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Volumes published in the series
Volume 1A. Singh, O.P. Ward (Eds.)Applied Bioremediation and Phytoremediation2004
Volume 2A. Singh, O.P. Ward (Eds.)Biodegradation and Bioremediation2004
Volume 3F. Buscot, A. Varma (Eds.)Microorganisms in Soils: Roles in Genesis and Functions2005
Volume 4S. Declerck, D.-G. Strullu, J.A. Fortin (Eds.)In Vitro Culture of Mycorrhizas2005
Volume 5R. Margesin, F. Schinner (Eds.)Manual for Soil Analysis –Monitoring and Assessing Soil Bioremediation2005
Volume 6H. König, A. Varma (Eds.)Intestinal Microorganisms of Termitesand Other Invertebrates2006
Volume 7K.G. Mukerji, C. Manoharachary, J. Singh (Eds.)Microbial Activity in the Rhizosphere2006
Volume 8P. Nannipieri, K. Smalla (Eds.)Nucleic Acids and Proteins in Soil2006
Barbara J.E. SchulzChristine J.C. BoyleThomas N. Sieber (Eds.)
Microbial RootEndophytesWith 29 Figures, 4 in Color
123
PD Dr. Barbara J. E. SchulzTechnical University of BraunschweigInstitute of MicrobiologySpielmannstraße 738106 BraunschweigGermanye-mail: [email protected]
Dr. Christine J. C. BoyleAugustastraße 3202826 GörlitzGermanye-mail: [email protected]
Dr. Thomas N. SieberSwiss Federal Institute of TechnologyDepartment of Environmental SciencesInstitute of Integrative BiologyForest Pathology and Dendrology8092 ZürichSwitzerlande-mail: [email protected]
Library of Congress Control Number: 2005938057
ISSN 1613-3382ISBN-10 3-540-33525-0 Springer Berlin Heidelberg New YorkISBN-13 978-3-540-33525-2 Springer Berlin Heidelberg New York
This work is subject to copyright. All rights reserved, whether the whole or part of thematerial is concerned, specifically the rights of translation, reprinting, reuse of illustrations,recitation, broadcasting, reproduction on microfilm or in any other way, and storage in databanks.Duplicationof thispublicationorparts thereof is permittedonlyunder theprovisionsof the German Copyright Law of September 9, 1965, in its current version, and permissionfor use must always be obtained from Springer. Violations are liable for prosecution underthe German Copyright Law.
Springer is a part of Springer Science + Business Mediaspringer.com
© Springer-Verlag Berlin Heidelberg 2006Printed in Germany
The use of general descriptive names, registered names, trademarks, etc. in this publicationdoes not imply, even in the absence of a specific statement, that such names are exemptfrom the relevant protective laws and regulations and therefore free for general use.
Editor: Dr. Dieter Czeschlik, Heidelberg, GermanyDesk Editor: Dr. Jutta Lindenborn, Heidelberg, GermanyCover design: design&production, Heidelberg, GermanyTypesetting and production: LE-TEX Jelonek, Schmidt & Vöckler GbR, Leipzig, Germany31/3150-YL - 5 4 3 2 1 0 - Printed on acid-free paper
Preface
Healthy plant roots are not only colonized by mycorrhizal fungi and rhi-zobial bacteria, but also by a myriad of other microorganisms, includingendophytic bacteria and fungi. Comparatively little is known about theseendophytic microorganisms, which do not cause apparent disease, butcolonize root tissues inter- and/or intracellulary. Although there had beenprevious research studying both bacterial and fungal endophytes, it wasin the mid-1980s that numerous investigators began studying these groupsof microorganisms more intensively. Initially, most work on endophytescentered on the diversity of isolates and correlations with ecological fac-tors. Recently it has become clear that some of these interactions withendophytic bacteria and fungi can be latently pathogenic and/or mutualis-tic. In mutualistic interactions, the endophyte may improve growth of thehost, convey stress tolerance, induce systemic resistance, or supply the hostwith nutrients. On the other hand, most endophytes are also able to growsaprotrophically, e.g., from surface-sterilized tissues on media containingdead organic substrates. Thus, it has become obvious that endophytes havemultiple life history strategies and that these can be extremely plastic, aswill become clear to the readers of the subsequent 19 chapters.
