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Unraveling the Dark Septate Endophyte Functions: Insights from the Arabidopsis Model

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Advances in Endophytic Research

Abstract

The global occurrence of plant root-associated fungal endophytes and their great abundance in many habitats necessitate studies to decipher their potential functions. Improved understanding of the basic endophyte ecology including host range, host preference, and host responses to endophyte colonization has been made possible through populations of endophytes (e.g., Periconia macrospinosa and Microdochium sp.) isolated from North American native tallgrass prairie. The recent demonstration of the endophyte symbiosis of the model plant Arabidopsis thaliana has provided additional tools to further elucidate the ecology of these endophytes. The availability of a large number of Arabidopsis ecotypes and mutants, microarrays, and databases allows the molecular dissection of endophyte symbiosis to better understand the importance of fungal endophytes in host nutrient uptake, defenses, and/or responses to pathogens and stress. In this chapter, we discuss the ecology and functions of endophytic fungi through experiments utilizing the Arabidopsis model system. We draw parallels with another deeply dissected Piriformospora indica root endophyte symbiosis, which has been demonstrated to promote growth of model and non-model plants.

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References

  • Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13

    Google Scholar 

  • Alberton O, Kuyper TW, Summerbell RC (2010) Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 328:459–470

    CAS  Google Scholar 

  • Alfano JR, Collmer A (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683–1698

    PubMed  CAS  Google Scholar 

  • Alfano G, Lewis Ivey ML, Cakir C, Bos JIB, Miller SA, Madden LV, Kamoun S, Hitink HAJ (2007) Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97:429–437

    PubMed  CAS  Google Scholar 

  • Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM (2009) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151:2006–2017

    PubMed  CAS  Google Scholar 

  • Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic related compounds predominantly modulate the soil microbiome. J Biol Chem. doi:10.1074/jbc.M112.433300

    Google Scholar 

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

    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

    PubMed  Google Scholar 

  • Beattie GA, Lindow SE (1995) The secret life of foliar bacterial pathogens on leaves. Annu Rev Phytopathol 33:145–172

    PubMed  CAS  Google Scholar 

  • Betsuyaku S, Sawa S, Yamada M (2011) The function of the CLE peptide in plant development and plant-microbe interactions. Arab Book 9:e0149

    Google Scholar 

  • Bonfante P (1984) Anatomy and morphology of VA Mycorrhizae. In: Powell CL, Joseph Bagyaraj D (eds) VA mycorrhiza. CRC Press, Conway, pp 5–33

    Google Scholar 

  • Bonfante P (2001) At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton. In: Hock B (ed) Mycota, IX fungal associations. Springer, Berlin, pp 45–91

    Google Scholar 

  • Bressan M, Roncato MA, Bellvert F, Comte G, Haichar FZ, Achouak W, Berge O (2009) Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J 3:1243–1257

    PubMed  CAS  Google Scholar 

  • Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744

    PubMed  CAS  Google Scholar 

  • Bulgarelli A, Rott M, Schlaeppi K, Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95

    PubMed  CAS  Google Scholar 

  • Camehl I, Sherameti I, Venus Y, Bethke A, Varma A, Lee J, Oelmüller R (2010) Ethylene signaling 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 Phytol 185:1062–1073

    PubMed  CAS  Google Scholar 

  • Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I et al (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7:e1002051

    PubMed  CAS  Google Scholar 

  • Cartieaux F, Thibaud MC, Zimmerli L, Lessard P, Sarrobert C, David P, Gerbaud A, Robaglia C, Somerville S, Nussaume L (2003) Transcriptome analysis of Arabidopsis colonized by a plant growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J 36:177–188

    PubMed  CAS  Google Scholar 

  • Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS One 8(2):e55731

    PubMed  CAS  Google Scholar 

  • Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kim YC (2008) 2R,3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant Microbe Interact 21:1067–1075

    PubMed  CAS  Google Scholar 

  • Conn VM, Walkr AR, Franco CMM (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–218

    PubMed  CAS  Google Scholar 

  • Day B, Knepper C (2010) From perception to activation: the molecular-genetic and biochemical landscape of disease resistance signaling in plants. Arab Book 8:e012

    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

    PubMed  CAS  Google Scholar 

  • Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145:875–889

    PubMed  CAS  Google Scholar 

  • Doornbos RF, Geraats BPJ, Kuamae EE, Van Loon LC, Bakker PAHM (2011) Effects of jasmonic acid, ethylene and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol Plant Microbe Interact 24:395–407

