Advertisement

Plant and Soil

, Volume 358, Issue 1–2, pp 201–212 | Cite as

Isolation and selection of plant growth-promoting rhizobacteria as inducers of systemic resistance in melon

  • Laura García-Gutiérrez
  • Diego Romero
  • Houda Zeriouh
  • Francisco M. Cazorla
  • Juan A. Torés
  • Antonio de Vicente
  • Alejandro Pérez-GarcíaEmail author
Regular Article

Abstract

Backgroud and aims

Powdery mildew elicited by Podosphaera fusca is an important threat to cucurbits. In order to find alternatives to the current use of chemicals, we examined the potential use of plant growth-promoting rhizobacteria (PGPR) for controlling the disease by induction of systemic resistance in the host plant.

Methods

A collection of Bacillus and Pseudomonas strains from different origins was studied, including strains isolated from roots of disease-free melon plants obtained from a greenhouse plagued by powdery mildew. The selection of best candidates was based on the evaluation of different traits commonly associated with PGPR, such as antifungal and siderophore production, swimming and swarming motilities, biofilm formation, auxin production and promotion of root development.

Results

Three Bacillus strains, B. subtilis UMAF6614 and UMAF6639 and B. cereus UMAF8564, and two Pseudomonas fluorescens strains, UMAF6031 and UMAF6033, were selected after ranking the strains using a nonparametric statistics test. Applied to melon seedlings, the selected strains were able to promote plant growth, increasing fresh weight up to 30%. Furthermore, these strains provided protection against powdery mildew and also against angular leaf spot caused by Pseudomonas syringae pv. lachrymans, with disease reductions of up to 60%.

Conclusions

These results suggest that the use of ISR-promoting PGPR could be a promising strategy for the integrated control of cucurbit powdery mildew and other cucurbit diseases.

Keywords

Bacillus cereus Bacillus subtilis Biological control Induced systemic resistance (ISR) Podosphaera fusca Powdery mildews Pseudomonas fluorescens 

Notes

Acknowledgements

This study was supported by grants from Plan Nacional de I+D+I of the Ministerio de Ciencia e Innovación, Spain (AGL2007-65340-C02-01 and AGL2010-21848-C02-01), cofinanced by FEDER funds (European Union).

