Mechanisms of Biocontrol

  • P. Parvatha Reddy


Plant pathogens such as fungi, bacteria, viruses, nematodes, etc., which cause various diseases in crop plants, are controlled by plant growth-promoting rhizobacteria (PGPR). The mechanisms of biocontrol may be competition or antagonism; however, the most studied phenomenon is the induction of systemic resistance by these rhizobacteria in the host plant. PGPR control the damage to plants from pathogens by a number of mechanisms including: outcompeting the pathogen by physical displacement, secretion of siderophores to prevent pathogens in the immediate vicinity from proliferating, synthesis of antibiotics and bacteriocins and a variety of small molecules that inhibit pathogen growth, production of enzymes that inhibit the pathogen and stimulation of the systemic resistance in the plants. PGPR may also stimulate the production of biochemical compounds associated with host defence. Enhanced resistance may be due to massive accumulation of phytoalexins and phenolic compounds; increases in the activities of PR proteins, defence enzymes and transcripts; and enhanced lignification. Biocontrol may also be improved by genetically engineered PGPR to overexpress one or more of these traits so that strains with several different anti-pathogen traits can act synergistically. PGPR may use more than one of these mechanisms as experimental evidence suggests that biocontrol of plant pathogens is the net result of multiple mechanisms that may be activated simultaneously.


Jasmonic Acid Root Colonization Phenylalanine Ammonia Lyase Fluorescent Pseudomonad Endophytic Bacterium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abriouel H, Franz CM, Ben Omar N, Gálvez A (2011) Diversity and applications of Bacillus bacteriocins. FEMS Microbiol Rev 35:201–232PubMedCrossRefGoogle Scholar
  2. Aino M, Maekawa Y, Mayama S, Kato H (1997) Biocontrol of bacterial wilt of tomato by producing seedlings colonized with endophytic antagonistic pseudomonads. In: Ogoshi A, Kobayashi K, Homma Y, Kodama F, Kondo N, Akino S (eds) Plant growth promoting rhizobacteria: present status and future prospects. Nakanishi Printing, Sapporo, pp 120–123Google Scholar
  3. Anderson AJ, Guerra D (1985) Responses of bean to root colonization with Pseudomonas putida in hydroponic system. Phytopathology 75:992–995CrossRefGoogle Scholar
  4. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32PubMedCrossRefGoogle Scholar
  5. Basnayake WVS, Birch RG (1995) A gene from Alcaligenes denitrificans that confers albicidin resistance by reversible antibiotic binding. Microbiology 141:551–560PubMedCrossRefGoogle Scholar
  6. Benhamou N, Belanger RR, Paulitz T (1996a) Ultrastructural and cytochemical aspects of the interaction between Pseudomonas fluorescens and Ri T-DNA transformed pea roots: host response to colonization by Pythium ultimum Trow. Planta 199:105–117CrossRefGoogle Scholar
  7. Benhamou N, Kloepper JW, Quadt-Hallmann A, Tuzun S (1996b) Induction of defense-related ultrastructural modifications in pea root tissues inoculated with endophytic bacteria. Plant Physiol 112:919–929PubMedPubMedCentralGoogle Scholar
  8. Benhamou N, Kloepper JW, Tuzun S (1998) Induction of resistance against Fusarium wilt of tomato by combination of chitosan with an endophytic bacterial strain: ultrastructural and cytochemistry of the host response. Planta 204:153–168CrossRefGoogle Scholar
  9. Benhamou N, Gange S, Quere D, Le Dehbi L (2000) Bacterial-mediated induced resistance in cucumber: beneficial effect of the endophytic bacterium Serratia plymuthica on the protection against infection by Pythium ultimum. Phytopathology 90:45–46PubMedCrossRefGoogle Scholar
