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Detection and Characterization of Endobacteria in the Fungal Endophyte Piriformospora indica

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Modern Tools and Techniques to Understand Microbes

Abstract

The nonpathogenic Alphaproteobacterium Rhizobium radiobacter (syn. Agrobacterium tumefaciens) (RrF4) is a subculture of the endobacterium R. radiobacter, which is intricately associated with its host, the beneficial plant-colonizing fungal basidiomycete Piriformospora indica. RrF4 is genetically very similar to the well-studied plant pathogenic R. radiobacter biovar I strain C58 (genomovar G8). Highly similar genetic content of RrF4 and C58 denotes the high potential for RrF4 to directly interact with plants. The failure to cure P. indica from its endobacterium still hampers a conclusive prediction of the bacterium’s extended role in the interaction of the fungus with a broad spectrum of host plants. However, beneficial activities shown in cereals and the Brassicaceae Arabidopsis thaliana were hardly distinguishable when induced either by RrF4 or P. indica. We discuss here the various strategies employed to detect, characterize, and eventually elucidate the endobacterium’s role in the tripartite symbiosis with its fungal host and a plant.

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References

  • Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC genomics 12:402. doi:10.1186/1471-2164-12-402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baltruschat B, Fodor J, Harrach B, Niemczyk E, Schwarzinger I, Barna B, Gullner G, Zuccaro A, Schäfer P, Kogel KH, Skoczowski A (2008) Salt tolerance induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist 180:501–510

    Article  CAS  PubMed  Google Scholar 

  • Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148. doi:10.3389/fmicb.2014.00148

    PubMed  PubMed Central  Google Scholar 

  • Bertaux J, Schmid M, Hutzler P, Hartmann A, Garbaye J, Frey-Klett P (2005) Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Environ Microbiol 7:1786–1795

    Article  CAS  PubMed  Google Scholar 

  • Bertaux J, Schmid M, Prévost-Bourre NC, Churin JL, Hartmann A, Garbaye J et al (2003) In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. App Environ Microbiol 69:4243–4248

    Article  CAS  Google Scholar 

  • Blom J, Albaum SP, Doppmeier D, Pühler A, Vorhölter FJ, Jewski MZ et al (2009) EDGAR: A software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10:154. doi:10.1186/1471-2105-10-154

    Article  PubMed  PubMed Central  Google Scholar 

  • Blom J, Kreis J, Spänig S, Juhre T, Bertelli C, Ernst C, Goesmann A (2016) EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic acids research 44:22–28

    Article  Google Scholar 

  • Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383

    Article  CAS  PubMed  Google Scholar 

  • Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, Lee J et al (2010) Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytologist 185:1062–1073

    Article  CAS  PubMed  Google Scholar 

  • Deshmukh SD, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M et al (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Desirò A, Faccio A, Kaech A, Bidartondo MI, Bonfante P (2015) Endogone, one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria. New Phytol 205:1464–1472

    Article  PubMed  Google Scholar 

  • Frost LS, Ippen-Ihler K, Skurray RA (1994) Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol Rev 58:162–210

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fuqua WC, Winans SC (1994) A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. J Bacteriol 176:2796–2806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glaeser SP, Imani J, Alabid I, Guo H, Kämpfer P, Hardt M, Blom J, Goesmann A, Rothballer M, Hartmann A, Kogel KH (2016) Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica. ISME J 10:871–884

    Article  PubMed  Google Scholar 

  • Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B et al (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323–2328

    Article  CAS  PubMed  Google Scholar 

  • Harrach BD, Baltruschat H, Barna B, Fodor J, Kogel KH (2013) The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. MPMI 26:599–604

    Article  CAS  PubMed  Google Scholar 

  • Hoffman MT, Arnold AE (2010) Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 76:4063–4075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V et al (2011) Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 156:726–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kai K, Furuyabu K, Tani A, Hayashi H (2012) Production of the quorum-sensing molecules N-acylhomoserine lactones by endobacteria associated with Mortierella alpina A-178. Chembiochem 13:1776–1784

    Article  CAS  PubMed  Google Scholar 

  • Kaprelyants AS, Gottschal JC, Kell DB (1993) Dormancy in non-sporulating bacteria. FEMS Microbiol Rev 10:271–285

    Article  CAS  PubMed  Google Scholar 

  • Lackner G, Möbius N, Scherlach K, Partida-Martinez LP, Winkler R, Schmitt I, Hertweck C (2009) Global distribution and evolution of a toxinogenic Burkholderia-Rhizopus symbiosis. Appl Environ Microbiol 75:2982–2986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lackner G, Moebius N, Partida-Martinez LP, Boland S, Hertweck C (2011) Evolution of an endofungal lifestyle: Deductions from the Burkholderia rhizoxinica genome. BMC Genomics 12:210. doi:10.1186/1471-2164-12-210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li D (2011) Phenotypic variation and molecular signaling in the interaction of the rhizosphere bacteria Acidovorax sp, N35 and Rhizobium radiobacter F4 with roots. Faculty of Biology, Ludwig Maximilian University München, Germany, Dissertation