This book is the first to deal with bacterial and fungal root endophytes,their diversity, life history strategies, interactions, applications in agricul-ture and forestry, and also with methods for isolation, cultivation, and bothconventional and molecular methods for identification and detection. Thefirst chapter deals with the question: What are endophytes? However, italso introduces the reader to the subjects treated in the subsequent chap-ters. We hope that readers will not only find this book informative, butwill also be provoked to further study these fascinating interactions, andin particular to better understand the mechanisms regulating them. It willbecome apparent that we are still far from understanding the factors thatdetermine whether a plant-microbial interaction remains asymptomatic,leads to disease, or is mutualistic.
VI Preface
We would like to thank our colleagues for their contributions and theirwork to make this book a successful unity, to Jutta Lindenborn of Springerfor her friendly help and advice, and to Ajit Varma for the invitation to edita book in this series.
Braunschweig, Barbara SchulzGörlitz and Zürich, Christine BoyleJune 2006 and Thomas Sieber
Contents
1 What are Endophytes? 1Barbara Schulz, Christine Boyle1.1 Introduction and Definitions ............................................ 11.2 Colonisation .................................................................. 21.3 Assemblages and Adaptation ............................................ 41.4 Life History Strategies ..................................................... 61.5 Balanced Antagonism...................................................... 71.6 Conclusions ................................................................... 9References ............................................................................. 10
Part I Endophytic Bacteria
2 Spectrum and Population Dynamicsof Bacterial Root Endophytes 15Johannes Hallmann, Gabriele Berg2.1 Introduction .................................................................. 152.2 Population Density ......................................................... 152.3 Bacterial Spectrum ......................................................... 162.4 Bacterial Diversity .......................................................... 212.5 Factors Influencing Colonisation....................................... 21
2.5.1 Methodology ....................................................... 212.5.2 Geography .......................................................... 222.5.3 Plant Species ....................................................... 222.5.4 Plant Genotype .................................................... 23
2.6 Interactions ................................................................... 242.6.1 Plant Pathogens ................................................... 242.6.2 Plant Symbionts ................................................... 252.6.3 Plant Defence Mechanisms .................................... 252.6.4 Agricultural Practices ........................................... 25
2.7 Potential Human Pathogens Among Root Endophytes.......... 262.8 Conclusions ................................................................... 27References ............................................................................. 28
VIII Contents
3 Bacterial Endophytes as Elicitors of Induced Systemic Resistance 33Joseph W. Kloepper, Choong-Min Ryu3.1 Introduction and Terminology ......................................... 333.2 Scope of Endophytes that Elicit Induced Resistance
and Pathosystems Affected............................................... 343.3 Internal Colonization of Endophytes
that Elicit Induced Resistance ........................................... 393.4 Plant Responses to Endophytic Elicitors ............................. 413.5 Implementation in Production Agriculture:
Two Case Studies ............................................................ 443.6 Conclusions ................................................................... 49References ............................................................................. 50
4 Control of Plant Pathogenic Fungi with Bacterial Endophytes 53Gabriele Berg, Johannes Hallmann4.1 Introduction .................................................................. 534.2 Spectrum of Indigenous Endophytic Bacteria
