Tropical Plant Pathology

, Volume 42, Issue 2, pp 96–108 | Cite as

Induced resistance in tomato plants promoted by two endophytic bacilli against bacterial speck

  • Roberto Lanna-Filho
  • Ricardo M. Souza
  • Eduardo Alves
Original Article

Abstract

Endophytic bacteria Bacillus pumilus and Bacillus amyloliquefaciens, indigenous from tomato, were evaluated for their ability to induce resistance against bacterial speck in tomato plants. Plants grown from seeds that were bacterized with the two Bacillus species and inoculated with a green fluorescent protein-marked Pseudomonas syringae pv. tomato NS4 displayed reduced disease severity when compared to control treatment (water). However, plants in an induced state had a slight negative effect on plant growth parameters such as plant height and plant dry weight. Under epifluorescence microscopy, on tomato phylloplane of plants grown from seeds bacterized with the bacilli, the GFP-marked strain population was drastically reduced and presented individual cells or few aggregates of the pathogen between the depressions along the junctions on the leaf surface. In addition, peroxidase (POX), polyphenol oxidase (PPO) and phenylalanine ammonia-lyase (PAL) enzyme activities were evaluated in plant extracts, and all showed increased activity. We report the ability of two Bacillus species in promoting the phenomenon of induced resistance in tomato plants by a significant increase in POX, PPO and PAL activities, which produced a protective effect in reducing disease severity in levels that reached 62%.

Keywords

Endophytic bacteria Fitness cost Induced state Peroxidase Polyphenol oxidase Phenylalanine ammonia-lyase 

Notes

Acknowledgements

This work was supported by a grant from the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We thank the Laboratory of Electronic Microscopy and Ultrastructural analysis of the Universidade Federal de Lavras for access to its facilities.