    Google Scholar 

  • Lumini E, Bianciotto V, Jargeat P, Novero M, Salvioli A, Faccio A, Bécard G, Bonfante P (2007) Presymbiotic growth and sporal morphology are affected in the arbuscular mycorrhizal fungus Gigaspora margarita cured of its endobacteria. Cell Microbiol 9:1716–1729

    Article  CAS  PubMed  Google Scholar 

  • Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J et al (2003) GenDB--an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31:2187–2195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naumann M, Schüssler A, Bonfante P (2010) The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME J 4:862–871

    Article  PubMed  Google Scholar 

  • Oberwinkler F, Riess K, Bauer R, Garnica S (2014) Morphology and molecules: the Sebacinales, a case study. Mycological Progress 13:445–470

    Article  Google Scholar 

  • Oliver JD (2005) The viable but nonculturable state in bacteria. J Microbiol 43:93–100

    PubMed  Google Scholar 

  • Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–888

    Article  CAS  PubMed  Google Scholar 

  • Peškan-Berghöfer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V et al (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plant 122:465–477

    Article  Google Scholar 

  • Piper WE, Ogrodniczuk JS, Joyce AS, McCallum M, Rosie JS, O'Kelly JG et al (1999) Prediction of dropping out in time-limited, interpretive individual psychotherapy. Psyc NET 36:114–122

    Google Scholar 

  • Qiang X, Weiss M, Kogel KH, Schäfer P (2012a) Piriformospora indica - a mutualistic basidiomycete with an exceptionally large plant host range. Mol Plant Pathol 13:508–518

    Article  CAS  PubMed  Google Scholar 

  • Qiang X, Zechmann B, Reitz MU, Kogel KH, Schäfer P (2012b) The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an ER stress-triggered caspase-dependent cell death. Plant Cell 24:794–809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiss K, Oberwinkler F, Bauer R, Garnicaet S (2014) Communities of endophytic sebacinales associated with roots of herbaceous plants in agricultural and grassland ecosystems are dominated by Serendipita herbamans sp. nov. PLoS ONE 9:e94676. doi:10.1371/journal.pone.0094676

    Article  Google Scholar 

  • Schenk ST, Hernández-Reyes C, Samans B, Stein E, Neumann C, Schikora M, Reichelt M, Mithöfer A, Becker A, Kogel KH, Schikora A (2014) N-Acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell. doi:10.1105/tpc.114.126763

    PubMed  PubMed Central  Google Scholar 

  • Schikora A, Schenk ST, Stein E, Molitor A, Zuccaro A, Kogel KH (2011) N-acyl-homoserine lactone confers resistance towards biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiol 157:1407–1418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma M, Schmid M, Rothballer M, Hause G, Zuccaro A, Imani J et al (2008) Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiol 11:2235–2246

    Article  Google Scholar 

  • Stein E, Molitor A, Kogel KH, Waller F (2008) Systemic resistance conferred by the root endophyte Piriformospora indica to Arabidopsis requires jasmonic acid and the cytoplasmic function of NPR1. Plant Cell Physiol 49:1747–1751

    Article  CAS  PubMed  Google Scholar 

  • Varma A, Bakshi M, Lou B, Hartmann A, Oelmueller R (2012) Piriformospora indica: a novel plant growth-promoting mycorrhizal fungus. Agric Res 1:117–131

    Article  Google Scholar 

  • Varma A, Verma S, Sudah SN, Franken P (1999) Piriformospora indica, a cultivable plant growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walker V, Bruto M, Bellvert F, Bally R, Muller D, Prigent-Combaret C, Moënne-Loccoz Y, Comte G (2013) Unexpected phytostimulatory behavior for Escherichia coli and Agrobacterium tumefaciens model strains. Mol Plant-Microbe Interact. 26:495–502

    Article  CAS  PubMed  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss M, Selosse MA, Rexer KH, Urban A, Oberwinkler F (2011) Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. PLOS ONE Res 108:1003–1010

    Google Scholar 

  • Ye W, Shen CH, Lin Y, Chen PJ, Xu X, Oelmüller R et al (2014) Growth promotion-related miRNAs in Oncidium orchid roots colonized by the endophytic fungus Piriformospora indica. PLoS ONE 9:e84920

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, Biedenkopf D et al (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathogens 7:e1002290. doi:10.1371/journal.ppat.1002290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgment

This work was supported by the German Science Foundation (DFG) to KHK (KO 1208/24-1) and PK (DFG KA 875/8-1). We acknowledge technical assistance by the Bioinformatics Core Facility at JLU Giessen and access to resources supported by the Bundesministerium fﺰr Bildung und Forschung (BMBF) grant FKZ 031A533 to AG within the de.NBI network.

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Correspondence to Karl-Heinz Kogel .

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Glaeser, S.P. et al. (2017). Detection and Characterization of Endobacteria in the Fungal Endophyte Piriformospora indica . In: Varma, A., Sharma, A. (eds) Modern Tools and Techniques to Understand Microbes. Springer, Cham. https://doi.org/10.1007/978-3-319-49197-4_15

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