Skip to main content
SpringerLink
Log in
Book cover

Piriformospora indica pp 201–219Cite as

Inhibitory Interactions of Rhizobacteria with the Symbiotic Fungus Piriformospora indica

  • Chapter
  • First Online:

Part of the book series: Soil Biology ((SOILBIOL,volume 33))

Abstract

Interactions between plant growth-promoting rhizobacteria (PGPRs) and the symbiotic plant growth-promoting fungus Piriformospora indica were demonstrated by adopting several working models. Different rhizobacteria either inhibit, promote, or have no influence on stimulatory effect of P. indica in gnotobiotic barley plants. In particular, it was demonstrated that, e.g., Pseudomonas fluorescens WS5 and Burkholderia cepacia LA3 inhibited the growth and development of P. indica including complete blockage of sporulation (chlamydospores). The interaction with Ps. fluorescens turned out to be “fungistatic” as well as “fungicidal” in nature. TEM study showed the degradation of cell walls. Gas chromatography/mass spectrometry ion fragmentation pattern suggests that one of the interactive compounds is pyoverdine—a potent siderophore. On the other hand, the severe inhibition of the P. indica by the excreted metabolites of B. cepacia was described at the metabolome level applying high accurate mass spectrometer measurements. It was observed that several pathways were deactivated in the fungus, but a few of them, like ubiquinone biosynthesis, limonene, and pinene degradation, were activated since increased number of metabolites was annotated. Saponin, a biosurfactant, also inhibited the fungus but did not affect the ubiquinone biosynthesis and the limonene–pinene degradation. The study clearly demonstrated that there is intense interaction at metabolome level between rhizobacteria, P. indica, and plant components. A balance maintained due to stimulation and inhibition of the fungus by different rhizobacteria appears to be one of the major factors responsible for fungal diversity, abundance, and function in the rhizosphere. The study opens new vistas to understand delicate balance among mycorrhizospheric organisms that largely allow diverse microbes to coexist and share common resources.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

    PubMed  CAS  Google Scholar 

  • Barazani O, Benderoth M, Groten K, Kuhlemeier C, Baldwin IT (2005) Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 146:234–243

    Article  PubMed  Google Scholar 

  • Barea JM, Azcon R, Azcon-Aguilar C (2004) Mycorrhizal fungi and plant growth promoting rhizobacteria. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, Germany, pp 351–362

    Google Scholar 

  • Bassler BL (2002) Small talk. Cell-to-cell communication in bacteria. Cell 109:421–424

    Article  PubMed  CAS  Google Scholar 

  • Chen XH, Vater J, Piel J, Franke P, Scholz R, Schneider K, Koumoutsi A, Hitzeroth G, Grammel N, Strittmatter AW, Gottschalk G, Süssmuth RD, Borriss R (2007) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB42. J Bacteriol 188:4024–4036

    Article  Google Scholar 

  • Deshmukh S, Hueckelhoven R, Schaefer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci USA 103:18450–18457

    Article  PubMed  CAS  Google Scholar 

  • Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59

    Article  CAS  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  PubMed  CAS  Google Scholar 

  • Fuchs R, Budzikiewicz H (2000) Structural studies of pyoverdines with cyclopeptidic substructures by electrospray ionization and collision induced fragmentation. Spectroscopy 14:229–246

    Article  CAS  Google Scholar 

  • Fuchs R, Budzikiewicz H (2001) Structural studies of pyoverdines by mass spectrometry. Curr Organ Chem 5:265–288

    Article  CAS  Google Scholar 

  • Garbaye J (1994) Tansley Review No. 76 Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–200

    Article  Google Scholar 

  • Glen M, Tommerup IC, Bougher NL, O’Brien PA (2002) Are Sebacinaceae common and widespread ectomycorrhizal associates of Eucalyptus spp. Mycorrhiza 12:243–247

    Article  PubMed  CAS  Google Scholar 

  • Hampp R, Maier A (2004) Interaction between soil bacteria and ectomycorrhiza-forming fungi. In: Varma A, Abbott LK, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, Germany

    Google Scholar 

  • Jha B, Thakur MC, Gontia I, Albrecht V, Stoffels M, Schmid M, Hartmann A (2009) Isolation, partial identification and application of diazotrophic rhizobacteria from traditional Indian rice cultivars. Eur J Soil Biol 45:62–72

    Article  CAS  Google Scholar 

  • Kilz S, Lenz C, Fuchs R, Budzikiewicz H (1999) A fast screening method for the identification of siderophores from fluorescent Pseudomonas spp. by liquid chromatography/electrospray mass spectrometry. J Mass Spectrometry 34:281–290

    Article  CAS  Google Scholar 

  • Kottke I, Beiter A, Weiss M, Haug I, Oberwinkler F, Nebel M (2003) Basal hymenomycetes belonging to the Sebacinaceae are ectomycorrhizal on temperate deciduous trees. Mycol Res 107:957–968

