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Role of Diverse Non-Systemic Fungal Endophytes in Plant Performance and Response to Stress: Progress and Approaches

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Abstract

Plant–fungal symbiotic associations are ubiquitously distributed in natural plant communities. Besides the well-studied mycorrhizal symbiosis and grass systemic clavicipitaceous endophytes, recently, nonsystemic and horizontally transmitted fungal endophytes serving as plant symbionts have been increasingly recognized. Pure culture isolation and culture-independent molecular methods indicate that all parts of healthy plant tissues potentially harbor diverse and previously unknown fungal lineages. Limited evidence also supports a hypothesis that endophytic mycobiota dynamics may have a role in evolution of plants. High variability or “balanced antagonism” can be generally characterized with host–endophyte interactions, which implies that the outcome of symbiotic interactions can fall within a continuum ranging from mutualism to commensalism, and ultimately pathogenicity. Despite this complicated system, admittedly, fungal endophytes really endow the host with an extended phenotype. Accumulating facts illustrate that plant nutrition acquisition, metabolism, and stress tolerance may be strengthened or modulated via fungal symbionts. Piriformospora indica, a member of the order Sebacinales, simultaneously confers host resistance to biotic and abiotic stress. The ecological relevance of other fungal groups, including foliar endophytes, root dark septate endophytes (DSEs), some opportunistic and avirulent microsymbionts (for example, Trichoderma and Fusarium), and even uncultured fungi structurally and physiologically integrated with host tissues, are also being deeply exploited. Production of bioactive metabolites by fungi, overexpression of stress-related enzymes, and induced resistance in hosts upon fungal colonization are responsible for direct or indirect beneficial effects to hosts. More knowledge of endophyte-mediated enhancement of host performance and fitness will offer alternatively valuable strategies for plant cultivation and breeding. Meanwhile, with unprecedented loss of biodiversity, discovery of indigenously novel symbiotic endophytes from natural habitats is urgently needed. In addition, we present some approaches and suggestions for studying host–endophyte interactions.

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References

  • Allen TR, Millar T, Berch SM, Berbee ML (2003) Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160:255–272

    CAS  Google Scholar 

  • Araim G, Saleem A, Arnason JT, Charest C (2009) Root colonization by an arbuscular mycorrhizal (AM) fungus increases growth and secondary metabolism of Purple Coneflower, Echinacea purpurea (L.) Moench. J Agric Food Chem. doi:10.1021/jf803173x

  • Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Carson WP, Schnitzer SA (eds) Tropical forest community ecology. Wiley-Blackwell, Oxford, pp 254–271

    Google Scholar 

  • Arnold AE, Lewis LC (2005) Evolution of fungal endophytes, and their roles against insects. In: Vega F, Blackwell M (eds) Ecological and evolutionary advances in insect-fungus associations. Oxford University Press, Oxford, pp 74–96

    Google Scholar 

  • Arnold AE, Maynard Z, Gilbert GS, Coley OD, Kursar TA (2002) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274

    Google Scholar 

  • Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654

    CAS  PubMed  Google Scholar 

  • Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206

    CAS  PubMed  Google Scholar 

  • Bacon CW, Yates IE (2006) Endophytic root colonization by Fusarium species: histology, plant interactions, and toxicity. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer-Verlag, Berlin, pp 133–152

    Google Scholar 

  • Baldi A, Jain A, Gupta N, Srivastava AK, Bisaria VS (2008) Co-culture of arbuscular mycorrhiza-like fungi (Piriformospora indica and Sebacina vermifera) with plant cells of Linum album for enhanced production of podophyllotoxins: a first report. Biotechnol Lett 30:1671–1677

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bartholdy, Berreck M, Haselwandter K (2001) Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. Biometals 14:33–42

    CAS  PubMed  Google Scholar 

  • Barrow JR, Lucero M, Osuna-Avila P, Reyes-Vera I, Aaltonen RE (2004a) Fungal genomes that influence basic physiological processes of black grama and fourwing salt bush in arid southwestern rangelands. In: Proceedings of Shrubland dynamics – fire and water. Lubbock, TX, 10–12 August 2004, pp 123–131

  • Barrow JR, Osuna-Avila P, Reyes I (2004b) Fungal endophytes intrinsically associated with micro-propagated plants regenerated from native Bouteloua eriopoda Torr. and Atriplex canescens (Pursh.) Nutt. In Vitro Cell Dev Biol Plants 40:608–612