with Antagonistic Potential Towards Fungal Plant Pathogens 544.3 Mode of Action of Antagonistic Bacteria ............................ 58
4.3.1 Antibiosis ........................................................... 584.3.2 Competition ........................................................ 594.3.3 Lysis ................................................................... 594.3.4 Induction of Plant Defence Mechanisms .................. 604.3.5 Plant Growth ....................................................... 60
4.4 Control Potential of Endophytic Bacteria............................ 604.5 Enhancing Biocontrol Efficiency ....................................... 614.6 Conclusions ................................................................... 65References ............................................................................. 66
5 Role of Proteins Secreted by Rhizobia in SymbioticInteractions with Leguminous Roots 71Maged M. Saad,William J. Broughton,William J. Deakin5.1 Introduction .................................................................. 715.2 Bacterial Protein Secretion Systems ................................... 73
5.2.1 Type I Secretion Systems ....................................... 735.2.2 Type II Secretion Systems ...................................... 775.2.3 Type III Secretion Systems..................................... 775.2.4 Type IV Secretion Systems..................................... 82
5.3 Conclusions ................................................................... 83References ............................................................................. 83
Contents IX
6 Research on Endophytic Bacteria: Recent Advanceswith Forest Trees 89Richa Anand, Leslie Paul, Chris Chanway6.1 Introduction .................................................................. 896.2 Bacterial Endophytes of Forest Trees.................................. 916.3 Endophytic Bacteria of Conifers........................................ 926.4 Modes and Sites of Entry.................................................. 956.5 Mechanisms of Plant Growth Promotion ............................ 976.6 Future Work................................................................... 102References ............................................................................. 103
Part II Endophytic Fungi
7 Biodiversity of Fungal Root-Endophyte Communitiesand Populations, in Particular of the Dark Septate EndophytePhialocephala fortinii s. l. 107Thomas N. Sieber, Christoph R. Grünig7.1 Introduction .................................................................. 1077.2 Species Diversity of Root Endophyte Communities .............. 108
7.2.1 Geography and Climate......................................... 1097.2.2 Soil .................................................................... 1147.2.3 Multitrophic Interactions ...................................... 1157.2.4 Natural and Anthropogenic Disturbances ................ 117
7.3 Dark Septate Endophytes ................................................. 1197.3.1 History ............................................................... 1197.3.2 Biodiversity ......................................................... 1197.3.3 Diversity of Phialocephala fortinii........................... 121
7.4 Conclusions ................................................................... 125References ............................................................................. 126
8 Endophytic Root Colonization by Fusarium Species:Histology, Plant Interactions, and Toxicity 133Charles W. Bacon, Ida E. Yates8.1 Introduction .................................................................. 1338.2 Plant and Fungus Interactions .......................................... 134
8.2.1 Hemibiotrophic Characteristics.............................. 1388.2.2 Histology ............................................................ 1398.2.3 Mycotoxins.......................................................... 1438.2.4 Mycotoxins and Host Relationships......................... 1448.2.5 Physiological Interactions and Defense Metabolites... 145
8.3 Summary....................................................................... 146References ............................................................................. 147
X Contents