References

  1. Abbasi PA, Khabbaz SE, Weselowski B, Zhang L (2015) Occurrence of copper-resistant strains and a shift in Xanthomonas spp. causing tomato bacterial spot in Ontario. Can J Microbiol 61:753–761CrossRefPubMedGoogle Scholar
  2. Ahn IP, Park K, Kim CH (2002) Rhizobacteria-induced resistance perturbs viral disease progress and triggers defense-related gene expression. Mol Cells 13:302–308PubMedGoogle Scholar
  3. Anterola AM, Lewis NG (2002) Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry 61:221–294CrossRefPubMedGoogle Scholar
  4. Bashan Y (1997) Alternative strategies for controlling plant diseases caused by Pseudomonas syringae. In: Rudolph K, Burr TJ, Mansfield JW, Stead D, Vivian A, von Kietzell J (eds) Pseudomonas syringae pathovars and related pathogens - developments in plant pathology. Kluwer Academic Publishers, Dordrecht, pp 575–583Google Scholar
  5. Behlau F, Hong JC, Jones JB, Graham JH (2013) Evidence for acquisition of copper resistance genes from different sources in citrus-associated Xanthomonads. Phytopathology 103:409–418CrossRefPubMedGoogle Scholar
  6. Blancard D, Laterrot H, Marchoux G, Candresse T (2012) Tomato diseases, identification, biology and control: a colour handbook, 2nd edn. Manson Publishing, VersaillesCrossRefGoogle Scholar
  7. Bordiec S, Paquis S, Lacroix H, Dhondt S, Barka EA, Kauffmann S, Jeandet P, Mazeyrat-Gourbeyre F, Clément C, Baillieul F, Dorey S (2011) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot 62:595–603CrossRefPubMedGoogle Scholar
  8. Boudet AM (1998) A new view of lignification. Trends Plant Sci 3:67–71CrossRefGoogle Scholar
  9. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  10. Brown JKM (2016) Fitness costs of pathogen recognition in plants and their implications for crop improvement. In: Collinge DB (ed) Plant pathogen resistance biotechnology. John Wiley & Sons, New Jersey, pp 385–400CrossRefGoogle Scholar
  11. Brown JKM, Andrivon D, Collinge DB, Nicholson P (2013) Fitness costs and trade-offs in plant disease. Plant Pathol 62:1CrossRefGoogle Scholar
  12. Cabanás CGL, Schilirò E, Valverde-Corredor A, Mercado-Blanco J (2014) The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Front Microbiol 5:427Google Scholar
  13. Cazorla FM, Arrebola E, Sesma A, Pérez-García A, Codina JC, Murillo J, de Vicente A (2002) Copper resistance in Pseudomonas syringae strains isolated from mango is encoded mainly by plasmids. Phytopathology 92:909–916CrossRefPubMedGoogle Scholar
  14. Cellini A, Fiorentini L, Buriani G, Yu J, Donati I, Cornish DA, Novak B, Costa G, Vanneste JL, Spinelli F (2014) Elicitors of the salicylic acid pathway reduce incidence of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidae. Ann Appl Biol 165:441–453CrossRefGoogle Scholar
  15. Chen NL, Hu M, Dai CY, Yang SM (2010) The effects of inducing treatments on phenolic metabolism of melon leaves. Acta Hortic Sin 37:1759–1766Google Scholar
  16. Chen X, Miché L, Sachs S, Wang Q, Buschart A, Yang H, Cruz CMV, Hurek T, Reinhold-Hurek B (2015) Rice responds to endophytic colonization which is independent of the common symbiotic signaling pathway. New Phytol 208:531–543CrossRefPubMedGoogle Scholar
  17. Chen X, Pizzatti C, Bonaldi M, Saracchi M, Erlacher A, Kunova A, Berg G, Cortesi P (2016) Biological control of lettuce drop and host plant colonization by rhizospheric and endophytic Streptomycetes. Front Microbiol 7:714PubMedPubMedCentralGoogle Scholar
  18. Choudhary DK, Varma A (eds) (2016) Microbial-mediated induced systemic resistance in plants. Springer Singapore, SingaporeGoogle Scholar
  19. Cipollini D, Heil M (2010) Costs and benefits of induced resistance to herbivores and pathogens in plants. CAB Rev: Perspect Agric Vet Sci Nutr Nat Resour 5:1–25CrossRefGoogle Scholar
