Skip to main content
SpringerLink
Log in

Biocontrol of Rhizoctonia solani: complex interaction of biocontrol strains, pathogen and indigenous microbial community in the rhizosphere of lettuce shown by molecular methods

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Co-inoculation of biocontrol agents with different modes of action is assumed to improve biocontrol activity. The present study aimed to investigate the effects of single or co-inoculation of Trichoderma viride strain GB7 and Serratia plymuthica strain 3Re4-18 on microbial communities in the rhizosphere of lettuce and their ability to suppress Rhizoctonia solani AG1-IB.

Methods

Growth chamber experiments with two different application modes were performed with single or co-inoculation of GB7 and 3Re4-18 in the presence or absence of R. solani. Biocontrol efficacy and plant growth parameters were assessed. Bacterial and fungal communities were analyzed by 16S rRNA gene and ITS fragments PCR-amplified from total community DNA of rhizosphere samples and analyzed by denaturing gradient gel electrophoresis.

Results

Compared to the single application, the co-inoculation of 3Re4-18 and GB7 resulted in an improved biocontrol efficacy. DGGE analysis revealed more pronounced effect on microbial community in co-inoculation treatment. The abundance of 3Re4-18 in the rhizosphere seemed to be increased in the presence of R. solani.

Conclusions

The applied cultivation-independent methods provided insights into the complex interaction in response to the pathogen and the antagonists. Co-inoculation resulted in an improved biocontrol efficacy and an increased evenness of the microbial communities.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abeysinghe S (2009) Effect of combined use of Bacillus subtilis CA32 and Trichoderma harzianum RU01 on biological control of Rhizoctonia solani on Solanum melongena and Capsicum annuum. Plant Pathol J 8:9–16

    Article  Google Scholar 

  • Adesina MF, Grosch R, Lembke A, Vatchev TD, Smalla K (2009) In vitro antagonists of Rhizoctonia solani tested on lettuce: rhizosphere competence, biocontrol efficiency and rhizosphere microbial community response. FEMS Microbiol Ecol 69:67–74

    Article  Google Scholar 

  • Berg G, Krechel A, Ditz M, Faupel A, Ulrich A, Hallmann J (2005) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51:215–229

    Article  PubMed  CAS  Google Scholar 

  • Blancard D, Lot H, Maisonneuve (2006) A color atlas of disease of lettuce and related salad crops: observation, biology and control. Elsevier, London

    Google Scholar 

  • Brewer MT, Larkin RP (2005) Efficacy of several potential biocontrol organisms against Rhizoctonia solani on potato. Crop Protect 24:939–950

    Article  Google Scholar 

  • Chellemi DO (2002) Nonchemical management of soilborne pests in fresh market vegetable production systems. Phytopathology 92:1367–1372

    Article  PubMed  CAS  Google Scholar 

  • De Curtis F, Lima G, Vitullo D, De Cicco V (2010) Biocontrol of Rhizoctonia solani and Sclerotium rolfsii on tomato by delivering antagonistic bacteria through a drip irrigation system. Crop Prot 29:663–670

    Article  Google Scholar 

  • 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 9:9

    Article  PubMed  Google Scholar 

  • Faltin F, Lottmann J, Grosch R, Berg G (2004) Strategy to select and assess antagonistic bacteria for biological control of Rhizoctonia solani Kühn. Can J Microbiol 50:811–820

    Article  PubMed  CAS  Google Scholar 

  • Felici C, Vettori L, Giraldi E, Forino LMC, Toffanin A, Tagliasacchi AM, Nuti M (2008) Single and co-inoculation of Bacillus subtilis and Azospirillum brasilense on Lycopersicon esculentum: effects on plant growth and rhizosphere microbial community. Appl Soil Ecol 40:260–270

    Article  Google Scholar 

  • González-García V, Portal Onco MA, Rubio Susan V (2006) Review. Biology and Systematics of the form genus Rhizoctonia. Span J Agric Res 4:55–79

    Google Scholar 

  • Götz M, Gomes NCM, Dratwinski A, Costa R, Berg G, Peixoto R, Mendonça-Hagler L, Smalla K (2006) Survival of gfp-tagged antagonistic bacteria in the rhizosphere of tomato plants and their effects on the indigenous bacterial community. FEMS Microbiol Ecol 56:207–218

    Article  PubMed  Google Scholar 

  • Gravel V, Martinez C, Antoun H, Tweddell RJ (2005) Antagonist microorganisms with the ability to control Pythium damping-off tomato seeds in rockwool. BioControl 50:771–786

    Article  Google Scholar 

  • Grosch R, Faltin F, Lottmann J, Kofoet A, Berg G (2005) Effectiveness of 3 antagonistic bacterial isolates to control Rhizoctonia solani Kühn on lettuce and potato. Can J Microbiol 51:345–353