9 Microbial Endophytes of Orchid Roots 153Paul Bayman, J. Tupac Otero9.1 Introduction .................................................................. 1539.2 Habits and Types of Orchid Roots ..................................... 1539.3 Bacteria as Epiphytes and Endophytes of Orchid Roots ........ 1549.4 Orchid Endophytes or Orchid Mycorrhizal Fungi? ............... 1559.5 Problems with the Taxonomy of Orchid Endophytic Fungi .... 1579.6 Host Specificity of Orchid Endophytes ............................... 1589.7 Endophytic Fungi in Roots of Terrestrial,
Photosynthetic Orchids ................................................... 1589.8 Endophytic Fungi in Roots of Myco-Heterotrophic Orchids .. 1679.9 Endophytic Fungi in Roots of Epiphytic
and Lithophytic Orchids .................................................. 1699.10 Endophytic Fungi in Epiphytic Orchid Roots:
Importance to Plant Hosts................................................ 1719.11 Conclusions ................................................................... 172References ............................................................................. 173
10 Fungal Endophytes in Submerged Roots 179Felix Bärlocher10.1 Introduction .................................................................. 17910.2 Aquatic Hyphomycetes .................................................... 18010.3 Fungi in Submerged Roots ............................................... 18110.4 Conclusions and Outlook................................................. 186References ............................................................................. 188
11 Nematophagous Fungi as Root Endophytes 191Luis V. Lopez-Llorca,Hans-Börje Jansson, José Gaspar Maciá Vicente,Jesús Salinas11.1 Introduction .................................................................. 19111.2 Nematophagous Fungi ..................................................... 191
11.2.1 Nematode Parasites .............................................. 19211.2.2 Mycoparasites...................................................... 19511.2.3 Root Endophytes.................................................. 195
11.3 Concluding Remarks ....................................................... 202References ............................................................................. 203
12 Molecular Diversity and Ecological Roles of Mycorrhiza-AssociatedSterile Fungal Endophytes in Mediterranean Ecosystems 207Mariangela Girlanda,Silvia Perotto,Anna Maria Luppi12.1 Introduction .................................................................. 207
Contents XI
12.2 Diversity of DSE Associates of Ecto- and Endo-MycorrhizalPlants in Mediterranean Ecosystems in Northern Italy ......... 209
12.3 Ecological Relationships with Conventional Mycorrhizaland Pathogenic Symbionts ............................................... 214
12.4 Conclusions ................................................................... 219References ............................................................................. 220
13 Oidiodendron maius: Saprobe in Sphagnum Peat,Mutualist in Ericaceous Roots? 227Adrianne V. Rice, Randolph S. Currah13.1 Introduction .................................................................. 22713.2 Oidiodendron maius as a Saprobe...................................... 23013.3 Ericoid Mycorrhizas ........................................................ 23413.4 Oidiodendron maius as an Ericoid Mycorrhizal Fungus ........ 23713.5 Significance and Relevance............................................... 23913.6 Conclusions ................................................................... 241References ............................................................................. 242
14 Mycorrhizal and Endophytic Fungi of Epacrids (Ericaceae) 247John W.G. Cairney14.1 Introduction .................................................................. 24714.2 Endophytes of Epacrid Roots............................................ 24814.3 Diversity and Spatial Distribution
of Endophyte Taxa in Epacrid Root Systems........................ 25114.4 Mycorrhizal Status of Endophytes from Epacrids................. 25314.5 Saprotrophic Potential of Mycorrhizal Fungi....................... 25414.6 Symbiotic Functioning of Mycorrhizal Fungi ...................... 25514.7 Conclusions ................................................................... 257References ............................................................................. 257