  20. Collinge DB (ed) (2016) Plant pathogen resistance biotechnology. John Wiley & Sons, New JerseyGoogle Scholar
  21. Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Amsterdam, pp 253–269CrossRefGoogle Scholar
  22. Cooksey DA (1990) Genetics of bactericide resistance in plant pathogenic bacteria. Annu Rev Phytopathol 28:201–219CrossRefGoogle Scholar
  23. Cooksey DA, Azad HR (1992) Accumulation of copper and other metals of copper-resistant plant-pathogenic and saprophytic pseudomonads. Appl Environ Microbiol 58:274–278PubMedPubMedCentralGoogle Scholar
  24. Denancé N, Sánchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155CrossRefPubMedPubMedCentralGoogle Scholar
  25. Dietrich R, Ploss K, Heil M (2005) Growth responses and fitness costs after induction of pathogen resistance depend on environmental conditions. Plant Cell Environ 28:211–222CrossRefGoogle Scholar
  26. Diomandé SE, Nguyen-The C, Guinebretière MH, Broussolle V, Brillard J (2015) Role of fatty acids in Bacillus environmental adaptation. Front Microbiol 6:813PubMedPubMedCentralGoogle Scholar
  27. Eljounaidi K, Lee SK, Bae H (2016) Bacterial endophytes as potential biocontrol agents of vascular wilt diseases - review and future prospects. Biol Control 103:62–68CrossRefGoogle Scholar
  28. El-Sayed ESA, El-Didamony G, El-Sayed EF (2002) Effects of mycorrhizae and chitin-hydrolysing microbes on Vicia faba. World J Microbiol Biotechnol 18:505–515CrossRefGoogle Scholar
  29. Gao L, Zhang Y (2013) Effect of salicylic acid on pear leaf induced resistance to pear ring rot. World Appl Sci J 22:1534–1539Google Scholar
  30. Gao X, Gong Y, Huo Y, Han Q, Kang Z, Huang L (2015) Endophytic Bacillus subtilis strain E1R-J is a promising biocontrol agent for wheat powdery mildew. BioMed Res Int. ID 462645:8Google Scholar
  31. Gauillard F, Richard-Forget F, Nicolas J (1993) New spectrophotometric assay for polyphenol oxidase activity. Anal Biochem 215:59–65CrossRefPubMedGoogle Scholar
  32. Gerhardt PE (1994) Methods for general and molecular bacteriology. American Society for Microbiology, WashingtonGoogle Scholar
  33. Goto M, Hikota T, Kyuda T, Nakajima M (1993) Induction of copper resistance plant-pathogenic bacteria exposed to glutamate, plant extracts, phosphate buffer, and some antibiotics. Dis Control Pest Manag 83:1449–1453Google Scholar
  34. Hallman J, Quadt-Hallman A, Mahafee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  35. Halo BA, Khan AL, Waqas M, AlHarrasi A, Hussain J, Ali L, Adnan M, Lee IJ (2015) Endophytic bacteria (Sphingomonas sp. LK11) and gibberellin can improve Solanum lycopersicum growth and oxidative stress under salinity. J Plant Interact 10:117–125CrossRefGoogle Scholar
  36. Heil M (2007) Trade-offs associated with induced resistance. In: Walters D, Newton A, Lyon G (eds) Induced resistance for plant defence: a sustainable approch to crop protection. Blackwell Publishing, Oxford, pp 157–177CrossRefGoogle Scholar
  37. Heil M, Hilpert A, Kaiser W, Linsenmair KE (2000) Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? J Ecol 88:645–654CrossRefGoogle Scholar
  38. Hwe-Su Y, Yang JW, Choong-Min R (2013) ISR meets SAR outside: additive action of the endophyte Bacillus pumilus INR7 and the chemical inducer, benzothiadiazole, on induced resistance against bacterial spot in field-grown pepper. Front Plant Sci 4:1–11Google Scholar
  39. Jardine DJ, Stephens CT (1987) Influence of timing of application and chemical on control of bacterial speck of tomato. Plant Dis 71:405–408CrossRefGoogle Scholar
  40. Jones JB, Zitter TA, Momol MT, Miller SA (2014) Compendium of tomato diseases, 2nd edn. APS Press, St. PaulGoogle Scholar
  41. Kado CI, Heskett MG (1970) Selective media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas and Xanthomonas. Phytopathology 60:969–979CrossRefPubMedGoogle Scholar
