296

    Google Scholar 

  • Gao Q-M, Zhu S, Kachroo P, Kachroo A (2015) Signal regulators of systemic acquired resistance. Front Plant Sci 6:228. doi:10.3389/fpls.2015.00228

    Article  PubMed  PubMed Central  Google Scholar 

  • Gehring C, Bennett A (2009) Mycorrhizal fungal–plant–insect interactions: the importance of a community approach. Environ Entomol 38:93–102

    PubMed  Google Scholar 

  • Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis: 2001 status. Curr Opin Plant Biol 4:301–308

    CAS  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    CAS  PubMed  Google Scholar 

  • Hammerschmidt R (1999) Induced disease resistance: how do induced plants stop pathogens? Physiol Mol Plant Pathol 55:77–84

    CAS  Google Scholar 

  • Hase S, Takahashi S, Takenaka S, Nakaho K, Arie T, Seo S, Ohashi Y, Takahashi H (2008) Involvement of jasmonic acid signalling in bacterial wilt disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathol 57:870–876

    CAS  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signalling in plant defense. Trends Plant Sci 13:264–272

    CAS  PubMed  Google Scholar 

  • Heitz T, Geoffroy P, Fritig B, Legrand M (1999) The PR-6 family: proteinase inhibitors in plant-microbe and plant-insects interactions. In: Datta SK, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC Press, Boca Raton, pp 131–155

    Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants-to grow or defend. Q Rev Biol 67:283–335

    Google Scholar 

  • 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 46:309–320

    CAS  Google Scholar 

  • 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 304:227–239

    CAS  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    CAS  PubMed  Google Scholar 

  • Iavicoli A, Boutet E, Buchala A, Métraux J-P (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant-Microbe Interact 16:851–858

    CAS  PubMed  Google Scholar 

  • Jain S, Choudhary DK (2014) Induced defense‑related proteins in soybean (Glycine max L. Merrill) plants by Carnobacterium sp. SJ‑5 upon challenge inoculation of Fusarium oxysporum. Planta. doi:10.1007/s00425-014-2032-3

    Article  PubMed  Google Scholar 

  • Jain S, Vaishnav A, Kasotia A, Kumari S, Gaur RK, Choudhary DK (2013) Rhizobacterium-mediated growth promotion and expression of stress enzymes in Glycine max L. Merrill against Fusarium wilt upon challenge inoculation. World J Microbiol Biotechnol. doi:10.1007/s11274-013-1455-5

    Article  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    CAS  PubMed  Google Scholar 

  • Katayama N, Zhang ZQ, Ohgushi T (2011) Community-wide effects of below-ground rhizobia on above-ground arthropods. Ecol Entomol 36:43–51

    Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885–886

    CAS  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang SA (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    CAS  PubMed  Google Scholar 

  • Kombrink E, Somssich IE (1997) Pathogenesis-related proteins and plant defense. In: Carroll G, Tudzynski P (eds) The mycota V. Part A. Plant relationships. Springer, Berlin, pp 107–128

    Google Scholar 

  • Król P, Igielski R, Pollmann S, KÄ™pczyÅ„ska E (2015) Priming of seeds with methyl jasmonate induced resistance to hemi-biotroph Fusarium oxysporum f.sp. lycopersici in tomato via 12-oxo-phytodienoic acid, salicylic acid, and flavonol accumulation. J Plant Physiol 179:122–132

    PubMed  Google Scholar 

  • Ku’c J (1982) Induced immunity to plant disease. BioScience 32:854–860

    Google Scholar 

  • Kuai X, MacLeod BJ, Després C (2015) Integrating data on the Arabidopsis NPR1/NPR3/NPR4 salicylic acid receptors; a differentiating argument. Front Plant Sci 6:235. doi:10.3389/fpls.2015.00235

    Article  PubMed  PubMed Central  Google Scholar 

  • Leitner M, Kaiser R, Hause B, Boland W, Mithofer A (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101