    Article  PubMed  Google Scholar 

  • Koumoutsi A, Chen X-H, Vater J, Borriss R (2007) DegU and YczE positively regulate the synthesis of Bacillomycin D by Bacillus amyloliquefaciens strain FZB42. Appl Environ Microbiol 73:6953–6964

    Article  PubMed  CAS  Google Scholar 

  • Lehr NA, Schrey SD, Bauer R, Hampp R, Tarkka MT (2007) Suppression of plant defence response by a mycorrhizal helper bacterium. New Phytol 174:892–903

    Article  PubMed  CAS  Google Scholar 

  • Mazzola M, Zhao X, Cohen MF, Raaijmakers JM (2007) Cyclic lipopeptide surfactant production by Pseudomonas fluorescens SS101 is not required for suppression of complex Pythium spp. populations. Phytopathology 97:1348–1355

    Article  PubMed  CAS  Google Scholar 

  • Oelmueller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica: a novel multifunctional symbiotic fungus. Symbiosis 49:1–18

    Article  CAS  Google Scholar 

  • Onega M, Jacques P (2007) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125

    Google Scholar 

  • Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant–rhizobacteria interactions. Plant Cell Environ 26:189–199

    Article  CAS  Google Scholar 

  • Peskan-Berghofer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, Oelmueller R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represent a novel system to study beneficial plant–microbe interactions and involve in early plant protein modifications in the endocytoplasmic reticulum and in the plasma membrane. Physiol Plant 122:465–477

    Article  Google Scholar 

  • Pham HG, Kumari R, Singh A, Malla R, Prasad R, Sachdev M, Kaldorf M, Buscot F, Oelmueller R, Hampp R, Saxena AK, Rexer KH, Kost G, Varma A (2004) Axenic cultures of Piriformospora indica. In: Varma A, Abbott LK, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, Germany, pp 593–613

    Google Scholar 

  • Raaijmakers JM, de Bruijn I, de Kock MJD (2006) Cyclic lipopeptide production by plant-associated Pseudomonas species: diversity, activity, biosynthesis and regulation. Mol Plant Microbe Interact 19:699–710

    Article  PubMed  CAS  Google Scholar 

  • Raajimakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere. A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361

    Article  Google Scholar 

  • Ryan PR, Dessaux Y, Thomashow LS, Weller DM (2009) Rhizosphere engineering and management for sustainable agriculture. Plant Soil 321:363–383

    Article  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932

    Article  PubMed  CAS  Google Scholar 

  • Sahay NS, Varma A (1999) Piriformospora indica: a new biological hardening tool for micropropagated plants. FEMS Microbiol Lett 181:297–302

    Article  PubMed  CAS  Google Scholar 

  • Selosse MA, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878

    Article  PubMed  CAS  Google Scholar 

  • Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531

    Article  PubMed  CAS  Google Scholar 

  • Shahollari B, Vadassery J, Varma A, Oelmueller R (2007) A leucine rich repeat protein is required for growth promotion and enhanced seed production mediated by the endophytic fungus Piriformospora indica in Arabidopsis thaliana. Plant J 50:1–13

    Article  PubMed  CAS  Google Scholar 

  • Shahollari B, Varma A, Oelmueller R (2005) Expression of a receptor kinase in Arabidopsis roots is stimulated by the basidiomycete Piriformospora indica and the protein accumulates in Triton X-100 insoluble plasma membrane microdomains. J Plant Physiol 162:945–958

    Article  PubMed  CAS  Google Scholar 

  • Sharma M, Schmid M, Rothballer M, Hause G, Zuccaro A, Imani J, Schäfer P, Hartmann A, Kogel K-H (2008) Detection and identification of mycorrhiza helper bacteria intimately associated with representatives of the order Sebacinales. Cell Microbiol 10:2235–2246

    Article  PubMed  CAS  Google Scholar 

  • Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmueller R (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor which binds to a conserved motif in their promoters. J Biol Chem 280:26241–26247

    Article  PubMed  CAS  Google Scholar 

  • Sherameti I, Tripathi S, Varma A, Oelmuller R (2008a) The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress–related genes in leaves. Mol Plant Microbe Interact 21:799–807

    Article  PubMed  CAS  Google Scholar 

  • Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM, Nitz I, Varma A, Grundler FM, Oelmueller R (2008b) PYK10, a β-glucosidase located in the endoplasmic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 54:428–439

    Article  PubMed  CAS  Google Scholar 

  • Suhre K, Schmitt-Kopplin P (2008) MassTRIX: mass translator into pathways. Nucl Acid Res 36:W481–W484

    Article  CAS  Google Scholar 

  • Szkopinska A (2000) Ubiquinone biosynthesis of quinone ring and its isoprenoid side chain. Intracellular localization. Acta Biochimica Polonica 47:469–480