15 Mutualistic Interactions with Fungal Root Endophytes 261Barbara Schulz15.1 Introduction .................................................................. 26115.2 Colonisation and Histology .............................................. 26215.3 Secondary Metabolites..................................................... 26415.4 Growth Enhancement...................................................... 26515.5 Disease Suppression ........................................................ 26915.6 Stress Tolerance .............................................................. 27115.7 Factors Determining the Status of the Interaction ................ 27215.8 Conclusions ................................................................... 273References ............................................................................. 276
XII Contents
16 Understanding the Roles of Multifunctional Mycorrhizaland Endophytic Fungi 281Mark C. Brundrett16.1 How Mycorrhizal Fungi Differ from Endophytes ................. 281
16.1.1 Definitions .......................................................... 28116.1.2 Roles of Endophytes and Mycorrhizal Fungi ............. 282
16.2 Endophytic Activity by Mycorrhizal Fungi.......................... 28316.2.1 Glomeromycotan (Vesicular-Arbuscular
Mycorrhizal) Fungi............................................... 28316.2.2 Ectomycorrhizal Fungi.......................................... 28616.2.3 Fungi in Orchids .................................................. 28716.2.4 Ericoid Mycorrhizal Fungi ..................................... 29016.2.5 Endophytic Fungi in Mycorrhizal Roots................... 290
16.3 Issues with the Identification and Categorisationof Fungi in Roots ............................................................ 291
16.4 Evolution of Root-Fungus Associations .............................. 29216.5 Conclusions ................................................................... 293References ............................................................................. 293
Part III Methods
17 Isolation Procedures for Endophytic Microorganisms 299Johannes Hallmann, Gabriele Berg, Barbara Schulz17.1 Introduction .................................................................. 29917.2 Surface Sterilisation ........................................................ 300
17.2.1 Pre-treatment ...................................................... 30017.2.2 Sterilising Agents ................................................. 30117.2.3 Surfactants .......................................................... 30517.2.4 Rinsing ............................................................... 30517.2.5 Sterility Check and Optimisation............................ 305
17.3 Culture of Tissue and Plant Fluid of Sterilised Rootson Nutrient Medium ....................................................... 30617.3.1 Segments ............................................................ 30617.3.2 Maceration of Root Tissue ..................................... 30617.3.3 Centrifugation of Root Tissue ................................ 307
17.4 Vacuum and Pressure Extraction ...................................... 30817.5 Media............................................................................ 309
17.5.1 Media for Isolating Bacteria ................................... 31017.5.2 Media for Isolating Fungi ...................................... 31017.5.3 Supplements........................................................ 31017.5.4 Selective Media .................................................... 311
Contents XIII
17.6 Cultivation-Independent Methods..................................... 31117.7 Quantification of Colonisation .......................................... 31317.8 Conclusions ................................................................... 313References ............................................................................. 314
18 Microbial Interactions with Plants: a Hidden World? 321Guido V. Bloemberg,Margarita M. Camacho Carvajal18.1 Introduction .................................................................. 32118.2 Microscopic Techniques for Studying
Plant-Microbe Interactions .............................................. 32218.2.1 Light Microscopy and Enzymatic Reporters ............. 32218.2.2 Scanning Electron Microscopy ............................... 32418.2.3 Epifluorescence Microscopy
and the Application of Auto-Fluorescent Proteins...... 32518.3 Visualisation of Bacterium-Plant Interactions ..................... 32718.4 Most Recent Developments in Visualising