    Google Scholar 

  • Barrow JR, Lucero ME, Reyes-Vera I, Havstad KM (2008) Do symbiotic microbes have a role in plant evolution, performance and response to stress? Commun Integr Biol 1:1–5

    Article  Google Scholar 

  • Carroll G (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69:2–9

    Google Scholar 

  • Carroll GC (1991) Beyond pest deterrence. Alternative strategies and hidden costs of endophytic mutualisms in vascular plants. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer-Verlag, NewYork, pp 358–375

    Google Scholar 

  • Clay K (2004) Fungi and the food of the gods. Nature 427:401–402

    CAS  PubMed  Google Scholar 

  • Collado J, González A, Platas G, Stchigel AM, Guarro J, Peláez F (2002) Monosporascus ibericus sp. nov., an endophytic ascomycete from plants on saline soils, with observations on the position of the genus based on sequence analysis of the 18S rDNA. Mycol Res 106:118–127

    CAS  Google Scholar 

  • Collado J, Platas G, Paulus B, Bills GF (2007) High-throughput culturing of fungi from plant litter by a dilution-to-extinction technique. FEMS Microbiol Ecol 60:521–533

    CAS  PubMed  Google Scholar 

  • Deshmukh S, Hückelhoven R, Schäfer 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

    CAS  PubMed  Google Scholar 

  • de Bary HA (1879) Die Erscheinung der Symbiose. de Bary, Strasburg

    Google Scholar 

  • Diouf D, Diop TA, Ndoye I (2003) Actinorhizal, mycorrhizal and rhizobial symbioses: how much do we know? Afr J Biotechnol 2:1–7

    CAS  Google Scholar 

  • Donoso EP, Bustamante RO, Carú M, Niemeyer HM (2008) Water deficit as a driver of the mutualistic relationship between the fungus Trichoderma harzianum and two wheat genotypes. Appl Envir Microbiol 74:1412–1417

    CAS  Google Scholar 

  • El-Morsy EM (2000) Fungi isolated from the endorhizosphere of halophytic plants from the Red Sea Coast of Egypt. Fungal Divers 5:43–54

    Google Scholar 

  • El-Zayat SA, Nassar MSM, El-Hissy FT, Abdel-Motaal FF, Ito S (2008) Mycoflora associated with Hyoscyamus muticus growing under an extremely arid desert environment (Aswan region, Egypt). J Basic Microbiol 48:82–92

    PubMed  Google Scholar 

  • Ernst M, Mendgen KW, Wirsel SG (2003) Endophytic fungal mutualists: seed-borne Stagonospora spp. enhance reed biomass production in axenic microcosms. Mol Plant Microbe Interact 16:580–587

    CAS  PubMed  Google Scholar 

  • Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42:360–368

    Google Scholar 

  • Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216:148–154

    CAS  PubMed  Google Scholar 

  • Freeman S, Rodriguez JR (1993) Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260:75–78

    PubMed  CAS  Google Scholar 

  • Fujihara S, Terakado J, Nishibori N (2006) Accumulation of an aromatic amine, β-phenethylamine, in root nodules of adzuki bean Vigna angularis. Plant Soil 280:229–237

    CAS  Google Scholar 

  • Ganley RJ, Brunsfeld SJ, Newcombe G (2004) A community of unknown, endophytic fungi in western white pine. Proc Natl Acad Sci USA 101:10107–10112

    CAS  PubMed  Google Scholar 

  • Ganley RJ, Sniezko RA, Newcombe G (2008) Endophyte-mediated resistance against white pine blister rust in Pinus monticola. Forest Ecol Manage 255:2751–2760

    Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    CAS  PubMed  Google Scholar 

  • Gasoni L, Stegman D, Gurfinkel B (1997) The endophyte Cladorrhinum foecundissimum in cotton roots: phosphorus uptake and host growth. Mycol Res 101:867–870

    Google Scholar 

  • Grunewaldt-Stocker G, Riediger N, Dietrich C (2007) Suitability of GFP-transformed isolates of the fungal root endophyte Acremonium strictum W. Gams for studies on induced Fusarium-wilt resistance in flax. Plant Root 1:46–56

    Google Scholar 

  • Güimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102:8066–8070

    PubMed  Google Scholar 

  • Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20:2989–3005

    CAS  PubMed  Google Scholar 

  • Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    CAS  PubMed  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    CAS  PubMed  Google Scholar 

  • Hawksworth DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revised. Mycol Res 105:1422–1432