    PubMed  CAS  Google Scholar 

  • Duplessis S, Courty P, Tagu D, Martin F (2005) Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol 165:599–611

    PubMed  CAS  Google Scholar 

  • Ercolani GL (1978) Pseudomonas savastanoi and other bacteria colonizing the surface of olive leaves in the field. J Gen Appl Microbiol 109:245–257

    Google Scholar 

  • Felle HH, Waller F, Molitor A, Kogel KH (2009) The mycorrhiza fungus Piriformospora indica induces fast root-surface pH signaling and primes systemic alkanization of the leaf apoplast upon powdery mildew infection. Mol Plant Microbe Interact 22:1179–1185

    PubMed  CAS  Google Scholar 

  • Franken P (2012) The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl Microbiol Biotechnol 96:1455–1464

    PubMed  CAS  Google Scholar 

  • Gallou A, Declereck S, Cranenbrouck S (2012) Transcriptional regulation of defence genes and involvement of the WRKY transcription factor in arbuscular mycorrhizal potato root colonization. Funct Integr Genomics 12:183–198

    PubMed  CAS  Google Scholar 

  • Garcia E, Alonso A, Platas G, Sacristan S (2012) The endophytic mycobiota of Arabidopsis thaliana. Fungal Divers. doi:10.1007/s13225-012-0219-0

    Google Scholar 

  • Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi and the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20:1407–1420

    PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    PubMed  CAS  Google Scholar 

  • Gorfer M, Klaubauf S, Bandian D, Strauss J (2007) Cadophora finlandia and Phialocephala fortinii: Agrobacterium-mediated transformation and functional GFP expression. Mycol Res 111:850–855

    PubMed  CAS  Google Scholar 

  • Grünig CR, Queloz V, Sieber TN, Holdenrieder O (2008a) Phialocephala fortinii s.l.-Acephala applanata species complex in tree roots: classification, population biology and ecology. Botany 86:1355–1369

    Google Scholar 

  • Grünig CR, Duò A, Sieber TN, Holdenrieder O (2008b) Assignment of species rank to six reproductively isolated cryptic species of the Phialocephala fortinii s.l.–Acephala applanata species complex. Mycologia 100:47–67

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Harman GE, Petzoldt R, Comis A, Chen J (2004b) Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology 94:147–153

    PubMed  Google Scholar 

  • Hartnett DC, Hetrick BAD, Wilson GWT, Gibson DJ (1993) Mycorrhizal influence on intra- and interspecific neighbour interactions among co-occurring prairie grasses. J Ecol 81:787–795

    Google Scholar 

  • Hartnett DC, Samanus RJ, Fischer LE, Hetrick BAD (1994) Plant demographic responses to mycorrhizal symbiosis in tallgrass prairie. Oecologia 99:21–26

    Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Stracck D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 58:101–110

    Google Scholar 

  • Hayward A, Vighnesh G, Delay C, Samian MR, Manoli S, Stiller J, McKenzie M, Edwards D, Batley J (2012) Second-generation sequencing for gene discovery in the Brassicaceae. Plant Biotechnol 10:750–759

    CAS  Google Scholar 

  • Herrera J, Khidir HH, Eudy DM, Porras-Alfaro A, Natvig DO, Sinsabaugh RL (2010) Shifting fungal endophyte communities colonize Bouteloua gracilis: effect of host tissue and geographical distribution. Mycologia 102:1012–1026

    PubMed  Google Scholar 

  • Hetrick BAD, Kitt DG, Wilson G (1988) Mycorrhizal dependence and growth of warm-season and cool-season tallgrass prairie plants. Can J Bot 66:1376–1380

    Google Scholar 

  • Hetrick BAD, Wilson GT, Todd TC (1992) Relationships of mycorrhizal symbiosis, rooting strategy and phenology among tallgrass prairie forbs. Can J Bot 70:1521–1528

    Google Scholar 

  • Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A (2012) Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol 196:520–534

    PubMed  CAS  Google Scholar 

  • Hirsch PR, Mauchline TH (2012) Who’s who in the plant root microbiome. Nat Biotechnol 30:961–962

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Jakob K, Goss EM, Araki H, Van T, Kreitman M, Bergelson J (2002) Pseudomonas viridiflava and P. syringae-natural pathogens of Arabidopsis thaliana. Mol Plant Microbe Interact 15:1195–1203