Plant-Microorganism Interactions..................................... 33018.5 Visualisation of Plant-Fungus Interactions ......................... 33118.6 Future Perspectives ......................................................... 333References ............................................................................. 333
19 Application of Molecular Fingerprinting Techniquesto Explore the Diversity of Bacterial Endophytic Communities 337Leo S. van Overbeek, Jim van Vuurde, Jan D. van Elsas19.1 Introduction .................................................................. 33719.2 Colonisation by Bacterial Endophytes ................................ 33819.3 Shifts of Bacterial Endophyte Communities ........................ 33819.4 Molecular methods to Study Bacterial Endophytes .............. 34019.5 Molecular Fingerprinting of Endophyte Communities.......... 341
19.5.1 Basic Concept of Molecular Fingerprinting .............. 34119.5.2 Sample Preparation .............................................. 34219.5.3 Nucleic Acid Extraction......................................... 34319.5.4 PCR and Molecular Community Fingerprinting........ 34419.5.5 Group-Specific Molecular
Community Fingerprinting ................................... 34519.5.6 Molecular Identification of Species and Genes .......... 348
19.6 Integration of Detection Techniques .................................. 34819.6.1 Polyphasic Approach ............................................ 348
19.7 Conclusions ................................................................... 349References ............................................................................. 350
Subject Index 355
Contributors
Anand, RichaFaculty of Land and Food Sciences, Faculty of Forestry, University of BritishColumbia, Vancouver, British Columbia, Canada V6T 1Z4; Current address:Department of Forest Mycology and Pathology, Swedish University of Agri-cultural Sciences (SLU), Box 7026, 750 07 Uppsala, Sweden
Bacon, Charles W.Richard B. Russell Research Center, ARS, United States Department ofAgriculture, Toxicology and Mycotoxin Research Unit, SAA, P.O. Box 5677,Athens, GA 30604, USA
Bärlocher, Felix63BYorkStreet,DepartmentofBiology,MountAllisonUniversity, Sackville,New Brunswick, E4L 1G7, Canada
Bayman, PaulDepartamento de Biologia, Universidad de Puerto Rico – Rio Piedras, POBox 23360, San Juan, PR 00931, USA
Berg, GabrieleGraz University of Technology, Department of Environmental Biotechnol-ogy, Petersgasse 12, 8010 Graz, Austria
Bloemberg, Guido V.Leiden University, Institute of Biology, Wassenaarseweg 64, 2333AL Leiden,The Netherlands
Boyle, ChristineAugustastraße 32, 02826 Görlitz, Germany
Broughton, William J.Université de Genève, Laboratoire de Biologie Moléculaire des PlantesSupérieures, Sciences III, 30QuaiErnest-Ansermet, 1211Genève4, Switzer-land
XVI Contributors
Brundrett, Mark C.School of Plant Biology, Faculty of Natural and Agricultural Sciences, TheUniversity of Western Australia, Crawley, WA 6009, Australia
Cairney, John W.G.Centre for Plant and Food Sciences, Parramatta Campus, University ofWestern Sydney, Locked Bag 1797, Penrith South DC, NSW 1797, Australia
Carvajal, Margarita M. CamachoLeiden University, Institute of Biology, Wassenaarseweg 64, 2333AL Leiden,The Netherlands
Chanway, ChrisFaculty of Land and Food Systems, Faculty of Forestry, University of BritishColumbia, Vancouver, British Columbia, Canada V6T 1Z4
Currah, Randolph S.Department of Biological Sciences, University of Alberta, Edmonton, AB,T6G 2E9, Canada
Deakin, William J.Université de Genève, Laboratoire de Biologie Moléculaire des PlantesSupérieures, Sciences III, 30QuaiErnest-Ansermet, 1211Genève4, Switzer-land
Elsas, Jan D. vanGroningen University, Department of Microbial Ecology, Biological Center,Kerklaan 30, 9751 NN, Haren, The Netherlands
Girlanda, MariangelaDipartimento di Biologia Vegetale and IPP - Torino, Viale PA Mattioli 25,10125 Torino, Italy
Grünig, Christoph R.Swiss Federal Institute of Technology, Department of Environmental Sci-ences, Institute of Integrative Biology, Forest Pathology and Dendrology,8092 Zürich, Switzerland
Hallmann, JohannesBiologische Bundesanstalt für Land- und Forstwirtschaft, Institut für Ne-matologie und Wirbeltierkunde, Toppheideweg 88, 48161 Münster, Ger-many
Contributors XVII