    PubMed  CAS  Google Scholar 

  • Thrane C, Olsson S, Nielsen TH, Sorensen J (1999) The use of vital fluorescent probes for the detection of stress in the fungi Pythium ultimum and Rhizoctonia solani challenged with viscosinamide from Pseudomonas fluorescens DR54. FEMS Microbiol Ecol 30:11–23

    Article  CAS  Google Scholar 

  • Urban A, Weiss M, Bauer R (2003) Ectomycorrhizas involving sebacinoid mycobionts. Mycol Res 107:3–14

    Article  PubMed  Google Scholar 

  • Vadassery J, Tripathi S, Prasad R, Varma A, Oelmueller R (2009) Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J Plant Physiol 165:60–70

    Google Scholar 

  • Varma A, Singh A, Sudha M, Sahay NS, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D, Bharti K, Hurek T, Blechert O, Rexer KH, Kost G, Hahn A, Maier W, Walter M, Strack D, Kranner I (2001) Piriformospora indica: a cultivable mycorrhiza-like endosymbiotic fungus. In: Hock B (ed) The mycota 9. Springer, Berlin, Germany, pp 125–150

    Google Scholar 

  • Varma A, Verma S, Sudha, Sahay N, Butehorn B, Franken P (1999) Piriformospora indica—a cultivable plant growth promoting root endophyte with similarities to arbuscular mycorrhizal fungi. Appl Environ Microbiol 65:2741–2744

    PubMed  CAS  Google Scholar 

  • Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Butehorn B, Franken P (1998) Piriformospora indica gen. nov., a new root-colonizing fungus. Mycologia 90:896–903

    Article  CAS  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hueckelhoven R, Neumann C, von Wettstein D et al (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391

    Article  PubMed  CAS  Google Scholar 

  • Weiss M, Selosse MA, Rexer KH, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Authors cordially thank Prof. Dr. Rainer Borriss (Humboldt University Berlin) for the provision with the Bacillus amyloliquefaciens FZB42 mutants and Prof. Dr. Jos Raaijimakers (Wageningen University, The Netherlands) for the kind supply with Ps. fluorescens SS101, its mutant 10.24, and a sample of pure massetolide A. Critical comments received from Prof. Paola Bonfante (Turin, Italy) are highly appreciated. Ajit Varma is thankful to Department of Biotechnology, New Delhi, for partial financial assistance.

Author information

Authors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University, Block E-3, Sector 125, Noida, UP, India

    Ajit Varma & Swati Tripathi

  2. Helmholtz Zentrum München, German Research Center for Environmental Health, Research Unit Analytical Biogeochemistry, Ingolstaedter Landstrasse 1, 85764, Neuherberg, Germany

    Agnes Fekete, Moritz Frommberger & Philippe Schmitt-Kopplin

  3. School of Engineering and Sciences, International University of Bremen, Campus Ring 6, 28759, Bremen, Germany

    Abhishek Srivastava

  4. Divisions of Microbiology, Indian Agricultural Research Institute, New Delhi, 110012, India

    Anil K Saxena

  5. Research Unit Microbe–Plant Interactions, Helmholtz Zentrum München, German Research Center for Environmental Health, Ingolstaedter Landstrasse 1, 85764, Neuherberg, Germany

    Dan Li, Silvia Gschwendter & Anton Hartmann

  6. Institute for General Botany and Plant Physiology, Friedrich-Schiller University of Jena, Biology and Pharmacy Faculty, Domburger Street 159, 07743, Jena, Germany

    Irena Sherameti & Ralf Oelmueller

Authors
  1. Ajit Varma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Agnes Fekete
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abhishek Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anil K Saxena
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Moritz Frommberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Silvia Gschwendter
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Irena Sherameti
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ralf Oelmueller
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Philippe Schmitt-Kopplin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Swati Tripathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Anton Hartmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anton Hartmann .

Editor information

Editors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, E-3 Block, Sector 125, Noida, 201303, Uttar Pradesh, India

    Ajit Varma

  2. , FB Biology, Systematic Botany & Mycology, Philipps University of Marburg, Karl von Frisch Str. 8, Marburg, 35032, Germany

    Gerhard Kost

  3. Inst. Allgemeine Botanik, LS Pflanzenphysiologie, Univ. Jena, Dornburger Str. 159, Jena, 07743, Thüringen, Germany

    Ralf Oelmüller

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Varma, A. et al. (2013). Inhibitory Interactions of Rhizobacteria with the Symbiotic Fungus Piriformospora indica . In: Varma, A., Kost, G., Oelmüller, R. (eds) Piriformospora indica. Soil Biology, vol 33. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-33802-1_12

Download citation

Publish with us

Policies and ethics

Search

Navigation