    PubMed  CAS  Google Scholar 

  • Johansson T, Le Quéré A, Ahren D, Söderström B, Erlandsson R, Lundberg J, Uhlén M, Tunlid A (2004) Transcriptional responses to Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant Microbe Interact 17:202–215

    PubMed  Google Scholar 

  • Jones AM, Chory J, Dangl JL, Esteelle M, Jacobson SE, Meyerowitz EM, Nordborg M, Weigel D (2008) The impact of Arabidopsis on human health: diversifying our portfolio. Cell 133:939–943

    PubMed  CAS  Google Scholar 

  • Jumpponen A (2001) Dark septate endophytes – are they mycorrhizal? Mycorrhiza 11:207–211

    Google Scholar 

  • Jumpponen A (2011) Analysis of ribosomal RNA indicates seasonal fungal community dynamics in Andropogon gerardii roots. Mycorrhiza 21:453–464

    PubMed  CAS  Google Scholar 

  • Jumpponen A, Trappe JM (1998a) Dark septate endophytes: a review of facultative biotrophic root colonizing fungi. New Phytol 140:295–310

    Google Scholar 

  • Jumpponen A, Trappe JM (1998b) Performance of Pinus contorta inoculated with two strains of root endophytic fungus Phialocephala fortinii: effects of resynthesis system and glucose concentration. Can J Bot 76:1205–1213

    CAS  Google Scholar 

  • Junker C, Draeger S, Schulz B (2012) A fine line-endophytes or pathogens in Arabidopsis thaliana. Fungal Ecol 5:657–662

    Google Scholar 

  • Kageyama SA, Mandyam K, Jumpponen A (2008) Diversity, function and potential functions of root associated endophytes. In: Varma A (ed) Mycorrhiza, 3rd edn. Springer, Berlin, pp 29–58

    Google Scholar 

  • Khatabi B, Molitor A, Lindermayr C, Pfiffi S, Durner J, von Wettstein D, Kogel KH, Schäfer P (2012) Ethylene supports colonization of plant roots by the mutualistic fungus Piriformospora indica. PLoS One 7:e35502

    PubMed  CAS  Google Scholar 

  • Khidir HH, Eudy DM, Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2010) A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. J Arid Environ 74:35–42

    Google Scholar 

  • Kloepper JW, Ryu CM (2006) Bacterial endophytes as elicitors of induced systemic resistance. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes, vol 9, Soil biology. Springer, Berlin/Heidelberg, pp 33–52

    Google Scholar 

  • Knapp DG, Pintye A, Kovács GM (2012) The dark side is not fastidious – dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PLoS One 7:e32570

    PubMed  CAS  Google Scholar 

  • Kniskern JM, Traw MB, Bergelson J (2007) Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol Plant Microbe Interact 20:1512–1522

    PubMed  CAS  Google Scholar 

  • Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921

    PubMed  CAS  Google Scholar 

  • Kwon YS, Ryu C-M, Lee S, Han KS, Lee JH, Lee K, Chung WS, Jeong M-J, Kim HK, Bae D-W (2010) Proteome analysis of Arabidopsis seedlings exposed to bacterial volatiles. Planta 232:1355–1370

    PubMed  CAS  Google Scholar 

  • Lahrmann U, Zuccaro A (2012) Opprimo ergo sum-evasion and suppression in the root endophytic fungus Piriformospora indica. Mol Plant Microbe Interact 25:727–737

    PubMed  CAS  Google Scholar 

  • Laluk K, Mengiste T (2010) Necrotroph attacks on plants: wanton destruction or covert extortion? Arab Book 8:e0136

    Google Scholar 

  • Le Quere A, Wright DP, Soderstrom B, Tunlid A, Johansson T (2005) Global patterns of gene regulation associated with the development of ectomycorrhiza between birch (Betula pendula Roth.) and Paxillus involutus (Batsch) Fr. Mol Plant Microbe Interact 18:659–673

    PubMed  Google Scholar 

  • Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B, Oelmuller R, Yeh KW (2011) Growth promotion of the Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol Plant Microbe Interact 24:421–431

    PubMed  CAS  Google Scholar 

  • Léon-Kloosterziel KM, Verhagen BWM, Keurentjes JJB, VanPelt JA, Rep M, VanLoon LC, Pieterse CMJ (2005) Colonization of the Arabidopsis rhizosphere by fluorescent pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle. Plant Mol Biol 57:731–748

    PubMed  Google Scholar 

  • Lin L, Ge HM, Yan T, Qin YH, Tan RX (2012) Thaxtomin A-deficient endophytic Streptomyces sp. enhances plant disease resistance to pathogenic Streptomyces scabies. Plants 236:1849–1861