References

  1. Ahimou F, Jacques P, Deleu M (2000) Surfactin and iturin A effects on Bacillus subtilis surface hydrophobicity. Enzyme Microb Technol 27:749–754PubMedCrossRefGoogle Scholar
  2. Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181PubMedCrossRefGoogle Scholar
  3. Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315CrossRefGoogle Scholar
  4. Arrebola E, Cazorla FM, Romero D, Pérez-García A, de Vicente A (2007) A nonribosomal peptide synthetase gene (mgoA) of Pseudomonas syringae pv. syringae is involved in mangotoxin biosynthesis and is required for full virulence. Mol Plant Microbe Interact 20:500–509PubMedCrossRefGoogle Scholar
  5. Bélanger RR, Labbé C (2002) Control of powdery mildews without chemicals: prophylactic and biological alternatives for horticultural crops. In: Bélanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews. A comprehensive treatise. APS Press, USA, pp 256–267Google Scholar
  6. Benhamou N, Kloepper JW, Tuzun S (1998) Induction of resistance against Fusarium wilt of tomato by combination of chitosan with an endophytic bacterial strain: ultrastructure and cytochemistry of the host response. Planta 204:153–168CrossRefGoogle Scholar
  7. Cazorla FM, Duckett SB, Bergström T, Noreen S, Odijk R, Lugtenberg BJJ, Thomas-Oates JE, Bloemberg GV (2006) Biocontrol of Dematophora root of avocado by antagonistic Pseudomonas fluorescens PCL1606 correlates with the production of 2-hexyl 5-propyl resorcinol. Mol Plant Microbe Interact 19:418–428PubMedCrossRefGoogle Scholar
  8. Cazorla FM, Romero D, Pérez-García A, Lugtenberg BJ, De Vicente A, Bloemberg GV (2007) Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J Appl Microbiol 103:1950–1959PubMedCrossRefGoogle Scholar
  9. Chambel L, Pelica F, Teodoro AM, Neves-Martins J, Palminha J (1994) Development of a new in vitro PGPR screening method. In: Proceedings of the Third International Workshop on Plant Growth-Promoting Rhizobacteria. Adelaide, Australia, p. 33Google Scholar
  10. Chen C, Bélanger R, Benhamou N, Paulitz TC (2000) Defense enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Phythium aphanidermatum. Physiol Mol Plant Pathol 56:13–23CrossRefGoogle Scholar
  11. Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Piel J, Borriss R (2009) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140:27–37PubMedCrossRefGoogle Scholar
  12. Codina JC, Cazorla FM, Pérez-García A, de Vicente A (2000) Heavy metal toxicity and genotoxicity in water and sewage determined by microbiological methods. Environ Toxicol Chem 19:1552–1558CrossRefGoogle Scholar
  13. Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959PubMedCrossRefGoogle Scholar
  14. Connelly MB, Young GM, Sloma A (2004) Extracellular proteolytic plays a central role in swarming motility in Bacillus subtilis. J Bacteriol 186:4159–4167PubMedCrossRefGoogle Scholar
  15. Dekkers LCCJ, de Weger BLA, Wijffelman CA, Spaink HP, Lugtenberg BJJ (1998) A two-component system plays an important role in the root-colonising ability of Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact 11:45–56PubMedCrossRefGoogle Scholar
  16. De Vleesschauwer D, Chernin L, Höfte MM (2009) Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice. BMC Plant Biol 9:9PubMedCrossRefGoogle Scholar
  17. Elad Y, Chet I, Baker R (1987) Increased growth response of plants induced by rhizobacteria antagonistic to soilborne pathogenic fungi. Plant Soil 98:325–330CrossRefGoogle Scholar
  18. Fernández-Ortuño D, Pérez-García A, López-Ruiz F, Romero D, de Vicente A, Torés JA (2006) Occurrence and distribution of resistance to QoI fungicides in populations of Podosphaera fusca in south central Spain. Eur J Plant Pathol 115:215–222CrossRefGoogle Scholar
  19. Friedman L, Kolter R (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675–690PubMedCrossRefGoogle Scholar
  20. Janda JM, Abbot SL (2010) The genus Aeromonas: taxonomy, pathogenicity and infection. Clin Microbiol Rev 23:35–73PubMedCrossRefGoogle Scholar
  21. Jeun YC, Park KS, Kim CH, Fowler WD, Kloepper JW (2004) Cytological observations of cucumber plants during induced resistance elicited by rhizobacteria. Biol Control 29:34–42CrossRefGoogle Scholar
  22. Joo G-J, Kim Y-M, Kim J-T, Rhee I-K, Kim J-H, Lee I-J (2005) Gibberellins-producing rhizobacteria increase endogenous gibberellins content and promote growth of red peppers. J Microbiol 43:510–515PubMedGoogle Scholar
  23. Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266PubMedCrossRefGoogle Scholar
  24. Latha P, Anand T, Ragupathi N, Prakasam V, Samiyappan R (2009) Antimicrobial activity of plant extracts and induction of systemic resistance in tomato plants by mixtures of PGPR strains and Zimmu leaf extract against Alternaria solani. Biol Control 50:85–93CrossRefGoogle Scholar
