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Disease-Induced Resistance and Plant Immunization Using Microbes

  • Miguel O. P. Navarro
  • Ane S. Simionato
  • André R. Barazetti
  • Igor M. O. dos Santos
  • Martha V. T. Cely
  • Andreas L. Chryssafidis
  • Galdino AndradeEmail author
Chapter

Abstract

The induction of resistance in plants presents as an alternative to be explored in several species. This process involves the activation of defense mechanisms, which are inactive or latent in the plant and do not require alterations in your genome. This activation can be effected by biotic and abiotic agents known as resistance inducers. The use of resistance inducers leads to activation of the systemic resistance, which leads to a marked reduction in symptoms of the disease after subsequent infections, including different species of pathogens. This chapter gathers information about diverse compounds of biological origin that can act as resistance inductors, as well as an interaction between plants and rhizosphere microorganisms that may result in the activation of this resistance system against pathogens.

Keywords

Jasmonic acid Ethylene Mycorrhiza Secondary metabolites 

References

  1. Abo-Elyousr KAM, Ibrahim Y, Balabel NM (2012) Induction of disease defensive enzymes in response to treatment with acibenzolar-s-methyl (ASM) and Pseudomonas fluorescens Pf2 and inoculation with Ralstonia solanacearum race 3, biovar 2 (phylotype II). J Phytopathol 160:382–389CrossRefGoogle Scholar
  2. Aimé S, Alabouvette C, Steinberg C, Olivain C (2013) The endophytic strain Fusarium oxysporum Fo47: a good candidate for priming the defense responses in tomato roots. MPMI 26:918–926CrossRefPubMedGoogle Scholar
  3. Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97:925–931CrossRefPubMedPubMedCentralGoogle Scholar
  4. Akiyama K, Ogasawara S, Ito S, Hayashi (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117CrossRefPubMedPubMedCentralGoogle Scholar
  5. Asensio D, Rapparini F, Peñuelas J (2012) AM fungi root colonization increases the production of essential isoprenoids vs. nonessential isoprenoids especially under drought stress conditions or after jasmonic acid application. Phytochemistry 77:149–161CrossRefPubMedGoogle Scholar
  6. Audenaert K, Pattery T, Cornelis P, Höfte M (2002) Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin and pyocyanin. MPMI 15:1147–1156CrossRefPubMedGoogle Scholar
  7. Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signaling in plant–microbe interactions. Science 276:726–733CrossRefPubMedGoogle Scholar
  8. Bektas Y, Eulgem T (2015) Synthetic plant defense elicitors. Front Plant Sci 5:804. doi: 10.3389/fpls.2014.00804 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bent E (2006) Induced systemic resistance mediated by plant growth-promoting rhizobacteria (PGPR) and Fungi (PGPF). In: Tuzun S, Bent E (eds) Multigenic and induced systemic resistance in plants. Springer, New York, pp 225–258CrossRefGoogle Scholar
  10. Campos-Soriano L, García-Martínez J, San Segundo B (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592CrossRefPubMedGoogle Scholar
  11. Che YZ, Li YR, Zou HS, Zou LF, Zhang B, Chen GY (2011) A novel antimicrobial protein for plant protection consisting of a Xanthomonas oryzae harpin and active domains of cecropin A and melittin. Microb Biotechnol 4(6):777–793CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1885CrossRefPubMedGoogle Scholar
  13. Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants – with special reference to induced systemic resistance (ISR). Microbiol Res 164(5):493–513CrossRefPubMedGoogle Scholar
  14. Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka EA (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693CrossRefPubMedPubMedCentralGoogle Scholar
  15. Copping LG, Duke SO (2007) Natural products that have been used commercially as crop protection agents. Pest Manag Sci 63:524–554CrossRefPubMedGoogle Scholar