    CAS  Google Scholar 

  • López-Bucio J, Campos-Cuevas JC, Hernández-Calderon E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20:207–217

    PubMed  Google Scholar 

  • Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Glavina del Rio T, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90

    PubMed  CAS  Google Scholar 

  • Mandyam K, Jumpponen A (2005) Abundance and possible functions of the root- colonizing dark septate endophytic fungi. In: Summerbell R, Currah RS, Sigler L (eds) The missing lineages: phylogeny and ecology of endophytic and other enigmatic root- associated fungi, vol 53, Studies in mycology., pp 173–189

    Google Scholar 

  • Mandyam K, Jumpponen A (2008) Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment. Mycorrhiza 18:145–155

    PubMed  Google Scholar 

  • Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102:813–821

    PubMed  Google Scholar 

  • Mandyam K, Fox C, Jumpponen A (2012) Septate endophyte colonization and host responses of grasses and forbs native to a tallgrass prairie. Mycorrhiza 22:109–119

    PubMed  Google Scholar 

  • Mandyam K, Roe J, Jumpponen A (2013) Arabidopsis thaliana model system reveals a continuum of responses to root endophyte colonization. Fungal Biol 117:25–260

    Google Scholar 

  • Mayerhofer MS, Kernaghan G, Harper KA (2013) The effects of fungal root endophytes in plant growth: a meta-analysis. Mycorrhiza 23:119–128

    PubMed  Google Scholar 

  • McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25:79–82

    PubMed  CAS  Google Scholar 

  • McLellan CA, Turbyville TJ, Wijeratne EMK, Kerschen A, Vierling E, Queitsch C, Whitesell L, Gunatilaka AAL (2007) A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an HSP90 inhibitor. Plant Physiol 145:174–182

    PubMed  CAS  Google Scholar 

  • Micali C, Göllner K, Humphry M, Consonni C, Panstruga R (2008) Powdery mildew disease of Arabidopsis: a paradigm for the interaction between plants and biotrophic fungi. Arab Book 6:e0115

    Google Scholar 

  • Micallef SA, Channer S, Shiiaris MP, Colon-Carmona A (2009a) Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere. Plant Signal Behav 4:777–780

    PubMed  Google Scholar 

  • Micallef SA, Shiaris MP, Colon-Carmona A (2009b) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742

    PubMed  CAS  Google Scholar 

  • Molitor A, Zajic D, Voll LM, Kühnemann JP, Samans B, Kogel KH, Waller F (2011) Barley leaf transcriptome and metabolite analysis reveals new aspects of compatibility and Piriformospora indica-mediated systemic induced resistance to powdery mildew. Mol Plant Microbe Interact 24:1427–1439

    PubMed  CAS  Google Scholar 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793

    PubMed  CAS  Google Scholar 

  • Nishimura MT, Dangl JL (2010) Arabidopsis and the plant immune system. Plant J 61:1053–1066

    PubMed  CAS  Google Scholar 

  • Nongbri P, Johnson JM, Sherameti I, Glawischnig E, Halkier BA, Oelmüller R (2012) Indole-3-acetaldoxime-derived compounds restrict root colonization in the beneficial interaction between Arabidopsis roots and the endophyte Piriformospora indica. Mol Plant Microbe Interact 25:1186–1197

    PubMed  CAS  Google Scholar 

  • Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17

    Google Scholar 

  • Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328

    PubMed  CAS  Google Scholar 

  • PeÅ¡kan-Berghöfer 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 Planta 122:465–477

    Google Scholar 

  • Petersen RL, Wagg C, Paulter M (2008) Associations between microfungal endophytes and roots: do structural features indicate function? Botany 86:445–456

    Google Scholar 

  • Pieterse CMJ, vanWees SCM, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Queloz V, Sieber TN, Holdenrieder O, McDonald BA, Grunig CR (2011) No biogeographical pattern for a root-associated fungal species complex. Glob Ecol Biogeogr 20:160–169

    Google Scholar 

  • Reboutier D, Bianchi M, Brault M, Roux C, Dauphin A, Rona JP, Legué V, Lapeyrie F, Bouteau F (2002) The indolic compound hypaphorine produced by ectomycorrhizal fungus interferes with auxin action and evokes early responses in non-host Arabidopsis thaliana. Mol Plant Microbe Interact 15:932–938