  25. López-Ruiz FJ, Pérez-García A, Fernández-Ortuño D, Romero D, García E, de Vicente A, Brown JKM, Torés JA (2010) Sensitivities to DMI fungicides in populations of Podosphaera fusca in south central Spain. Pest Manag Sci 66:801–808PubMedCrossRefGoogle Scholar
  26. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedCrossRefGoogle Scholar
  27. McGrath MT (2001) Fungicide resistance in cucurbit powdery mildew: experiences and challenges. Plant Dis 85:236–245CrossRefGoogle Scholar
  28. Ongena M, Jacques P, Touré Y, Destain J, Jabrane A, Thonart P (2005) Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potencial of Bacillus subtilis. Appl Environ Microbiol 69:29–38Google Scholar
  29. Ongena M, Adam A, Paquot M, Brams A, Joris B, Arpigny JL, Thonart P (2007) Surfactin and fengycin lipoptides of Bacillus subtilis as elecitors of induced systemic resistance in plant. Environ Microbiol 9:1084–1090PubMedCrossRefGoogle Scholar
  30. Pérez-García A, Olalla L, Rivera ME, del Pino D, Canovas I, de Vicente A, Torés JA (2001) Development of Sphaerotheca fusca on susceptible, resistant and temperature-sensitive resistant cultivars. Mycol Res 105:1216–1222CrossRefGoogle Scholar
  31. Pérez-García A, Romero D, Fernández-Ortuño D, López-Ruiz F, de Vicente A, Torés JA (2009) The powdery mildew fungus Podosphaera fusca (synonym Podosphaera xanthii), a constant threat to cucurbits. Mol Plant Pathol 10:153–160PubMedCrossRefGoogle Scholar
  32. Pérez-García A, Romero D, de Vicente A (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotechnol 22:187–193PubMedCrossRefGoogle Scholar
  33. 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 Protect 20:1–11CrossRefGoogle Scholar
  34. Raupach GS, Kloepper JW (1998) Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88:1158–1164PubMedCrossRefGoogle Scholar
  35. Romero D, Pérez-García A, Rivera ME, Cazorla FM, de Vicente A (2004) Isolation and evaluation of antagonist bacteria towards the cucurbit powdery mildew fungus Podosphaera fusca. Appl Microbiol Biotechnol 64:263–269PubMedCrossRefGoogle Scholar
  36. Romero D, de Vicente A, Rakotoaly RH, Dufour SE, Veening JW, Arrebola E, Cazorla FM, Kuipers OP, Paquot M, Pérez-García A (2007a) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant Microbe Interact 20:430–440PubMedCrossRefGoogle Scholar
  37. Romero D, de Vicente A, Zeriouh H, Cazorla FM, Fernandez-Ortuño D, Torés JA, Pérez-García A (2007b) Evaluation of biological control agents for managing cucurbit powdery mildew on greenhouse-grown melon. Plant Pathol 56:976–986CrossRefGoogle Scholar
  38. Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, Berg G, van der Lelie D, Dow JM (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7:514–525PubMedCrossRefGoogle Scholar
  39. Ryu CM, Hu CH, Reddy MS, Kloepper JW (2003) Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytol 160:413–420CrossRefGoogle Scholar
  40. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026PubMedCrossRefGoogle Scholar
  41. Schwym B, Neidlands JB (1987) Universal assay for the detection and determination of siderophores. Anal Biochem 160:47–56CrossRefGoogle Scholar
  42. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857PubMedCrossRefGoogle Scholar
  43. Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254CrossRefGoogle Scholar
  44. Van Loon LC, Bakker PA, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483PubMedCrossRefGoogle Scholar
  45. Verhagen BWM, Glazebrook J, Zhu T, Chang HS, Van Loon LC, Pieterse CMJ (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant Microbe Interact 17:895–908PubMedCrossRefGoogle Scholar
  46. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586CrossRefGoogle Scholar
  47. Zehnder GW, Murphy JF, Sikora EJ, Kloepper JW (2001) Application of rhizobacteria for induced resistance. Eur J Plant Pathol 107:39–50CrossRefGoogle Scholar
  48. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, GrimsonM FMA, Ryu CM, Allen R, Melo IS, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Laura García-Gutiérrez
    • 1
  • Diego Romero
    • 1
  • Houda Zeriouh
    • 1
  • Francisco M. Cazorla
    • 1
  • Juan A. Torés
    • 2
  • Antonio de Vicente
    • 1
  • Alejandro Pérez-García
    • 1
    Email author
  1. 1.Departamento de MicrobiologíaUniversidad de Málaga, Instituto de Hortofruticultura Subtropical y Mediterránea “La Mayora” (IHSM-UMA-CSIC)MálagaSpain
  2. 2.Instituto de Hortofruticultura Subtropical y Mediterránea “La Mayora” (IHSM-UMA-CSIC)MálagaSpain

Personalised recommendations