  16. De Meyer G, Audenaert K, Höfte M (1999a) Pseudomonas aeruginosa 7NSK2-induced systemic resistance in tobacco depends on in planta salicylic acid accumulation but is not associated with PR1a expression. Eur J Plant Pathol 105:513–517CrossRefGoogle Scholar
  17. De Meyer G, Capieau K, Audenaert K, Buchala A, Métraux J, Höfte M (1999b) Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. MPMI 12:450–458CrossRefPubMedGoogle Scholar
  18. De Oliveira AG, Murate LS, Spago FR, Lopes LP, Beranger JPO, San Martin JAB, Nogueira MA, Mello JCP, Andrade CGTJ, Andrade G (2011) Evaluation of the antibiotic activity of extracellular compounds produced by the Pseudomonas strain against the Xanthomonas citri pv. Citri 306 strain. Biol Control 56:125–131CrossRefGoogle Scholar
  19. De Oliveira AG, Spago FR, Simionato AS, Navarro MO, Silva CS, Barazetti AR, Cely MV, Tischer CA, San Martin JA, Andrade CG, Novello CR, Mello JC, Andrade G (2016) Bioactive organocopper compound from Pseudomonas aeruginosa inhibits the growth of Xanthomonas citri subsp. citri. Front Microbiol 7:1–12Google Scholar
  20. De Vleesschauwe D, Cornelis P, Höfte M (2006) Redox-active pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. MPMI 19:1406–1419CrossRefGoogle Scholar
  21. Dimlioğlu G, Daş ZA, Bor M, Özdemir F, Türkan İ (2015) The impact of GABA in harpin-elicited biotic stress responses in Nicotiana tabaccum. J Plant Physiol 188:51–57CrossRefPubMedGoogle Scholar
  22. Djonovic S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant-Microbe Interact 19:838–885CrossRefPubMedGoogle Scholar
  23. Dong HD, Zhong JJ (2002) Enhanced taxane productivity in bioreactor cultivation of Taxus chinensis cells by combining elicitation, sucrose and ethylene incorporation. Enzym Microb Technol 31:116–121CrossRefGoogle Scholar
  24. Friedrich L, Lawton K, Ruess W, Masne P, Specker N, Gut Rella M, Meier B, Dincher S, Staub T, Uknes S, Metraux JP, Kessmann H, Ryals J (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J 10:61–70CrossRefGoogle Scholar
  25. Fritig B, Heitz T, Legrand M (1998) Antimicrobial proteins in induced plant defense. Curr Opin Immunol 10:16–22CrossRefPubMedGoogle Scholar
  26. Giovannetti M, Avio L, Sbrana C (2010) Fungal spore germination and pre-symbiotic mycelial growth – physiological and genetic aspects. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, New York, pp 3–31CrossRefGoogle Scholar
  27. Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Ann Rev Cell Dev Biol 29:593–617CrossRefGoogle Scholar
  28. Gutjahr C, Siegler H, Haga K, Iino M, Paszkowski (2015) Full establishment of arbuscular mycorrhizal symbiosis in rice occurs independently of enzymatic jasmonate biosynthesis. PLoS One. doi: 10.1371/journal.pone.0123422
  29. Hammond-Kosack KE, Parker JE (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotech 14:177–193CrossRefPubMedGoogle Scholar
  30. Harrison MJ (2012) Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 15:691–698CrossRefPubMedGoogle Scholar
  31. Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hermosa R, Rubio M, Cardoza RE, Nicolas C, Monte E, Gutiérrez S (2013) The contribution of Trichoderma to balancing the costs of plant growth and defense. Int Microbiol 16:69–80PubMedGoogle Scholar
  33. Iavicoli A, Boutet E, Buchala A, Métraux JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHAO. MPMI 16:851–858CrossRefPubMedGoogle Scholar
  34. Iwata M, Umemura K, Midoh N (2004) Probenazole (Oryzemate®)-A plant defense activator. In: Rice blast: interaction with rice and control. Springer, Dordrecht, pp 163–171Google Scholar
  35. Jankiewicz U, Koltonowicz M (2012) The involvement of Pseudomonas bacteria in induced systemic resistance in plants (review). Appl Biochem Microbiol 48:244–249CrossRefGoogle Scholar