    PubMed  CAS  Google Scholar 

  • Reininger V, Sieber TN (2012) Mycorrhiza reduces adverse effects of dark septate endophytes (DSE) on growth of conifers. PLoS One 7:e42865

    PubMed  CAS  Google Scholar 

  • Reininger V, Grunig CR, Sieber TN (2012) Host species and strain combination determine growth reduction of spruce and birch seedlings colonized by root-associated dark septate endophytes. Environ Microbiol 14:1064–1076

    PubMed  Google Scholar 

  • Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ryu CM, Farag M, Hu CH, Reddy MS, Pare P, Kloepper JW (2004a) Bacterial volatiles induced systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    PubMed  CAS  Google Scholar 

  • Ryu C-M, Murphy JF, Mysore KS, Kloepper JW (2004b) Plant Growth-Promoting Rhizobacteria Protect Systemically Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J 39:381–392

    PubMed  CAS  Google Scholar 

  • Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 286:285–292

    Google Scholar 

  • Ryu C-M, Murphy JF, Reddy MS, Kloepper JW (2007) A two strain mixture of rhizobacteria elicits induction of systemic resistance against Pseudomonas syringae and Cucumber mosaic virus coupled to promote plant growth on Arabidopsis thaliana. J Microbiol Biotechnol 17:280–286

    PubMed  CAS  Google Scholar 

  • Scervino JM, Gottlieb A, Silvani VA, Pérgola M, Fernández L, Godeas AM (2008) Exudates of dark septate endophyte (DSE) modulate the development of the arbuscular mycorrhizal fungus (AMF) Gigaspora rosea. Soil Biol Biochem 41:1753–1756

    Google Scholar 

  • Schäfer P, Khatabi B, Kogl KH (2007) Root cell death and systemic effects of Piriformospora indica: a study on mutualism. FEMS Microbiol Lett 275:1–7

    PubMed  Google Scholar 

  • Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, Scholz U, Pons-Kühnemann J, Sonnewald S, Sonnewald U, Kogel KH (2009) Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 59:461–474

    PubMed  Google Scholar 

  • Schwachtje J, Karojet S, Thormahlen I, Bernholz C, Kunz S, Brouwer S, Shwochow M, Kohl K, van Dongen JT (2011) A naturally associated rhizobacterium of Arabidopsis thaliana induces a starvation-like transcriptional response while promoting growth. PLoS One 6(12):e29382

    PubMed  CAS  Google Scholar 

  • Selosse MA, Dubois MP, Alavrez A (2009) Do sebacinales commonly associate with plant roots as endophytes? Mycol Res 113:1062–1069

    PubMed  CAS  Google Scholar 

  • Shahollari B, Vadassery J, Varma A, Oelmüller 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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 which binds to a conserved motif in their promoters. J Biol Chem 280:2641–2647

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Shi CL, Park HB, Lee JB, Ryu S, Ryu CM (2010) Inhibition of primary roots and stimulation of lateral root development in Arabidopsis thaliana by the rhizobacterium Serratia marcescens 90-166 is through both auxin-dependent and –independent signaling pathways. Mol Cells 29:251–258

    PubMed  CAS  Google Scholar 

  • Shoresh M, Harman GE (2008) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147:2147–2163

    PubMed  CAS  Google Scholar 

  • Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76–84

    PubMed  CAS  Google Scholar 

  • Shoresh M, Gal-On A, Leibman D, Chet I (2006) Characterization of a mitogen-activated protein kinase gene from cucumber required for Trichoderma-conferred plant resistance. Plant Physiol 142:1169–1179

    Google Scholar 

  • Sirrenburg 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 Planta 131:581–589

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Stacey G, McAlwin CB, Kim SY, Olivares J, Soto MJ (2006) Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicas and Medicago truncatula. Plant Physiol 141:1473–1481

    PubMed  CAS  Google Scholar 

  • Stein E, Molitor A, Kogel KH, Wallr F (2008) Systemic resistance in Arabidopsis by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49:1747–1751

    PubMed  CAS  Google Scholar 

  • Sugiyama A, Bakker MG, Badri DV, Manter DK, Vivanco JM (2013) Relationships between Arabidopsis genotype-specific biomass accumulation and associated soil microbial communities. Botany 91:123–126

    CAS  Google Scholar 

  • Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers drought resistance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017

    PubMed  CAS  Google Scholar 

  • Tellenbach C, Sieber TN (2012) Do colonization by dark septate endophytes and elevated temperature affect pathogenicity of oomycetes? FEMS Microbiol Ecol 82:157–168