  10. Burkhead KD, Schisler DA, Slininger PJ (1994) Pyrrolnitrin production by biological control agent Pseudomonas cepacia B37w in culture and in colonized wounds of potatoes. Appl Environ Microbiol 60:2031–2039PubMedPubMedCentralGoogle Scholar
  11. Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubès R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Microbiol Mol Biol Rev 71:158–229PubMedCrossRefPubMedCentralGoogle Scholar
  12. Castillo UF, Strobel GA, Ford EJ, Hess WM, Porter H, Jensen JB, Albert H, Robison R, Condron MAM, Teplow DB, Steevens D, Yaver D (2002) Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans. Microbiology 148:2675–2685PubMedGoogle Scholar
  13. Chatterton S, Sutton JC, Boland GJ (2004) Timing Pseudomonas chlororaphis applications to control Pythium aphanidermatum, Pythium dissotocum, and root rot in hydroponic peppers. Biol Control 30:360–373CrossRefGoogle Scholar
  14. Chen C, Bauske EM, Musson G, Rodriguez-Kabana R, Kloepper JW (1995) Biological control of Fusarium wilt on cotton by use of endophytic bacteria. Biol Control 5:83–91CrossRefGoogle Scholar
  15. Chen J, Abawi GS, Zuckerman BM (2000) Efficacy of Bacillus thuringiensis, Paecilomyces marquandii and Streptomyces costaricanus with and without organic amendments against Meloidogyne hapla infecting lettuce. J Nematol 32:70–77PubMedPubMedCentralGoogle Scholar
  16. Chernin L, Chet I (2002) Microbial enzymes in biocontrol of plant pathogens and pests. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology, and applications. Marcel Dekker, New York, pp 171–225Google Scholar
  17. Chernin L, Toklikishvili N, Ovadis M, Kim S, Ben-Ari J, Khmel I, Vainstein A (2011) Quorum-sensing quenching by rhizobacterial volatiles. Environ Microbiol Rep 3:698–704PubMedCrossRefGoogle Scholar
  18. Chin-A-Woeng TFC, Bloemberg GV, van der Bij AJ, van der Drift KMGM, Schripsema J, Kroon B, Scheffer RJ, Keel C, Bakker PAHM, De Bruijn FJ, Thomas-Oates JE, Lugtenberg BJJ (1998) Biocontrol by phenazine-1-carboxamide producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicis-lycopersici. Mol Plant Microbe Interact 10:79–86CrossRefGoogle Scholar
  19. Corbell N, Loper JE (1995) A global regulator of secondary metabolite production in Pseudomonas fluorescens Pf-5. J Bacteriol 177:6230–6236PubMedPubMedCentralGoogle Scholar
  20. De Meyer G, Capieau C, Audenaert K, Buchala A, Metraux JP, Hofte 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 12:450–458PubMedCrossRefGoogle Scholar
  21. De Weger LA, Bakker PAHM, Schippers B, van Loosdrecht MCM, Lugtenberg B (1989) Pseudomonas spp. with mutational changes in the O-antigenic side chain of their lipopolysaccharides are affected in their ability to colonize potato roots. In: Lugtenberg BJJ (ed) Signal molecules in plant-microbe interactions. Springer, Berlin, pp 197–202CrossRefGoogle Scholar
  22. Degenhardt J, Gershenzon J, Baldwin IT, Kessler A (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotechnol 14:169–176PubMedCrossRefGoogle Scholar
  23. Dekkers LC, Phoelich CC, van der Fits L, Lugtenberg BJJ (1998) A site-specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365. Proc Natl Acad Sci U S A 95:7051–7056PubMedCrossRefPubMedCentralGoogle Scholar
  24. Dekkers LC, Mulders IH, Phoelich CC, Chin-A-Woeng TFC, Wijfjes AH, Lugtenberg BJJ (2000) The sss colonization gene of the tomato-Fusarium oxysporum f. sp. radicis-lycopersici biocontrol strain Pseudomonas fluorescens WCS365 can improve root colonization of other wild-type Pseudomonas spp. bacteria. Mol Plant Microbe Interact 13:1177–1183PubMedCrossRefGoogle Scholar
  25. Desbrosses G, Contesto C, Varoquaux F, Galland M, Touraine B (2009) PGPR-Arabidopsis interactions is a useful system to study signalling pathways involved in plant developmental control. Plant Signal Behav 4:321–323PubMedCrossRefPubMedCentralGoogle Scholar