Jansson, Hans-BörjeDepartamento de Ciencias del Mar y Biología Aplicada, Universidad deAlicante, Apdo. 99, 03080 Alicante, Spain
Kloepper, Joseph W.Department of Entomology and Plant Pathology, Auburn University, Au-burn, AL 36849, USA
Lopez-Llorca, Luis V.Departamento de Ciencias del Mar y Biología Aplicada, Universidad deAlicante, Apdo. 99, 03080 Alicante, Spain
Luppi, Anna MariaDipartimento di Biologia Vegetale and IPP, Viale PA Mattioli 25, 10125Torino, Italy
Otero, J. TupacUniversidad Nacional de Colombia-Palmira, Departamento de CienciasAgrícolas, AA 237, Palmira, Valle del Cauca, Colombia
Overbeek, Leo S. vanPlant Research International B.V, Droevendaalsesteeg 1, 6708 PB, Wagenin-gen, The Netherlands
Paul, LeslieFacultyofLandandFoodSciences, Systems,UniversityofBritishColumbia,Vancouver, British Columbia, Canada V6T 1Z4
Perotto, SilviaDipartimento di Biologia Vegetale and IPP - Torino, Viale PA Mattioli 25,10125 Torino, Italy
Rice, Adrianne V.Northern Forestry Centre, Canadian Forest Service, Natural ResourcesCanada, 5320-122 St., Edmonton, AB, T6H 3S5 Canada
Ryu, Choong-MinPlant Biology Division, The Samuel Roberts Noble Foundation, 2510 SamNoble Parkway, Ardmore, OK 73401, USA
XVIII Contributors
Saad, Maged M.Université de Genève, Laboratoire de Biologie Moléculaire des PlantesSupérieures, Sciences III, 30QuaiErnest-Ansermet, 1211Genève4, Switzer-land
Salinas, JesúsDepartamento de Ciencias del Mar y Biología Aplicada, Universidad deAlicante, Apdo. 99, 03080 Alicante, Spain
Schulz, BarbaraInstitute of Microbiology, Technical University of Braunschweig, Spiel-mannstraße 7, 38106 Braunschweig, Germany
Sieber, Thomas N.Swiss Federal Institute of Technology, Department of Environmental Sci-ences, Institute of Integrative Biology, Forest Pathology and Dendrology,8092 Zürich, Switzerland
Vicente, José Gaspar MaciáDepartamento de Ciencias del Mar y Biología Aplicada, Universidad deAlicante, Apdo. 99, 03080 Alicante, Spain
Vuurde, Jim vanPlant Research International B.V, Droevendaalsesteeg 1, 6708 PB, Wagenin-gen, The Netherlands
Yates, Ida E.Richard B. Russell Research Center, ARS, United States Department ofAgriculture, Toxicology and Mycotoxin Research Unit, Athens, GA 30604,USA
Abbreviations
ACC 1-aminocyclopropane-1-carboxylateAHL acyl homoserine lactonesAM arbuscular mycorrhizaAMF arbuscular mycorrhizal fungiARA acetylene reduction activityAUDPC area under the disease progress curveBAC bacterial artificial chromosomeBCA biocontrol agentsBRD root border cellsBrdU bromide oxyuridineCfu colony forming unitsCLSM confocal laser scanning microscopyCMA corn meal agarCMV Cucumber mosaic virusCPS capsular polysaccharidesCTAB cetyl trimethyl ammonium bromideDGGE denaturing gradient gel electrophoresisDIC differential interference microscopyDON deoxynivalenolDSE dark septate endophytesDSF dark septate fungiDSM dark sterile myceliaECFP enhanced cyan fluorescent proteinECM ectomycorrhizaeECM extracellular materialEGFP Enhanced GFPELISA enzyme-linked immunosorbent assayEPS extra-cellular polysaccharidesEYFP Enhanced Yellow Fluorescent ProteinFISH fluorescence in situ hybridizationGFP Green fluorescent proteinGSP general secretory pathwayGUS β-glucuronidase
XX Abbreviations
IAA indole acetic acidICR induced systemic resistanceISSR inter-simple sequence repeatITS internal transcribed spacerITS-RFLP internal transcribed spacer-restriction fragment length
polymorphismLPS lipo-polysaccharidesMLH multilocus haplotypesMRA Mycelium radicis atrovirensNDFA nitrogen derived from the atmospherePAH polyaromatic hydrocarbonPAR photosynthetically active radiationPBM peribacteroid membranePCR polymerase chain reactionPCR-RFLP polymerase chain reaction -restriction fragment length
polymorphismPDA potato dextrose agarPGPR plant growth promoting rhizobacteriaPR pathogenesis-relatedPVP polyvinylpyrrolidoneRAPD random amplified polymorphic DNARDNA 16S rRNA geneRFLP restriction fragment length polymorphismRFP red fluorescent proteinRGR relative growth rateSAR systemic acquired resistanceSEM Scanning electron microscopySPB sterile phosphate bufferSPS Surface polysaccharidesSSCP single strand conformational polymorphismTGGE temperature gradient gel electrophoresisTNV tobacco necrosis virusToMoV Tomato mottle virusTRFLP terminal restriction fragment length polymorphismTSA tryptic soya agarVAM vesicular arbuscular mycorrhizaVOC volatile organic compoundVWT variable white taxonWA Western Australia