  42. Kloepper JW, Ryu CM (2006) Bacterial endophytes as elicitors of enduced systemic resistance. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Amsterdam, pp 33–52CrossRefGoogle Scholar
  43. La Camera S, Gouzert G, Dhondt S, HoVman L, Fritig B, Legrand M, Heitz T (2004) Metabolic reprogramming in plant immunity: the contributions of phenylpropanoid and oxylipins pathways. Immunol Rev 198:267–281CrossRefPubMedGoogle Scholar
  44. Lacava PT, Azevedo JL (2013) Endophytic bacteria: a biothnological potential in agrobiology system. In: Maheshwaki DK, Saraf M, Aeron A (eds) Bacteria in agrobiology: crop productivity. Springer, Amsterdam, pp 1–44CrossRefGoogle Scholar
  45. Lacava PT, Azevedo JL (2014) Biological control of insect-pest and diseases by endophytes. In: Verma VC, Gange AC (eds) Advances in endophytic research. Springer India, New Delhi, pp 231–256CrossRefGoogle Scholar
  46. Lanna-Filho R, Souza R, Magalhães M, Villela L, Zanotto E, Ribeiro-Júnior P, Resende MLV (2013a) Induced defense responses in tomato against bacterial spot by proteins synthesized by endophytic bacteria. Trop Plant Pathol 38:295–302CrossRefGoogle Scholar
  47. Lanna-Filho R, Souza RM, Ferreira A, Quecine MC, Alves E, Azevedo JL (2013b) Biocontrol activity of Bacillus against a GFP-marked Pseudomonas syringae pv. tomato on tomato phylloplane. Australas Plant Pathol 42:643–651CrossRefGoogle Scholar
  48. Larran S, Simón MR, Moreno MV, Siurana MPS, Perelló A (2016) Endophytes from wheat as biocontrol agents against tan spot disease. Biol Control 92:17–23CrossRefGoogle Scholar
  49. Lee H, León J, Raskin I (1995) Biosynthesis and metabolism of salicylic acid. Proc Natl Acad Sci U S A 92:4076–4079CrossRefPubMedPubMedCentralGoogle Scholar
  50. Li Y, Gu Y, Li J, Xu M, Wei Q, Wang Y (2015) Biocontrol agent Bacillus amyloliquefaciens LJ02 induces systemic resistance against cucurbits powdery mildew. Front Microbiol 6:883PubMedPubMedCentralGoogle Scholar
  51. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883CrossRefPubMedPubMedCentralGoogle Scholar
  52. Martins G, Lauga B, Miot-Sertier C, Mercier A, Lonvaud A, Soulas ML, Soulas G, Masneuf-Pomarède I (2013) Characterization of epiphytic bacterial communities from grapes, leaves, bark and soil of grapevine plants grown, and their relations. PLoS ONE 8, e73013Google Scholar
  53. McManus PS, Stockwell VO, Sundin GW, Jones AL (2002) Antibiotic use in plant agriculture. Annu Rev Phytopathol 40:443–465CrossRefPubMedGoogle Scholar
  54. Melnick RL, Zidack NK, Bryan AB, Maximova SN, Guiltinan M, Backman PA (2008) Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao. Biol Control 46:46–56CrossRefGoogle Scholar
  55. Mohammadi M, Kazemi H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci 162:491–498CrossRefGoogle Scholar
  56. Mori T, Sakurai M, Sakuta M (2001) Effects of conditioned medium on activities of PAL, CHS, DAHP synthase (DS-Co and DS-Mn) and anthocyanin production in suspension cultures of Fragaria ananassa. Plant Sci 160:355–360CrossRefPubMedGoogle Scholar
  57. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 15:473–497CrossRefGoogle Scholar
  58. Nahar K, Gretzmacher R (2011) Response of shoot and root development of seven tomato cultivars in hydrophonic system under water stress. Acad J Plant Sci 4:57–63Google Scholar
  59. Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin HL, Guo JH (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol Plant-Microbe Interact 24:533–542Google Scholar
  60. Niu D, Wang X, Wang Y, Song X, Wang J, Guo J, Zhao H (2016) Bacillus cereus AR156 activates PAMP-triggered immunity and induces a systemic acquired resistance through a NPR1-and SA-dependent signaling pathway. Biochem Biophys Res Commun 469:120–125CrossRefPubMedGoogle Scholar