    Google Scholar 

  • Herre EA, Van Bael SA, Maynard Z, Robbins N, Bischoff J, Arnold AE, Rojas E, Mejia LC, Cordero RA, Woodward C, Kyllo DA (2005) Tropical plants as chimera: some implications of foliar endophytic fungi for the study of host plant defense, physiology, and genetics. In: Burslem DFRP, Pinard MA, Hartley SE (eds) Biotic interactions in the tropics. Cambridge University Press, Cambridge, pp 226–237

    Google Scholar 

  • Herre EA, Mejía LC, Kyllo DA, Rojas E, Maynard Z, Butler A, Van Bael SA (2007) Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology 88:550–558

    PubMed  Google Scholar 

  • Hjeljord L, Tronsmo A (1998) Trichoderma and Gliocladium in biological control: an overview. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium, vol 2. Enzymes, biological control and commercial application. Taylor and Francis Ltd, London, pp 129–151

    Google Scholar 

  • Hoffman M, Gunatilaka M, Ong J, Shimabukuro M, Arnold AE (2008) Molecular analysis reveals a distinctive fungal endophyte community associated with foliage of Montane oaks in southeastern Arizona. J Arizona Nevada Acad Sci 40:91–100

    Google Scholar 

  • Hung PQ, Kumar SM, Govindsamy V, Annapurna K (2007) Isolation and characterization of endophytic bacteria from wild and cultivated soybean varieties. Biol Fertil Soils 44:155–162

    Google Scholar 

  • Johnson JA, Whitney NJ (1994) Cytotoxicity and insecticidal activity of endophytic fungi from black spruce (Picea mariana) needles. Can J Microbiol 40:24–27

    Google Scholar 

  • Kemppainen M, Duplessis S, Martin F, Pardo AG (2008) T-DNA insertion, plasmid rescue and integration analysis in the model mycorrhizal fungus Laccaria bicolor. Microbiol Biotechnol 1:258–269

    CAS  Google Scholar 

  • Khan SA, Hamayun M, Kim H, Yoon H, Seo J, Choo Y, Lee I, Kim S, Rhee I, Kim J (2009) A new strain of Arthrinium phaeospermum isolated from Carex kobomugi Ohwi is capable of gibberellin production. Biotechnol Lett 31:283–287

    CAS  PubMed  Google Scholar 

  • Kharkwal AC, Prasad R, Kharkwal H, Das A, Bhatnagar K, Sherameti I, Oelmüller R, Varma A (2007) Co-cultivation with Sebacinales. In: Varma A, Oelmüller R (eds) Advanced techniques in soil microbiology. Springer, Berlin, pp 247–270

    Google Scholar 

  • Kharkwal AC, Kharkwal H, Sherameti I, Oelmuller R, Varma A (2008) Novel symbiotrophic endophytes. In: Varma A (ed) Mycorrhiza—state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer-Verlag, Berlin, pp 753–766

    Google Scholar 

  • Kogel KH, Langen G (2005) Induced disease resistance and gene expression in cereals. Cell Microbiol 7:1555–1564

    CAS  PubMed  Google Scholar 

  • Kogel KH, Schafer P (2009) The Sebacinoid fungus Piriformospora indica: an orchid mycorrhiza which may increase host plant reproduction and fitness. In: Esser K (ed) Plant relationships, 2nd edn., Series: The Mycota V. Springer-Verlag, Berlin, pp 99–112

    Google Scholar 

  • Kogel KH, Franken P, Huckelhoven R (2006) Endophyte or parasite—what decides? Curr Opin Plant Biol 9:358–363

    PubMed  Google Scholar 

  • Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71

    Google Scholar 

  • Li YC, Tao WY (2009) Interactions of Taxol-producing endophytic fungus with its host (Taxus spp.) during Taxol accumulation. Cell Biol Int 33:106–112

    PubMed  Google Scholar 

  • Lucero ME, Barrow JR, Osuna P, Reyes I (2006) Plant-fungal interactions in arid and semiarid ecosystems: large scale impacts from microscale processes. J Arid Environ 65:276–284

    Google Scholar 

  • Lucero ME, Barrow JR, Osuna P, Reyes I, Duke SE (2008) Enhancing native grass productivity by cocultivating with endophyte-laden calli. Rangel Ecol Manage 61:124–130

    Google Scholar 

  • Maccheroni W, Azevedo JL (1998) Synthesis and secretion of phosphatases by endophytic isolates of Colletotrichum musae grown under conditions of nutritional starvation. J Gen Appl Microbiol 44:381–387