  26. Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci U S A 97:3526–3531PubMedCrossRefPubMedCentralGoogle Scholar
  27. Duan J, Muller KM, Charles TC, Vesely S, Glick BR (2009) 1-Aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from Southern Saskatchewan. Microb Ecol 57:423–436PubMedCrossRefGoogle Scholar
  28. Duffy BK (2001) Competition. In: Maloy OC, Murray TD (eds) Encyclopedia of plant pathology. Wiley, New York, pp 243–244Google Scholar
  29. Duijff BJ, Gianinazzi-Pearson V, Lemanceau P (1997) Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol 135:325–334CrossRefGoogle Scholar
  30. Frankowski J, Lorito M, Scala F, Schmidt R, Berg G, Bahl H (2001) Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Arch Microbiol 176:421–426PubMedCrossRefGoogle Scholar
  31. Fridlender M, Inbar J, Chet I (1993) Biological control of soilborne plant pathogens by a β-1, 3-glucanase-producing Pseudomonas cepacia. Soil Biol Biochem 25:1211–1221CrossRefGoogle Scholar
  32. Gadoury DM, Wakefield LM, Cadle-Davidson L, Dry IB, Seem RC (2012) Effects of prior vegetative growth, inoculum density, light, and mating on conidiation of Erysiphe necator. Phytopathology 102:65–72PubMedCrossRefGoogle Scholar
  33. Glick BR, Bashan Y (1997) Genetic manipulation of plant growth-promoting bacteria to enhance biocontrol of phytopathogens. Biotechnol Adv 15:353–376PubMedCrossRefGoogle Scholar
  34. Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiol Biochem 39:11–17CrossRefGoogle Scholar
  35. Hammer PE, Hill DS, Lam ST, van Pee KH, Ligon JM (1997) Four genes from Pseudomonas fluorescens that encode the biosynthesis of pyrrolnitrin. Appl Environ Microbiol 63:2147–2154PubMedPubMedCentralGoogle Scholar
  36. Holden MTG et al (1999) Quorum-sensing cross-talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol Microbiol 33:1254–1266PubMedCrossRefGoogle Scholar
  37. Hynes RK, Lazarovits G (1989) Effect of seed treatment with plant growth promoting rhizobacteria on the protein profiles of intercellular fluids from bean and tomato leaves. Can J Plant Pathol 11:191Google Scholar
  38. Kamensky M, Ovadis M, Chet I, Chernin L (2003) Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol Biochem 35:323–331CrossRefGoogle Scholar
  39. Kloepper JW (1993) Plant growth promoting rhizobacteria as biological control agents. In: Metting FB Jr (ed) Soil microbial ecology- applications in agricultural and environmental management. Marcel Dekker, New York, pp 255–274Google Scholar
  40. Knee EM, Gong FC, Gao M, Teplitski M, Jones AR, Foxworthy A, Mort AJ, Bauer WD (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant Microbe Interact 14:775–784PubMedCrossRefGoogle Scholar
  41. Kuiper I, Bloemberg GV, Noreen S, Thomas-Oates JE, Lugtenberg BJJ (2001) Increased uptake of putrescine in the rhizosphere inhibits competitive root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact 14:1096–1104PubMedCrossRefGoogle Scholar
  42. Lee JY, Moon SS, Hwang BK (2003) Isolation and antifungal and antioomycete activities of aerugine produced by Pseudomonas fluorescens strain MM-B16. Appl Environ Microbiol 69:2023–2031PubMedCrossRefPubMedCentralGoogle Scholar
  43. Lim HS, Kim YS, Kim SD (1991) Pseudomonas stutzeri YPL-1 genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot. Appl Environ Microbiol 57:510–516PubMedPubMedCentralGoogle Scholar
  44. Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, van der Lelie D (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606CrossRefGoogle Scholar
  45. Lugtenberg BJJ, Dekkers LC (1999) What make Pseudomonas bacteria rhizosphere competent? Environ Microbiol 1:9–13PubMedCrossRefGoogle Scholar
  46. Lugtenberg BJ, Kravchenko LV, Simons M (1999) Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains, and role in rhizosphere colonization. Environ Microbiol 1:439–446PubMedCrossRefGoogle Scholar