  61. Oliveira MDM, Varanda CMR, Félix MRF (2016) Induced resistance during the interaction pathogen x plant and the use of resistance inducers. Phytochem Lett 15:152–158CrossRefGoogle Scholar
  62. Onkokesung N, Reichelt M, van Doorn A, Schuurink RC, Dicke M (2016) Differential costs of two distinct resistance mechanisms induced by different herbivore species in Arabidopsis. Plant Physiol 170:891–906CrossRefPubMedGoogle Scholar
  63. Padgham JL, Sikora RA (2007) Biological control potential and modes of action of Bacillus megaterium against Meloidogyne graminicola on rice. Crop Prot 26:971–977CrossRefGoogle Scholar
  64. Park KS, Kloepper JW (2000) Activation of PR-1a promoter by rhizobacteria that induce systemic resistance in tobacco against Pseudomonas syringae pv. tabaci. Biol Control 18:2–9CrossRefGoogle Scholar
  65. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265CrossRefPubMedGoogle Scholar
  66. Pavlo A, Leonid O, Iryna Z, Natalia K, Maria PA (2011) Endophytic bacteria enhancing growth and disease resistance of potato (Solanum tuberosum L.). Biol Control 56:43–49CrossRefGoogle Scholar
  67. Piccoli P, Bottini R (2013) Abiotic stress tolerance induced by endophytic PGPR. In: Aroca R (ed) Symbiotic endophytes, soil biology, vol 37. Springer, Berlin, pp 151–163CrossRefGoogle Scholar
  68. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375CrossRefPubMedGoogle Scholar
  69. Rajendran L, Saravanakumar D, Raguchander T, Samiyappan R (2006) Endophytic bacterial induction of defence enzymes against bacterial blight of cotton. Phytopathol Mediterr 45:203–214Google Scholar
  70. Rajendran L, Akila R, Karthikeya G, Raguchander T, Samiyappan R (2015) Defense related enzyme induction in coconut by endophytic bacteria (EPC 5). Acta Phytopathol Entomol Hung 50:29–43CrossRefGoogle Scholar
  71. Ramli NR, Mohamed MS, Seman IA, Zairun MA, Mohamad N (2016) The potential of endophytic bacteria as a biological control agent for ganoderma disease in oil palm. Sains Malays 45:401–409Google Scholar
  72. Reiter B, Pfeifer U, Schwab H, Sessitsch A (2002) Response of endophytic bacterial communities in potato plants to infection with Erwinia carotovora subsp. atroseptica. Appl Environ Microbiol 68:2261–2268CrossRefPubMedPubMedCentralGoogle Scholar
  73. Reynolds GJ, Gordon TR, McRoberts N (2016) Quantifying the impacts of systemic acquired resistance to pitch canker on monterey pine growth rate and hyperspectral reflectance. Forests 20:1–10Google Scholar
  74. Romeiro RS, Lanna-Filho R, Vieira-Júnior R, Silva HSA, Baracat-Pereira MC, Carvalho MG (2005) Macromolecules released by a plant growth-promoting rhizobacterium as elicitors of systemic resistance in tomato to bacterial and fungal pathogens. J Phytopathol 153:120–123CrossRefGoogle Scholar
  75. Ryu CM, Farag MA, Hu CH, Munagala SR, Kloepper JW, Paré P (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026CrossRefPubMedPubMedCentralGoogle Scholar
  76. Sánchez-Rangel D, Rivas-San Vicente M, de la Torre-Hernández ME, Nájera-Martínez M, Plasencia J (2015) Deciphering the link between salicylic acid signaling and sphingolipid metabolism. Front Plant Sci 6:125CrossRefPubMedPubMedCentralGoogle Scholar
  77. Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668CrossRefPubMedGoogle Scholar
  78. Sathiyabama M (2015) Role of defense enzymes in the control of plant pathogenic bacteria. In: Kannan VR, Bastas KK (eds) Sustainable approaches to controlling plant pathogenic bacteria. CRC Press, New York, pp 311–322CrossRefGoogle Scholar
  79. Schilirò E, Ferrara M, Nigro F, Mercado-Blanco J (2012) Genetic responses induced in olive roots upon colonization by the biocontrol endophytic bacterium Pseudomonas fluorescens PICF7. PLoS ONE 7, e48646CrossRefPubMedPubMedCentralGoogle Scholar