    Article  PubMed  CAS  Google Scholar 

  • Grosch R, Koch T, Kofoet A (2006) Signum, ein neues Fungizid zur Bekämpfung der Salatfäule: Sicher gegen Rhizoctonia solani an Salat. Gemüse 42:14–16

    Google Scholar 

  • Grosch R, Rehn VNC, Rehn KG, Mendonça-Hagler L, Smalla K, Lottmann J, Berg G (2007) Analysis of antagonistic interactions between Trichoderma isolates from Brazilian weeds and the soil-borne pathogen Rhizoctonia solani. J Plant Dis Protect 114:167–175

    CAS  Google Scholar 

  • Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Rev Microbiol 3:307–319

    Article  CAS  Google Scholar 

  • Haichar FZ, Achouak W, Christen R, Heulin T, Marol Ch, Marais MF, Mougel Ch, Ranjard L, Balesdent J, Berge O (2007) Identification of cellulolytic bacteria in soil by stable isotope probing. Env Microbiol 9:625–634

    Article  Google Scholar 

  • Herschkovitz Y, Lerner A, Davidov Y, Rothballer M, Harmann A, Okon Y, Jurkevitch E (2005) Inoculation with the plant-growth-promoting rhizobacterium Azospirillum brasilense causes little disturbance in the rhizosphere and rhizoplane of maize (Zea mays). Microb Ecol 50:277–288

    Article  PubMed  CAS  Google Scholar 

  • Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241

    PubMed  CAS  Google Scholar 

  • Heuer H, Wieland G, Schönfeld J, Schönwälder A, Gomes NCM, Smalla K (2001) In: Rouchelle P (ed) Bacterial community profiling using DGGE or TGGE analysis. Environmental molecular microbiology: protocols and applications. Horizon Scientific Press, Wymondham, UK, pp 177–190

    Google Scholar 

  • Kozdroj J, Trevors JT, van Elsas JD (2004) Influence of introduced biocontrol agents on maize seedling growth and bacterial community structure in the rhizosphere. Soil Biol Biochem 36:1775–1784

    Article  CAS  Google Scholar 

  • Lahlali R, Hijri M (2010) Screening, identification and evaluation of potential biocontrol fungal endophytes against Rhizoctonia solani AG3 on potato plants. FEMS Microbial Letters 311:152–159

    Article  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  PubMed  CAS  Google Scholar 

  • Marimuthu S, Subbian P, Ramamoorthy V, Samiyappan R (2002) Synergistic effect of combined application of Azospirillum and Pseudomonas fluorescens with inorganic fertilizer on root rot incidence and yield of cotton. J Plant Dis Protect 109:569–577

    Google Scholar 

  • Martin FN (2003) Development of alternative strategies for management of soilborne pathogens currently controlled with methyl bromide. Ann Review Phytopathol 41:325–350

    Article  CAS  Google Scholar 

  • Meyer SLF, Roberts DP (2002) Combinations of biocontrol agents for management of plant-parasitic nematodes and soilborne plant-pathogenic fungi. J Nematol 34:1–8

    PubMed  Google Scholar 

  • Michelsen CF, Stougaard P (2011) A novel antifungal Pseudomonas fluorescens isolated from potato soils in Greenland. Curr Microbiol 62:1185–1192

    Article  PubMed  CAS  Google Scholar 

  • Müller H, Westendorf C, Leitner E, Chernin L, Riedel K, Schmidt S, Eberl L, Berg G (2009) Quorum-sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. FEMS Microbiol Ecol 67:468–478

    Article  PubMed  Google Scholar 

  • Pierson EA, Weller DM (1994) Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. Phytopathology 84:940–947

    Article  Google Scholar 

  • Raaijmakers JM, Weller DM (2001) Exploiting genotypic diversity of 2,4-diacetylphloroglucinol-producing Pseudomonas spp.: characterization of superior root-colonizing P. fluorescens strain Q8r1-96. Appl Environ Microbiol 67:2545–2554

    Article  PubMed  CAS  Google Scholar 

  • Raupach GS, Kloepper JW (1998) Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Biol Control 88:1158–1164

    CAS  Google Scholar 

  • Roberts DP, Lohrke SM, Meyer SLF, Buyer JS, Bowers JH, Baker CJ, Li W, de Souza JT, Lewis JA, Chung S (2005) Biocontrol agents applied individually and in combination for suppression of soilborne diseases of cucumber. Crop Prot 24:141–155

    Article  Google Scholar 

  • Robinson-Boyer L, Jeger MJ, Xu XM, Jeffries P (2009) Management of strawberry grey mold using mixtures of biocontrol agents with different mechanisms of action. Biocontrol Sci Techn 19:1051–1065