    CAS  Google Scholar 

  • Macia-Vicente JG, Jansson HB, Abdullah SK, Descals E, Salinas J, Lopez-Llorca LV (2008a) Fungal root endophytes from natural vegetation in Mediterranean environments with special reference to Fusarium spp. FEMS Microbiol Ecol 64:90–105

    CAS  PubMed  Google Scholar 

  • Macia-Vicente JG, Jansson HB, Mendgen K, Lopez-Llorca LV (2008b) Colonization of barley roots by endophytic fungi and their reduction of take-all caused by Gaeumannomyces graminis var. tritici. Can J Microbiol 54:600–609

    CAS  PubMed  Google Scholar 

  • Malla R, Prasad R, Giang PH, Kumari R, Pokharel U, Oelmuller R, Varma A (2004) Phosphorus solubilizing symbiotic fungus: Piriformospora indica. Endocytobiosis Cell Res 15:579–600

    Google Scholar 

  • Mandayam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophyte fungi. Stud Mycol 53:173–189

    Google Scholar 

  • Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515

    PubMed  Google Scholar 

  • McGee PA (2002) Reduced growth and deterrence from feeding of the insect pest Helicoverpa armigera associated with fungal endophytes from cotton. Aust J Exp Agric 42:995–999

    Google Scholar 

  • Miller JD, Mackenzie S, Foto M, Adams GW, Findlay JA (2002) Needles of white spruce inoculated with rugulosin-producing endophytes contain rugulosin reducing spruce budworm growth rate. Mycol Res 106:471–479

    Google Scholar 

  • Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104:8627–8633

    CAS  PubMed  Google Scholar 

  • Mucciarelli M, Scannerini S, Bertea CM, Maffei M (2002) An ascomycetous endophyte isolated from Mentha piperita L.: biological features and molecular studies. Mycologia 94:28–39

    Google Scholar 

  • Mucciarelli M, Scannerini S, Bertea C, Maffei M (2003) In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. New Phytol 158:579–591

    Google Scholar 

  • Mucciarelli M, Camusso W, Maffei M, Panicco P, Bicchi C (2007) Volatile terpenoids of endophyte-free and infected peppermint (Mentha piperita L.): chemical partitioning of a symbiosis. Microb Ecol 54:685–696

    CAS  PubMed  Google Scholar 

  • Nikolcheva LG, Bärlocher F (2005a) Molecular approaches to estimate fungal diversity. I. terminal restriction fragment length polymorphism (T-RFLP). In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Berlin, pp 169–176

    Google Scholar 

  • Nikolcheva LG, Bärlocher F (2005b) Molecular approaches to estimate fungal diversity. II. denaturing gradient gel electrophoresis (DGGE). In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Berlin, pp 177–183

    Google Scholar 

  • Nurnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345

    PubMed  Google Scholar 

  • Obledo EN, Barragán-Barragán LB, Gutiérrez-González P, Ramírez-Hernández BC, Ramírez JJ, Rodríguez-Garay B (2003) Increased photosynthetic efficiency generated by fungal symbiosis in Agave victoria-reginae. Plant Cell Tissue Organ Cult 74:237–241

    CAS  Google Scholar 

  • O’Brien HE, Parrent JL, Jackson JA, Moncalvo JM, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550

    PubMed  Google Scholar 

  • Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8:1899–1913

    CAS  PubMed  Google Scholar 

  • Peay KG, Kennedy PG, Bruns TD (2008) Fungal community ecology: a hybrid beast with a molecular master. Bioscience 58:799–810

    Google Scholar 

  • Peskan-Berghofer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, Oelmüller R (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 Plantarum 122:465–477

    Google Scholar 

  • Peters S, Aust AJ, Draeger S, Schulz B (1998) Interaction in dual cultures of endophytic fungi with host and non-host plant calli. Mycologia 90:360–367

    Google Scholar 

  • Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenbach KJ, Lowrey T, Natvig DO (2008) Novel root fungal consortium associated with a dominant desert grass. Appl Environ Microbiol 74:2805–2813

    CAS  PubMed  Google Scholar 

  • Posada F, Aime MC, Peterson SW, Rehner SA, Vega FE (2007) Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycol Res 111:748–757

    CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    CAS  PubMed  Google Scholar 

  • Quesada-Moraga E, Landa BB, Muñoz-Ledesma J, Jiménez-Diáz RM, Santiago-Alvarez C (2006) Endophytic colonisation of opium poppy, Papaver somniferum, by an entomopathogenic Beauveria bassiana strain. Mycopathologia 161:323–329