  36. Jentschel K, Thiel D, Rehn F, Ludwig-Müller J (2007) Arbuscular mycorrhiza enhances auxin levels and alters auxin biosynthesis in Tropaeolum majus during early stages of colonization. Physiol Plant 129:320–333CrossRefGoogle Scholar
  37. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664CrossRefPubMedGoogle Scholar
  38. Kaldorf M, Ludwig-Müller J (2000) AM fungi might affect the root morphology of maize by increasing indole-3-butyric acid biosynthesis. Physiol Plantarum 109:58–67CrossRefGoogle Scholar
  39. Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146:1459–1468CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kurc J (1982) Induced immunity to plant diseases. Bioscience 32:854–860CrossRefGoogle Scholar
  41. Kuźniak E, Głowacki R, Chwatko G, Skłodowska M (2014) Involvement of ascorbate, glutathione, protein S-thiolation and salicylic acid in benzothiadiazole-inducible defence response of cucumber against Pseudomonas syringae pv lachrymans. Physiol Mol Plant Path 86:89–97CrossRefGoogle Scholar
  42. Leadbeater A, Staub T (2014) Exploitation of induced resistance: a commercial perspective. In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defense: a sustainable approach to crop protection. Wiley-Blackwell, Oxford, pp 300–315Google Scholar
  43. Leite B, Roncato LDB, Pascholati SF, Lambais MR (1997) Reconhecimento e transdução de sinais moleculares em interações planta-fungos fitopatogênicos. RAPP 5:235–280Google Scholar
  44. Li X, Han B, Xu M, Han L, Zhao Y, Liu Z, Dong H, Zhang C (2014) Plant growth enhancement and associated physiological responses are coregulated by ethylene and gibberellin in response to harpin protein Hpa1. Planta 239:831–846CrossRefPubMedPubMedCentralGoogle Scholar
  45. Loake G, Grant M (2007) Salicylic acid in plant defence-the players and protagonists. Curr Opin Plant Biol 10:466–472CrossRefPubMedGoogle Scholar
  46. Louws FJ, Wilson M, Campbell HL, Cuppels DA, Jones JB, Shoemaker PB, Sahin F, Miller SA (2001) Field control of bacterial spot and bacterial speck of tomato using a plant activator. Plant Dis 85:481–488CrossRefGoogle Scholar
  47. Lu H, Greenberg JT, Holuigue L (2016) Editorial: salicylic acid signaling networks. Front Plant Sci. doi: 10.3389/fpls.2016.00238
  48. Ludwig-Müller J (2010) Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, New York, pp 3–31Google Scholar
  49. Mandal B, Mandal S, Csinos S, Martinez N, Culbreath AK, Pappu HR (2008) Biological and molecular analyses of the acibenzolar-S-methyl-induced systemic acquired resistance in flue-cured tobacco against tomato spotted wilt virus. Phytopathology 98:196–204CrossRefPubMedGoogle Scholar
  50. Martínez-Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CMJ, Van Wees SCM (2016) Shifting from priming of salicylic acid-to jasmonic acid-regulated defenses by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol. doi: 10.1111/nph.14251
  51. Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222(4):709–715CrossRefPubMedGoogle Scholar
  52. Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663. doi: 10.1111/1574-6976.12028 CrossRefPubMedGoogle Scholar
  53. Meziane H, Van Der SI, Van Loon LC, Höfte M, Bakker PA (2005) Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol Plant Pathol 6:177–185CrossRefPubMedGoogle Scholar
  54. Muthamilarasan M, Prasad M (2013) Plant innate immunity: an updated insight into defense mechanism. J Biosci 38:433–449CrossRefPubMedGoogle Scholar
  55. Parkinson LE, Crew KS, Thomas JE, Dann EK (2015) Efficacy of acibenzolar-S-methyl (Bion®) treatment of Australian commercial passion fruit, Passiflora edulis f. sp. flavicarpa, on resistance to Passionfruit woodiness virus (PWV) and activities of chitinase & β-1,3-glucanase. Australas Plant Pathol 44:311–318CrossRefGoogle Scholar
  56. Pascholati SF (2003) Indução de resistência: opção para o controle de doenças de plantas no século XXI. Summa Phytopathol l29:115–116Google Scholar