  80. Senthilkumar M, Anandham R, Madhaiyan M, Venkateswaran V, Sa T (2011) Endophytic bacteria: perspectives and applications in agricultural crop production. In: Maheshwaki DK (ed) Bacteria in agrobiology: crop ecosystems. Springer, Amsterdam, pp 61–96CrossRefGoogle Scholar
  81. STATSOFT (2005) Statistica for Windows: user’s manual. Statsoft Incorporation. Available at: http://www.statsoft.com. Accessed 30 June 2015
  82. Sturz AV, Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl Soil Ecol 15:183–190CrossRefGoogle Scholar
  83. Sundar AR, Viswanathan R, Nagarathinam S (2009) Induction of systemic acquired resistance (SAR) using synthetic signal molecules against Colletotrichum falcatum in sugarcane. Sugar Tech 11:274–281CrossRefGoogle Scholar
  84. Sundin GW, Castiblanco LF, Yuan X, Zeng Q, Yang CH (2016) Bacterial disease management: challenges, experience, innovation and future prospects. Mol Plant Pathol 17:1506–1518CrossRefPubMedGoogle Scholar
  85. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77CrossRefPubMedGoogle Scholar
  86. Trotel-Aziz P, Couderchet M, Biagianti S, Aziz A (2008) Characterization of new bacterial biocontrol agents Acinetobacter, Bacillus, Pantoea and Pseudomonas spp. mediating grapevine resistance against Botrytis cinerea. Environ Exp Bot 64:21–32CrossRefGoogle Scholar
  87. Urbanek H, Kuzniak-Gebarowska E, Herka H (1991) Elicitation of defence responses in bean leaves by Botrytis cinerea polygalacturonase. Acta Physiol Plant 13:43–50Google Scholar
  88. van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588CrossRefPubMedGoogle Scholar
  89. van Loon LC, Bakker PA, Pieterse CM (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483CrossRefPubMedGoogle Scholar
  90. van Mölken T, Kuzina V, Munk KR, Olsen CE, Sundelin T, van Dam NM, Hauser TP (2014) Consequences of combined herbivore feeding and pathogen infection for fitness of Barbarea vulgaris plants. Oecologia 175:589–600CrossRefPubMedGoogle Scholar
  91. van Overbeek LS, Saikkonen K (2016) Impact of bacterial-fungal interactions on the colonization of the endosphere. Trends Plant Sci 21:230–242CrossRefPubMedGoogle Scholar
  92. Verma VC, Gange AC (eds) (2014) Advances in endophytic research. Part V. Bio-control and bioremediation. Springer India, New Delhi, pp 231–335Google Scholar
  93. Vos IA, Pieterse CMJ, Van Wees SCM (2013) Costs and benefits of hormone regulated plant defences. Plant Pathol 62:43–55Google Scholar
  94. Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17CrossRefGoogle Scholar
  95. War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6:1787–1792CrossRefPubMedPubMedCentralGoogle Scholar
  96. Yi HS, Yang JW, Ryu CM (2013) ISR meets SAR out side: additive action ofthe endophyte Bacillus pumilus INR7 and the chemical inducer, benzothiadiazole, on induced resistance against bacterial spot infield-grown pepper. Front Plant Sci 4:1–11CrossRefGoogle Scholar
  97. Zhao S, Guo J (2003) Systemic acquired resistance and signal transduction. Agric Sci China 2:539–548Google Scholar
  98. Zhao L, Xu Y, Lai XH, Shan C, Deng Z, Ji Y (2015) Screening and characterization of endophytic Bacillus and Paenibacillus strains from medicinal plant Lonicera japonica for use as potential plant growth promoters. Braz J Microbiol 46:977–989CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Sociedade Brasileira de Fitopatologia 2017

Authors and Affiliations

  • Roberto Lanna-Filho
    • 1
  • Ricardo M. Souza
    • 2
  • Eduardo Alves
    • 2
  1. 1.Departmento de FitossanidadeUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Departmento de FitopatologiaUniversidade Federal de LavrasLavrasBrazil

Personalised recommendations