    CAS  PubMed  Google Scholar 

  • Rai M, Acharya D, Singh A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128

    Google Scholar 

  • Rai MK, Varma A, Pandey AK (2004) Antifungal potential of Spilanthes calva after inoculation of Piriformospora indica. Mycoses 47:479–481

    CAS  PubMed  Google Scholar 

  • Redman RS, Freeman S, Clifton DR, Morrel J, Brown G, Rodriguez RJ (1999) Biochemical analysis of plant protection afforded by a nonpathogenic endophytic mutant of Colletotrichum magna. Plant Physiol 119:795–804

    CAS  PubMed  Google Scholar 

  • Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol 151:705–716

    Google Scholar 

  • Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581

    CAS  PubMed  Google Scholar 

  • Rodriguez RJ (2007) It’s a very thin line between love and hate: symbiotic adaptation, modulation and lifestyle switching. Available at http://www.tc.umn.edu/~plpagrad/2007/speakers/

  • Rodriguez RJ, Redman RS (2005) Balancing the generation and elimination of reactive oxygen species. Proc Natl Acad Sci USA 102:3175–3176

    CAS  PubMed  Google Scholar 

  • Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416

    Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    CAS  PubMed  Google Scholar 

  • Saikkonen K, Faeth SH, Helander ML, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Google Scholar 

  • Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280

    CAS  PubMed  Google Scholar 

  • Savouré A, Magyar Z, Pierre M, Brown S, Schultze M, Dudits D, Kondorosi A, Kondorosi E (1994) Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions. EMBO J 13:1093–1102

    PubMed  Google Scholar 

  • Saxena PK, Cole IB, Murch SJ (2005) Approaches to quality plant based medicine: significance of chemical profiling. In: Verpoorte R, Alfermann AW, Johnson TS (eds) Applications of plant metabolic engineering. Springer, Amsterdam, pp 311–330

    Google Scholar 

  • Scannerini S, Fusconi A, Mucciarelli M (2002) The effect of endophytic fungi on host plant morphogenesis. In: Seckbach J (ed) Cellular origin and life in extreme habitats, Symbiosis. Kluwer Academic Publishers, Amsterdam, pp 427–447

    Google Scholar 

  • Schliemann W, Ammer C, Strack D (2008) Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 69:112–146

    CAS  PubMed  Google Scholar 

  • Schmit JP, Mueller GM (2007) An estimate of the lower limit of global fungal diversity. Biodivers Conserv 16:99–111

    Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    PubMed  Google Scholar 

  • Schulz B, Boyle C (2006) What are endophytes? In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer-Verlag, Berlin, pp 1–13

    Google Scholar 

  • Shahollari B, Bhatnagar K, Sherameti I, Varma A, Oelmüller R (2007) Molecular symbiotic analysis between Arabiopsis thaliana and Piriformospora indica. In: Varma A, Oelmüller R (eds) Advanced techniques in soil microbiology. Springer-Verlag, Berlin, pp 307–318

    Google Scholar 

  • Sharma M, Schmid M, Rothballer M, Hause G, Zuccaro A, Imani J, Kämpfer P, Domann E, Schäfer P, Hartmann A, Kogel KH (2008) Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiol 10:2235–2246

    CAS  PubMed  Google Scholar 

  • Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller 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 that binds to a conserved motif in their promoters. J Biol Chem 280:26241–26247

    CAS  PubMed  Google Scholar 

  • Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) 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

    CAS  PubMed  Google Scholar 

  • Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K (2007) Piriformospora indica affects plant growth by auxin production. Physiol Plantarum 131:581–589

    CAS  Google Scholar 

  • Strobel GA (2006) Muscodor albus and its biological promise. J Ind Microbiol Biotechnol 33:514–522

    CAS  PubMed  Google Scholar 

  • Strobel GA (2007) Plant-associated microorganisms (endophytes) as a new source of bioactive natural products. In: Kayser O, Quax WJ (eds) Medicinal plant biotechnology: from basic research to industrial applications. Wiley-VCH, New York, pp 49–70

    Google Scholar 

  • Strobel GA, Kluck K, Hess WM, Sears J, Ezra D, Vargas PN (2007) Muscodor albus E-6, an endophyte of Guazuma ulmifolia making volatile antibiotics: isolation, characterization and experimental establishment in the host plant. Microbiology 153:2613–2620