  57. Pascholati SF, Leite B (1995) Hospedeiro: Mecanismos de resistência. In: Bergamin Filho A, Kimati H, Amorim L (eds) Manual de fitopatologia: princípios e conceitos. Ed. Agronômica Ceres, São Paulo, pp 193–217Google Scholar
  58. Patel JS, Zhang S, McGrath M (2016) Red light increases suppression of downy mildew in basil by chemical and organic products. Plant Phytopathol 164(11–12):1022–1029CrossRefGoogle Scholar
  59. Paul EA, Clark FE (1989) Soil microbiology and biochemistry. Academic, New YorkGoogle Scholar
  60. Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. National Research Council of Canada, OttawaGoogle Scholar
  61. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316CrossRefPubMedGoogle Scholar
  62. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Ann Rev Cell Dev Biol 28:489–521CrossRefGoogle Scholar
  63. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398CrossRefPubMedGoogle Scholar
  64. Pozo MJ, Van-Loon LC, Pieterse CMJ (2005) Jasmonates: signals in plant-microbe interactions. J Plant Growth Regul 23:211–222Google Scholar
  65. Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defense mechanisms. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, New York, pp 3–31Google Scholar
  66. Pozo MJ, Lopez-R JÁ, Azcon-Aguilar C, Garcia-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436CrossRefPubMedGoogle Scholar
  67. Reglinski T, Wurms K, Elmer P (2011) Short report on commercially available elicitors, natural products and microbes for evaluation against Pseudomonas syringae pv. Actinidiae. Plant & Food Research, RuakuraGoogle Scholar
  68. Roberts R, Taylor JE (2016) Exploiting plant induced resistance as a route to sustainable crop protection. In: Collige DB (ed) Plant pathogen resistance biotechnology. Wiley-Blackwell, Hoboken, pp 317–339CrossRefGoogle Scholar
  69. Ryu C, Farag MA, Hu C, Reddy MS, Wei HX, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. PNAS 100:4927–4932CrossRefPubMedPubMedCentralGoogle Scholar
  70. Ryu C, Farag MA, Hu C, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026CrossRefPubMedPubMedCentralGoogle Scholar
  71. Sarma BK, Mehta S, Singh HB, Singh UP (2002) Plant growth-promoting rhizobacteria elicited alteration in phenolic profile of chickpea (Cicer arietinum) infected by Sclerotium rolfsii. Phytopathol J 150:277–282CrossRefGoogle Scholar
  72. Schlumbaum A, Mauch F, Vogeli U, Boller T (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324:365–367. acibenzolar-S-methyl against Meloidogyne incognita. Nat Prod Res. doi: 10.1080/14786419.2016.1230111 CrossRefGoogle Scholar
  73. Schouteden N, Lemmens E, Stuer N, Curtis R, Panis B, De Waele D (2016) Direct nematicidal effects of methyl jasmonate and acibenzolar-S-methyl against Meloidogyne incognita. Nat Prod Res 23:1–4Google Scholar
  74. Schuhegger R et al (2006) Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918CrossRefPubMedGoogle Scholar
  75. Selosse MA, Bessis A, Pozo MJ (2014) Microbial priming of plant and animal immunity: symbionts as developmental signals. Trends Microbiol 22:607–613CrossRefPubMedGoogle Scholar
  76. Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorrhiza-induced changes in disease severity and pr protein expression in tobacco leaves. Mol Plant Microbe 12(11):1000–1007CrossRefGoogle Scholar
  77. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, New YorkGoogle Scholar
  78. Song YY, Ye M, Li CY, Wang RL, Wei XC, Luo SM, Zeng RS (2013) Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J Chem Ecol 39:1036–1044CrossRefPubMedGoogle Scholar
  79. Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different life styles. Proc Natl Acad Sci U S A 104:18842–18847CrossRefPubMedPubMedCentralGoogle Scholar
  80. Staskawicz BJ (2001) Genetics of plant-pathogen interactions specifying plant disease resistance. Plant Physiol 125:73–76CrossRefPubMedPubMedCentralGoogle Scholar