    PubMed  Google Scholar 

  • Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RAM, Ritsema T, Pieterse CMJ (2009) Ethylene modulates the role of NPR1 in cross-talk between salicylate and jasmonate signaling. Plant Physiol 149:1797–1809

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liang X, Dron M, Schmid J, Dixon R, Lamb C (1989) Developmental and environmental regulation of a phenylalanine ammonia-lyase-b-glucuronidase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci 86:9284–9288

    CAS  PubMed  PubMed Central  Google Scholar 

  • Loake G, Grant M (2007) Salicylic acid in plant defence-the players and protagonists. Curr Opin Plant Biol 10:466–472

    CAS  PubMed  Google Scholar 

  • Mauch-Mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203–212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mayer AM, Harel E (1979) Polyphenol oxidases in plants. Phytochemistry 18:193–215

    CAS  Google Scholar 

  • McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci U S A 94:5473–5477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mendes R, Kruijt M, DeBruijn I, Dekkers E, Van Der Voort M, Schneider JHM et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100

    CAS  PubMed  Google Scholar 

  • Mohan R, Vijayan P, Kolattukudy PE (1993) Developmental and tissue specific expression of a tomato anionic peroxidase (tap1) gene by a minimal promoter with wound and pathogen induction by an additional 5′-flanking region. Plant Mol Biol 22:475–490

    CAS  PubMed  Google Scholar 

  • Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:139

    PubMed  PubMed Central  Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Ann Rev Ecol Evol Syst 36:81–105

    Google Scholar 

  • Paparu P, Dubois T, Coyne D, Viljoen A (2007) Defense-related gene expression in susceptible and tolerant bananas (Musa spp.) following inoculation with nonpathogenic Fusarium oxysporum endophytes and challenge with Radopholus similis. Physiol Mol Plant Pathol 71:149–157

    CAS  Google Scholar 

  • Park S-W, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116

    CAS  PubMed  Google Scholar 

  • Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265

    CAS  PubMed  Google Scholar 

  • Pel MJC, Pieterse CMJ (2013) Microbial recognition and evasion of host immunity. J Exp Bot 64:1237–1248

    CAS  PubMed  Google Scholar 

  • Penninckx IAMA, Eggermont K, Terras FRG, Thomma BPHJ, De Samblanx GW, Buchala A, Métraux J-P, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Penninckx IAMA, Thomma BPHJ, Buchala A, Métraux J-P, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, Van Loon LC (1999) Salicylic acid-independent plant defence pathways. Trends Plant Sci 4:52–58

    CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7:456–464

    CAS  PubMed  Google Scholar 

  • 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 pathogenesis-related gene expression. Plant Cell 8:1225–1237

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, van Wees SCM, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signalling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, Ton J, Van Loon LC (2001) Cross-talk between plant defence signalling pathways: boost or burden? Ag Biotech Net 3:1–8

    Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    CAS  PubMed  Google Scholar 

  • Pineda A, Zheng SJ, Van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514

    CAS  PubMed  Google Scholar 

  • Pineda A, Soler R, Weldegergis BT, Shimwela MM, VAN Loon JJ, Dicke M (2013) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via Jasmonic acid signaling. Plant Cell Environ 36:393–404

    CAS  PubMed  Google Scholar 

  • Planchamp C, Glauser G, Mauch-Mani B (2014) Root inoculation with Pseudomonas putida KT2440 induces transcriptional and metabolic changes and systemic resistance in maize plants. Front Plant Sci 5:719. doi:10.3389/fpls.2014.00719

    Article  PubMed  Google Scholar 

  • Potter S, Uknes S, Lawton K, Winter AM, Chandler D, DiMaio J, Novitzky R, Ward E, Ryals J (1993) Regulation of a hevein-like gene in Arabidopsis. Mol Plant-Microbe Interact 6:680–685

    CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opion Plant Biol 10:393–398

    CAS  Google Scholar 

  • Press CM, Wilson M, Tuzun S, Kloepper JW (1997) Salicylic acid produced by Serratia marcescens 91-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol Plant-Microbe Interact 10:761–768