    PubMed  CAS  Google Scholar 

  • Tellenbach C, Grunig CR, Sieber TN (2011) Negative effects on survival and performance of Norway spruce seedlings colonized by dark septate root endophytes are primarily isolate-dependent. Environ Microbiol 1:2508–2517

    Google Scholar 

  • Tellenbach C, Sumarah MW, Grünig CR, Miller JD (2013) Inhibition of Phytophthora species by secondary metabolites produced by the dark septate endophyte Phialocephala europaea. Fungal Ecol 6:12–18

    Google Scholar 

  • Thaler JS, Fidantsef AL, Duffey SS, Bostock RM (1999) Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. J Chem Ecol 25:1597–1609

    CAS  Google Scholar 

  • Thaler JS, Owen B, Higgins VJ (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 135:530–538

    PubMed  CAS  Google Scholar 

  • Thilmony R, Fumiaki Katagiri F, He SY (2002) The Arabidopsis thaliana-Pseudomonas syringae interaction. Arab Book 1:e0039

    Google Scholar 

  • Thomma B, Penninckx I, Broekaert WF, Cammue BPA (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68

    PubMed  CAS  Google Scholar 

  • Traw BM, Knsikern JM, Bergelson J (2007) SAR increases fitness of Arabidopsis thaliana in the presence of natural bacterial pathogens. Evolution 61:2444–2449

    PubMed  Google Scholar 

  • Truyens S, Weyens N, Cuypers A, Vangronsveld J (2012) Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana. Plant Biol. doi:10.1111/j.1438-8677.2012.00711.x

    PubMed  Google Scholar 

  • Tsuji J, Somerville SC (1992) First report of the natural infection of Arabidopsis thaliana by Xanthomonas campestris pv. campestris. Plant Dis 761:539

    Google Scholar 

  • Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe Interact 21:1371–1383

    PubMed  CAS  Google Scholar 

  • Vadassery J, Ranf S, Drzewiecki C, Mithöfer A, Mazarsa C, Scheel D, Lee J, Oelmüller R (2009a) A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59:193–206

    PubMed  CAS  Google Scholar 

  • Vadassery J, Tripathi S, Prasad R, Varma A, Oelmüller R (2009b) Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J Plant Physiol 166:1263–1274

    PubMed  CAS  Google Scholar 

  • Varma A, Sudha S, 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 

  • Venus Y, Oelmüler R (2012) Arabidopsis ROP1 and ROP5 influence germination time, root morphology, the formation of F-actin bundles and symbiotic fungal interactions. Mol Plant. doi:10.1093/mp/sss101

    PubMed  Google Scholar 

  • Walker JF, Aldrich-Wolfe L, Riffel A, Barbare H, Simpson NB, Trowbridge J, Jumpponen A (2011) Diverse helotiales associated with the roots of three species of arctic ericaceae provide no evidence for host specificity. New Phytol 191:515–527

    PubMed  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Wettstein DV, 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

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Wang Y, Ohara Y, Nakayashiki H, Tosa Y, Mayama S (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant Microbe Interact 18:385–396

    PubMed  CAS  Google Scholar 

  • Weiss M, Sykorova Z, Garnica S, Riess K, Martos F, Krause C, Oberwinkler F, Bauer R, Redecker D (2011) Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. PLoS One 6:e16793

    PubMed  CAS  Google Scholar 

  • Woo SL, Scala F, Ruocco M, Lorito M (2006) The molecular biology of the interactions between Trichoderma spp., pathogenic fungi and plants. Phytopathology 96:181–185

    PubMed  CAS  Google Scholar 

  • Yu T, Nassuth A, Peterson RL (2001) Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots. Can J Bot 47:741–753

    CAS  Google Scholar 

  • Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Pare PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851

    PubMed  CAS  Google Scholar 

  • Zhao YF, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003) Virulence systems of Pseudomonas syringae pv. in tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–499

    PubMed  CAS  Google Scholar 

  • Zuccaro A, Lahrmann U, Guldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel KH (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7:e1002290

    PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported in part by the National Science Foundation Grants No. 0344838 and 0221489 (to AJ).

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Correspondence to Ari Jumpponen .

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Mandyam, K., Jumpponen, A. (2014). Unraveling the Dark Septate Endophyte Functions: Insights from the Arabidopsis Model. In: Verma, V., Gange, A. (eds) Advances in Endophytic Research. Springer, New Delhi. https://doi.org/10.1007/978-81-322-1575-2_6

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