    CAS  PubMed  Google Scholar 

  • Suryanarayanan TS, Kumaresan V (2000) Endophytic fungi of some halophytes from an estuarine mangrove forest. Mycol Res 104:1465–1467

    Google Scholar 

  • Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066

    CAS  PubMed  Google Scholar 

  • Tao G, Liu ZY, Hyde KD, Liu XZ, Yu ZN (2008) Whole rDNA analysis reveals novel and endophytic fungi in Bletilla ochracea (Orchidaceae). Fungal Divers 33:101–122

    Google Scholar 

  • Thomas SE, Crozier J, Aime MC, Evans HC, Holmes KA (2008) Molecular characterisation of fungal endophytic morphospecies associated with the indigenous forest tree, Theobroma gileri in Ecuador. Mycol Res 112:852–860

    CAS  PubMed  Google Scholar 

  • Unterseher M, Schnittler M (2009) Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.)—different cultivation techniques influence fungal biodiversity assessment. Mycol Res 113:645–654

    PubMed  Google Scholar 

  • Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184

    CAS  PubMed  Google Scholar 

  • Van Bael SA, Maynard Z, Rojas E, Mejía LC, Kyllo DA, Herre EA, Robbins N, Bischoff JF, Arnold AE (2005) Emerging perspectives on the ecological roles of endophytic fungi in tropical plants. In: Dighton J, White F, Oudemans P (eds) The fungal community: its organization and role in the ecosystem. Marcel-Dekker, New York, pp 181–192

    Google Scholar 

  • Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JP (2002) Extensive fungal diversity in plant roots. Science 295:2051

    PubMed  Google Scholar 

  • Vega FE, Posada FJ, Aime MC, Pava-Ripoll M, Infante F, Rehner SA (2008) Entomopathogenic fungal endophytes. Biol Control 46:72–82

    Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (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

    CAS  PubMed  Google Scholar 

  • Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schäfer P, Kogel KH (2008) Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. J Plant Physiol 165:60–70

    CAS  PubMed  Google Scholar 

  • Wang JW, Zhang Z, Tan RX (2001) Stimulation of artemisinin production in Artemisia annua hairy roots by the elicitor from the endophytic Colletotrichum sp. Biotechnol Lett 23:857–860

    CAS  Google Scholar 

  • Wilberforce EM, Griffith GW, Boddy L, Griffiths R (2002a) Effect of agricultural management on diversity of root endophytes: the role of dark septate endophytes. The 7th International Mycological Congress, p 102

  • Wilberforce EM, Griffith GW, Boddy L, Griffiths R (2002b) The widespread occurrence of dark septate endophyte fungi in grassland communities. The 7th International Mycological Congress, p 319

  • Wilson D (1995) Endophyte—the evolution of a term, and clarification. Oikos 73:274–276

    Google Scholar 

  • Yuan ZL, Dai CC, Chen LQ (2007) Regulation and accumulation of secondary metabolites in plant-fungus symbiotic system. Afr J Biotechnol 6:1266–1271

    CAS  Google Scholar 

  • Yuan ZL, Chen YC, Yang Y (2009) Diverse non-mycorrhizal fungal endophytes inhabiting an epiphytic, medicinal orchid (Dendrobium nobile): estimation and characterization. World J Microbiol Biotechnol 25:295–303

    Google Scholar 

  • Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735

    CAS  PubMed  Google Scholar 

  • Zuccaro A, Schoch CL, Spatafora JW, Kohlmeyer J, Draeger S, Mitchell JI (2008) Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Appl Environ Microbiol 74:931–941

    CAS  PubMed  Google Scholar 

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Acknowledgment

This work was supported by grants from the National Natural Science Foundation of China (No. 30600002) and the Science and Technology Project of Zhejiang Province (No. 2006C12088) to Chulong Zhang. We are grateful to three anonymous reviewers and reviewing editors for valuable comments and language corrections that greatly improved the manuscript. We also thank Professor Kari Saikkonen (Turku University) for providing suggestive information and Professor Jerry R. Barrow (USDA-ARS) for polishing the language of the manuscript.

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Correspondence to Chu-long Zhang or Fu-cheng Lin.

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Yuan, Zl., Zhang, Cl. & Lin, Fc. Role of Diverse Non-Systemic Fungal Endophytes in Plant Performance and Response to Stress: Progress and Approaches. J Plant Growth Regul 29, 116–126 (2010). https://doi.org/10.1007/s00344-009-9112-9

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