    CAS  Google Scholar 

  • Ramamoorthy V, Raguchander T, Samiyappan R (2002) Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. Plant Soil 239:55–68

    CAS  Google Scholar 

  • Ramanathan A, Samiyappan R, Vidhyasekaran P (2000) Induction of defense mechanisms in greengram leaves and suspension cultured cells by Macrophomina phaseolina and its elicitors. J Plant Dis Protect 107:245–257

    CAS  Google Scholar 

  • Reimers PJ, Guo A, Leach JE (1992) Increased activity of a cationic peroxidase associated with an incompatible interaction between Xanthomonas oryzae pv. oryzae and rice (Oryza sativa). Plant Physiol 99:1044–1050

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411

    CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343

    CAS  PubMed  Google Scholar 

  • Rosahl S (1996) Lipoxygenases in plants: their role in development and stress response. Z Naturforsch C 51:123–138

    CAS  PubMed  Google Scholar 

  • Ross AF (1961) Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340–358

    CAS  PubMed  Google Scholar 

  • Ryu C-M, Hu C-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 160:413–420

    CAS  PubMed  Google Scholar 

  • Samac DA, Hironaka CM, Yallaly PE, Shah DM (1990) Isolation and characterization of the genes encoding basic and acidic chitinase in Arabidopsis thaliana. Plant Physiol 93:907–914

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saravitz DM, Siedow JN (1996) The differential expression of wound-inducible lipoxygenase genes in soybean leaves. Plant Physiol 110:287–299

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Shah J, Zeier J (2013) Long-distance communication and signal amplification in systemic acquired resistance. Front Plant Sci 4:30

    PubMed  PubMed Central  Google Scholar 

  • Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100

    CAS  PubMed  Google Scholar 

  • Stein E, Molitor A, Kogel K-H, 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 49:1747–1751

    CAS  PubMed  Google Scholar 

  • Thakker JN, Patel N, Kothari IL (2007) Fusarium oxysporum derived Elicitor-induced changes in Enzymes of Banana leaves against wilt disease. J Mycol Plant Pathol 37:510–513

    Google Scholar 

  • Thakker JN, Shah K, Kothari IL (2009) Elicitation, partial purification and antifungal activity of \( \beta \)- 1, 3 glucanase from banana plants. J Pure App Sci PRAJNA 17:10–16

    Google Scholar 

  • Thipyapong P, Steffens JC (1997) Tomato polyphenol oxidase (Differential response of the polyphenol oxidase F promoter to injuries and wound signals). Plant Physiol 115:409–418

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylic acid-dependent defense response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci U S A 95:15107–15111

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomma BPHJ, Penninckx IAMA, Cammue BPA, Broekaert WF (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Tran H, Ficke A, Asiimwe T, Höfte M, Raaijmakers JM (2007) Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol 175:731–742

    CAS  PubMed  Google Scholar 

  • Truman W, Bennett 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 U S A 104:1075–1080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4:645–656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vaan loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765

    Google Scholar 

  • Van der Ent S, Verhagen BWM, Van Doorn R, Bakker D, Verlaan MG, Pel MJC, Joosten RG, Proveniers MCG, Van Loon LC, Ton J, Pieterse CMJ (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146:1293–1304

    PubMed  PubMed Central  Google Scholar 

  • Van Loon LC (2000) Systemic induced resistance. In: Slusarenko AJ, Fraser RSS, Van Loon LC (eds) Mechanisms of resistance to plant diseases. Kluwer Academic Publishers, Dordrecht, pp 521–574

    Google Scholar 

  • Van Loon LC, Bakker PAHM (2006) Root-associated bacteria inducing systemic resistance. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 269–316

    Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    PubMed  Google Scholar 

  • Van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    PubMed  Google Scholar 

  • van Wees SCM, Luijendijk M, Smoorenburg I, Leendert C, van Loon Pieterse CMJ (1999) Rhizobacteria-mediated 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 41:537–549