    Article  Google Scholar 

  • Scher FM, Ziegle JS, Kloepper JW (1994) A method for assessing the root-colonizing capacity of bacteria on maize. Can J Microbiol 30:151–157

    Article  Google Scholar 

  • Scherwinski K, Wolf A, Berg G (2007) Assessing the risk of biological control agents on the indigenous microbial communities: Serratia plymuthica HRO-C48 and Streptomyces sp. HRO-71 as model bacteria. BioControl 52:87–112

    Article  CAS  Google Scholar 

  • Schisler DA, Slininger PJ, Bothast RJ (1997) Effects of antagonist cell concentration and two-strain mixtures on biological control of Fusarium dry rot of potatoes. Phytopathology 87:177–183

    Article  PubMed  CAS  Google Scholar 

  • Schmidt CS, Agostini F, Simon AM, Whyte J, Townend J, Lifert C, Killham K, Mullins C (2004) Influence of soil type and pH on the colonization of sugar beet seedlings by antagonistic Pseudomonas and Bacillus strains, and on their control of Pythium damping-off. Eur J Plant Pathol 110:1025–1046

    Article  Google Scholar 

  • Van den Boogert PHJF, Luttikholt AJG (2004) Compatible biological and chemical control systems for Rhizoctonia solani in potato. Eur J Pl Pathol 110:111–118

    Article  Google Scholar 

  • Vargas Gil S, Meriles J, Conforto C, Basanta M, Radl V, Hagn A, Schloter M, March GJ (2011) Response of soil microbial communities to different management practices in surface soils of a soybean agroecosystem in Argentina. Eur J Soil Biol 47:55–60

    Article  CAS  Google Scholar 

  • Vestberg M, Kukkonen S, Saari K, Prikka P, Huttunen J, Tainio L, Devos N, Weekers F, Kevers C, Thonart P, Lemoine MC, Cordier C, Alabouvette C, Gianinazzi S (2004) Microbial inoculation for improving the growth and health of micropropagated strawberry. Appl Soil Ecol 27:243–258

    Article  Google Scholar 

  • Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NC, Schloter M et al (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microbiol 75:3859–3865

    Article  PubMed  CAS  Google Scholar 

  • Wilson P, Ahvenniemi P, Lehtonen M (2008) Biological and chemical control and their combined use to control different stages of the Rhizoctonia disease complex on potato through the growing season. Ann Appl Biol 153:307–320

    Article  Google Scholar 

  • Xu XM, Robinson J, Jeger M, Jeffries P (2010) Using combinations of biocontrol agents to control Botrytis cinerea on strawberry leaves under fluctuating temperatures. Biocontrol Sci Techn 4:359–373

    Article  Google Scholar 

  • Zachow Ch, Fatehi J, Cardinale M, Tilcher R, Berg G (2010) Strain-specific colonization pattern of Rhizoctonia antagonists in the root system of sugar beet. FEMS Microbiol Ecol 74:124–135

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the bilateral project between Brazil and Germany funded by the BMBF BRA 05/021 and the DFG SM59/11-1/GR568121. We would also like to thank Angelika Fandrey for her skilled technical assistance and Christin Zachow for her helpful comments.

Author information

Authors and Affiliations

  1. Leibniz-Institute of Vegetable and Ornamental Crops, Theodor-Echtermeyer-Weg 1, 14979, Großbeeren, Germany

    Rita Grosch

  2. Julius Kühn-Institut - Federal Research Centre for Cultivated Plants (JKI), Institute for Epidemiology and Pathogen Diagnostics, Messeweg 11-12, 38104, Braunschweig, Germany

    Simone Dealtry, Susanne Schreiter & Kornelia Smalla

  3. Graz University of Technology, Institute for Environmental Biotechnology, Petersgasse 12, 8010, Graz, Austria

    Gabriele Berg

  4. Universidade Federal do Rio de Janeiro, Instituto de Microbiologia Prof. Paulo de Departmento de Microbiologia Geral-UFRJ Góes, CCS Bloco I SS04, Ilha do Fundao, RJ, 21941-590, Rio de Janeiro, Brazil

    Simone Dealtry & Leda Mendonça-Hagler

Authors
  1. Rita Grosch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simone Dealtry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susanne Schreiter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriele Berg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Leda Mendonça-Hagler
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kornelia Smalla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rita Grosch.

Additional information

Responsible Editor: Bernard Glick.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grosch, R., Dealtry, S., Schreiter, S. et al. Biocontrol of Rhizoctonia solani: complex interaction of biocontrol strains, pathogen and indigenous microbial community in the rhizosphere of lettuce shown by molecular methods. Plant Soil 361, 343–357 (2012). https://doi.org/10.1007/s11104-012-1239-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-012-1239-y

Keywords

Search

Navigation