  47. Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Ann Rev Phytopathol 38:461–490CrossRefGoogle Scholar
  48. Mauch F, Hadwiger LA, Boller T (1994) Ethylene: symptom, not signal for the induction of chitinase and β-1, 3-glucanase in pea pods by pathogens and elicitors. Plant Physiol 76:607–611CrossRefGoogle Scholar
  49. Maurhofer M, Hase C, Meuwly P, Metraux JP, Defago G (1994) Induction of systemic resistance of tobacco to tobacco necrosis virus by the root colonizing Pseudomonas fluorescens strain CHAO: influence of the gagA gene and of pyoverdine production. Phytopathology 84:678–684CrossRefGoogle Scholar
  50. M’Piga P, Belanger RR, Paulitz TC, Benhamou N (1997) Increased resistance to Fusarium oxysporum f. sp. radicis-lycopersici in tomato plants treated with the endophytic bacterium Pseudomonas fluorescens strain 63–28. Physiol Mol Plant Pathol 50:301–320CrossRefGoogle Scholar
  51. Nelson EB (2004) Microbial dynamics and interactions in the spermosphere. Ann Rev Phytopathol 42:271–309CrossRefGoogle Scholar
  52. Newton JA, Fray RG (2004) Integration of environmental and host-derived signals with quorum sensing during plant-microbe interactions. Cell Microbiol 6:213–224PubMedCrossRefGoogle Scholar
  53. Okubara PA, Kornoely JP, Landa BB (2004) Rhizosphere colonization of hexaploid wheat by Pseudomonas fluorescens strains Q8rl-96 and Q2-87 is cultivar-variable and associated with changes in gross root morphology. Biol Control 30:392–403CrossRefGoogle Scholar
  54. Ordentlich A, Elad Y, Chet I (1988) The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii. Phytopathology 78:84–88Google Scholar
  55. Ovadis M, Liu X, Gavriel S, Ismailov Z, Chet I, Chernin L (2004) The global regulator genes from biocontrol strain Serratia plymuthica IC1270: cloning, sequencing, and functional studies. J Bacteriol 186:4986–4993PubMedCrossRefPubMedCentralGoogle Scholar
  56. Pettersson M, Baath E (2004) Effects of the properties of the bacterial community on pH adaptation during recolonization of a humus soil. Soil Biol Biochem 36:1383–1388CrossRefGoogle Scholar
  57. Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, Van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580PubMedCrossRefPubMedCentralGoogle Scholar
  58. Pieterse CMJ, Ton J, Van Loon LC (2001) Cross-talk between plant defence signalling pathways: boost or burden? AgBiotechNet 3:ABN068Google Scholar
  59. Ramamoorthy V, Samiyappan R (2001) Induction of defense-related genes in Pseudomonas fluorescens treated chilli plants in response to infection by Colletotrichum capsici. J Mycol Plant Pathol 31:146–155Google Scholar
  60. Ramamoorthy V, Viswanathan R, Raguchander T, Prakasam V, Samiyappan R (2001) Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Prot 20:1–11CrossRefGoogle Scholar
  61. Reinhold B, Hurek T, Fendrik I (1985) Strain-specific chemotaxis of Azospirillum spp. J Bacteriol 162:190–195PubMedPubMedCentralGoogle Scholar
  62. Ren D, Sims JJ, Wood TK (2001) Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone. Environ Microbiol 3:731–736PubMedCrossRefGoogle Scholar
  63. Riley M (1993) Molecular mechanisms of colicin evolution. Mol Biol Evol 10:1380–1395PubMedGoogle Scholar
  64. Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and application. Ann Rev Microbiol 56:117–137CrossRefGoogle Scholar
  65. Rovira AD (1965) Interactions between plant roots and soil microorganisms. Ann Rev Microbiol 19:241–266CrossRefGoogle Scholar
  66. Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34:635–648PubMedCrossRefGoogle Scholar