  81. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456CrossRefPubMedGoogle Scholar
  82. Tang RJ, Zhao FG, Garcia VJ, Kleist TJ, Yang L, Zhang HX et al (2015) Tonoplast CBL–CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis. Proc Natl Acad Sci U S A 112:3134–3139. doi: 10.1073/pnas.1420944112 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Tripathi D, Pappu HR (2015) Evaluation of acibenzolar-S-methyl-induced resistance against iris yellow spot tospovirus. Eur J Plant Pathol 142:855–864CrossRefGoogle Scholar
  84. Van Loon LC, van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97CrossRefGoogle Scholar
  85. Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van’tWestende YAM, Hartog F, Van Loon LC (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. MPMI 10:716–724CrossRefPubMedGoogle Scholar
  86. Vasconsuelo A, Boland R (2007) Molecular aspects of the early stages of elicitation of secondary metabolites in plants. Plant Sci 172:861–875CrossRefGoogle Scholar
  87. Verhagen BWM, Trotel-Aziz P, Couderchet M, Höfte M, Aziz A (2010) Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defense responses in grapevine. J Exp Bot 61:249–260CrossRefPubMedGoogle Scholar
  88. Vos CM, Yang Y, de Coninck B, Cammue BPA (2014) Fungal (-like) biocontrol organisms in tomato disease control. Biol Control 74:65–81CrossRefGoogle Scholar
  89. Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64:1263–1280. doi: 10.1093/jxb/ert026 CrossRefPubMedGoogle Scholar
  90. Wang W, Zhong JJ (2002) Manipulation of ginsenoside heterogeneity in cell cultures of Panax notoginseng by addition of jasmonates. J Biosci Bioeng 93:48–53CrossRefPubMedGoogle Scholar
  91. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697CrossRefPubMedPubMedCentralGoogle Scholar
  92. Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY, Collmer A, Bee SV (1992) Harpin elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85–88CrossRefPubMedGoogle Scholar
  93. Withers J, Dong X (2016) Posttranslational modifications of NPR1: a single protein playing multiple roles in plant immunity and physiology. PLoS Pathog. doi: 10.1371/journal.ppat.1005707
  94. Yu K, Niranjana M, Hahn E, Paek K (2005) Ginsenoside production by hairy root cultures of Panax ginseng: influence of temperature and light quality. Biochem Eng J 23:53–56CrossRefGoogle Scholar
  95. Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Li Q, Yang D, He Z (2007) Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 5:313–324CrossRefPubMedGoogle Scholar
  96. Zhu Z, Zhang X (2016) Effect of harpin on control of postharvest decay and resistant responses of tomato fruit. Postharvest Biol Technol 112:241–246CrossRefGoogle Scholar
  97. Zhu Z, Gao J, Yang JX, Wang XY, Ren GD, Ding YL, Kuai BK (2015) Synthetic promoters consisting of defined cis-acting elements link multiple signaling pathways to probenazole-inducible system. J Zhejiang Univ Sci B 16:253–263CrossRefPubMedPubMedCentralGoogle Scholar
  98. Ziadi S, Barbedette S, Godard F, Monot C, Le-Corre D, Silue AD (2001) Production of pathogenesis-related proteins in the cauliflower (Brassica oleracea var botrytis) downy mildew (Peronospora parasitica) pathosystem treated with acibenzolar-S-methyl. Plant Pathol 50:579–586CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Miguel O. P. Navarro
    • 1
  • Ane S. Simionato
    • 1
  • André R. Barazetti
    • 1
  • Igor M. O. dos Santos
    • 1
  • Martha V. T. Cely
    • 2
  • Andreas L. Chryssafidis
    • 3
  • Galdino Andrade
    • 1
    Email author
  1. 1.Laboratory of Microbial Ecology, Department of MicrobiologyState University of LondrinaLondrinaBrazil
  2. 2.Institute of Agrarian and Environmental SciencesFederal University of Mato GrossoSinopBrazil
  3. 3.Laboratory of Veterinary Toxicology, Department of Preventive Veterinary MedicineState University of LondrinaLondrinaBrazil

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