    PubMed  Google Scholar 

  • 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 U S A 97:8711–8716

    PubMed  PubMed Central  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    PubMed  Google Scholar 

  • Verberne MC, Hoekstra J, Bol JF, Linthorst HJM (2003) Signaling of systemic acquired resistance in tobacco depends on ethylene perception. Plant J 35:27–32

    CAS  PubMed  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma–plant–pathogen interactions. Soil Biol Biochem 40:1–10

    CAS  Google Scholar 

  • Vleesschauwer D, Ho¨Fte M (2009) Rhizobacteria-induced systemic resistance. Adv Bot Res 51:223–281

    Google Scholar 

  • Vlot AC, Klessig DF, Park SW (2008a) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11:436–442

    CAS  PubMed  Google Scholar 

  • Vlot AC, Liu P-P, Cameron RK, Park S-W, Yang Y, Kumar D, Zhou F, Padukkavidana T, Gustafsson C, Pichersky E, Klessig DF (2008b) Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J 56:445–456

    CAS  PubMed  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    CAS  PubMed  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schaefer P, Kogel KH (2008) Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. J Plant Physiol 165:60–70

    CAS  PubMed  Google Scholar 

  • Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64:1263–1280

    CAS  PubMed  Google Scholar 

  • Wasternack C, Parthier B (1997) Jasmonate-signaled plant gene expression. Trends Plant Sci 2:302–307

    Google Scholar 

  • Wendehenne D, Gao QM, Kachroo A, Kachroo P (2014) Free radical-mediated systemic immunity in plants. Curr Opin Plant Biol 20:127–134. doi:10.1016/j.pbi.2014.05.012

    Article  CAS  PubMed  Google Scholar 

  • 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 92:1329–1333

    CAS  PubMed  Google Scholar 

  • Yang YX, Ahammed GJ, Wu C, Fan SY, Zhou YH (2015) Crosstalk among jasmonate, salicylate and ethylene signaling pathways in plant disease and immune responses. Curr Protein Pept Sci 16(5):450–461

    CAS  PubMed  Google Scholar 

  • Zamioudis C, Pieterse C (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25:139–150

    CAS  PubMed  Google Scholar 

  • Zdor RE, Anderson AJ (1992) Influence of root colonizing bacteria on the defense responses in bean. Plant Soil 140:99–107

    Google Scholar 

  • Zhang S, Moyne A-L, Reddy MS, Kloepper JW (2002) The role of salicylic acid in induced systemic resistance elicited by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol Control 25:288–296

    Google Scholar 

Download references

Acknowledgment

Some of the research in the present review has partially been supported by DBT and SERB grant no. BT/PR1231/AGR/021/340/2011 and SR/FT/LS-129/2012, respectively, to DKC.

Author information

Authors and Affiliations

  1. Department of Science, Faculty of Arts, Science & Commerce, Mody University of Science & Technology, Lakshmangarh, 332311, Rajasthan, India

    Shekhar Jain

  2. Amity Institute of Microbial Technology (AIMT), Amity University, Sector-125, Gautam Buddha Nagar, Noida, 201313, Uttar Pradesh, India

    Shekhar Jain, Ajit Varma, Narendra Tuteja & Devendra Kumar Choudhary

Authors
  1. Shekhar Jain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ajit Varma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Narendra Tuteja
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Devendra Kumar Choudhary
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Devendra K. Choudhary

  2. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ajit Varma

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Singapore

About this chapter

Cite this chapter

Jain, S., Varma, A., Tuteja, N., Choudhary, D.K. (2016). Plant Growth-Promoting Microbial-Mediated Induced Systemic Resistance in Plants: Induction, Mechanism, and Expression. In: Choudhary, D.K., Varma, A. (eds) Microbial-mediated Induced Systemic Resistance in Plants. Springer, Singapore. https://doi.org/10.1007/978-981-10-0388-2_15

Download citation

Publish with us

Policies and ethics

Search

Navigation