  67. Schouten A, van der Berg G, Edel-Hermann V, Steinberg C, Gautheron N, Alabouvette C, de Vos CH, Lemanceau P, Raaijmakers JM (2004) Defense responses of Fusarium oxysporum to 2, 4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by Pseudomonas fluorescens. Mol Plant Microbe Interact 17:1201–1211PubMedCrossRefGoogle Scholar
  68. Sessitsch A, Reiter B, Berg G (2004) Endophytic bacterial communities of field-grown potato plants and their plant growth-promoting and antagonistic abilities. Can J Microbiol 50:239–249PubMedCrossRefGoogle Scholar
  69. Simons M, Permentier HP, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1997) Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact 10:102–106CrossRefGoogle Scholar
  70. Singh PP, Shin YC, Park CS, Chung YR (1999) Biological control of Fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89:92–99PubMedCrossRefGoogle Scholar
  71. Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506PubMedCrossRefGoogle Scholar
  72. Sturz AV, Christie BR, Matheson BG, Arsenault WJ, Buchanan NA (1999) Endophytic bacterial communities in the periderm of potato tubers and their potential to improve resistance to soil-borne plant pathogens. Plant Pathol 48:360–369CrossRefGoogle Scholar
  73. Toyoda H, Hashimoto H, Utsumi R, Kobayashi H, Ouchi S (1988) Detoxification of fusaric acid by a fusaric acid-resistant mutant of Pseudomonas solanacearum and its application to biological control of Fusarium wilt of tomato. Phytopathology 78:1307–1311CrossRefGoogle Scholar
  74. Van der Broek D, Chin-A-Woeng TFC, Eijkemans K, Mulders IHM, Bloemberg GV, Lugtenberg BJJ (2003) Biocontrol traits of Pseudomonas spp. are regulated by phase variation. Mol Plant Microbe Interact 16:1003–1012PubMedCrossRefGoogle Scholar
  75. Van Overbeek LS, Van Elsas JD (1995) Root exudates-induced promoter activity in Pseudomonas fluorescens mutants in the wheat rhizosphere. Appl Environ Microbiol 61:890–898PubMedPubMedCentralGoogle Scholar
  76. Van Peer R, Niemann GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. WCS417r. Phytopathology 81:728–734CrossRefGoogle Scholar
  77. von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Ann Rev Phytopathol 41:455–482CrossRefGoogle Scholar
  78. Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483PubMedCrossRefGoogle Scholar
  79. Walker MJ, Birch RG, Pemberton JM (1988) Cloning and characterization of an albicidin resistance gene from Klebsiella oxytoca. Mol Microbiol 2:443–454PubMedCrossRefGoogle Scholar
  80. Welbaum G, Sturz AV, Dong Z, Nowak J (2004) Fertilizing soil microorganisms to improve productivity of agroecosystems. Crit Rev Plant Sci 23:175–193CrossRefGoogle Scholar
  81. Wright SAI, Zumoff CH, Schneider L, Beer SV (2001) Pantoea agglomerans strain EH318 produces two antibiotics that inhibit Erwinia amylovora in vitro. Appl Environ Microbiol 67:284–292PubMedCrossRefPubMedCentralGoogle Scholar
  82. Yamada Y, Nihira T (1998) Microbial hormones and microbial chemical ecology. In: Barton DHR, Nakanishi K (eds) Comprehensive natural products chemistry, vol 8. Elsevier Sciences, Amsterdam, pp 377–413Google Scholar
  83. Zdor RE, Anderson AJ (1992) Influence of root colonizing bacteria on the defense responses of bean. Plant Soil 140:99–107CrossRefGoogle Scholar
  84. Zhang L, Birch RG (1997) The gene for albicidin detoxification from Pantoea dispersa encodes an esterase and attenuates pathogenicity of Xanthomonas albilineans to sugarcane. Proc Natl Acad Sci U S A 94:9984–9989PubMedCrossRefPubMedCentralGoogle Scholar
  85. Zhang LH, Dong YH (2004) Quorum sensing and signal interference: diverse implications. Mol Microbiol 53:1563–1571PubMedCrossRefGoogle Scholar

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© Springer India 2014

Authors and Affiliations

  • P. Parvatha Reddy
    • 1
  1. 1.Indian Institute of Horticultural ResearchBangaloreIndia

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