Skip to main content
SpringerLink
Log in
Book cover

Fungal Associations pp 231–254Cite as

13 The Symbiotic Fungus Piriformospora indica: Review

  • Chapter
  • First Online:

Part of the book series: The Mycota ((MYCOTA,volume 9))

Abstract

The root endophyte Piriformospora indicabelongs to the Hymenomycetes (Basidiomycota), with a relatively close relationship to Rhizoctoniaand Sebacina. It drastically improves plant growth and overall biomass and can be easily cultivated on a variety of synthetic media. The hyphae colonize the plant root and show inter- and intracellular structures (vesicles and hyphal differentiations like arbuscules). Chlamydospores are formed both inside the root tissues and externally into the environment. It is already shown that P. indicahas a wide host range among monocots and dicots, including legumes. Biotechnological applications of this fungus open new perspectives in agriculture, floriculture, viticulture and the reclamation of degraded and heavily mined soils.

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

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

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Achatz B, Rüden SV, Andrade D, Neumann E, Kühnemann JP, Kogel KH, Philipp F, Waller F (2010) Root colonization by Piriformospora indicaenhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil 22:9–70

    Google Scholar 

  • Amiour N, Recorbet G, Robert F, Gianinazzi S, Dumas-Gaudot E (2006) Mutations in DMI2 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza. Mol Plant Microbe Interact 19:988–997

    Article  PubMed  CAS  Google Scholar 

  • Bandoni RJ (1984) The Tremellales and Auriculariales and alternative classification. Trans Mycol Soc Jpn 25:489–520

    Google Scholar 

  • Basiewicz M, Weiss M, Kogel K-H, Langen G, Zorn H, Zuccaro A (2012) Molecular and phenotypic characterization of Sebacina vermiferastrains associated with orchids, and the description of Piriformospora williamsiisp. nov. Fungal Biol 116:204–213

    Article  PubMed  CAS  Google Scholar 

  • Bhardwaj S (2011) Micronutrient enhancement in rice. PhD thesis, Amity University, Uttar Pradesh, India

    Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–8

    Article  PubMed  CAS  Google Scholar 

  • Broekaert WF, Delauré SL, De Bolle MF, Cammue BP (2006) The role of ethylene in host-pathogen interactions. Annu Rev Phytopathol 44:292–416

    Article  Google Scholar 

  • Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, Lee J, Oelmüller R (2010) Ethylene signalling and ethylene-targeted transcription factors are required to balance benefi cial and nonbenefi cial traits in the symbiosis between the endophytic fungus Piriformospora indicaand Arabidopsis thaliana. New Phytol 185:1062–1072

    Article  PubMed  CAS  Google Scholar 

  • Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmüller R (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7(5):e1002051

    Article  PubMed  CAS  Google Scholar 

  • Chauhan AK, Das A, Kharkwal AC, Varma A (2006) Impact of micro-organisms on environment and health. In: Chauhan AK, Varma A (eds) Microbiology series-microbes: health and environment. International Publishing, I.K, New Delhi, pp 1–12

    Google Scholar 

  • Contesto C, Milesi S, Mantelin S, Zancarini A, Desbrosses G, Varoquaux F, Bellini C, Kowalczyk M, Touraine B (2010) The auxin-signaling pathway is required for the lateral root response of Arabidopsisto the rhizobacterium Phyllobacterium brassicacearum. Planta 222:1455–1470

    Article  Google Scholar 

  • Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592

    Article  PubMed  CAS  Google Scholar 

  • Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18

    Article  PubMed  Google Scholar 

  • Deshmukh S, Kogel KH (2007) Piriformospora indicaprotects barley from root rot disease caused by Fusarium. J Plant Dis Prot 114:262–268

    Google Scholar 

  • Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH (2006) The root endophytic fungus Piriformospora indicarequires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci USA 102:18450–18457

    Article  Google Scholar 

  • Druege U, Baltruschat H, Franken P (2007) Piriformospora indicapromotes adventitious root formation in cuttings. Sci Hortic 112:422–426

    Article  Google Scholar 

  • Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Büttner C, Grosch R, Schwarz D, Franken P (2009) Impact of Piriformospora indicaon tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20:191–200

    Article  PubMed  Google Scholar 

  • Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legué V (2009) The ectomycorrhizal fungus Laccaria bicolorstimulates lateral root formation in poplar and Arabidopsisthrough auxin transport and signaling. Plant Physiol 151:1991–2005

    Article  PubMed  CAS  Google Scholar 

  • Fester T, Maier W, Strack D (1998) Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza 8:241–246

    Article  Google Scholar 

  • Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987

    Article  PubMed  CAS  Google Scholar 

  • Franken P, Requena N, Butehorn B, Krajinski F, Kuhn G, Lapopin L, Mann P, Rhody D, Stommel M (2000) Molecular analysis of the arbuscular mycorrhiza symbiosis. Arch Acker Pft Boden 45:271–286

    CAS  Google Scholar 

  • Ginzberg I, David R, Shaul O, Elad Y, Winiger S, Ben-Dor B, Badani H, Fang Y, von Rhijn P, Li Y, Hirsch AM, Kapulnik Y (1998) Glomus intraradicescolonization regulates gene expression in tobacco roots. Symbiosis 25:145–157

    CAS  Google Scholar 

  • Gosal SK, Karlupia A, Gosal SS, Chhibba IM, Varma A (2010) Biotization with Piriformospora indicaand Pseudomonas fluorescensimproves survival rate, nutrient acquisition, field performance and saponin content of micropropagated Chlorophytumsp. Indian J Biotechnol 9:289–297

    CAS  Google Scholar 

  • Grunewald W, Cannoot B, Friml J, Gheysen G (2009a) Parasitic nematodes modulate PIN mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266

    Article  PubMed  Google Scholar 

  • Grunewald W, Van Noorden G, Van Isterdael G, Beeckman T, Gheysen G, Mathesius U (2009b) Manipulation of auxin transport in plant roots during Rhizobiumsymbiosis and nematode parasitism. Plant Cell 21:2552–2562

    Google Scholar 

  • Harman GE (2011) Multifunctional fungal plant symbiont: new tools to enhance plant growth and productivity. New Phytol 189:647–649

    Article  PubMed  Google Scholar 

  • Hill TW, Käfer E (2001) Improved protocols for aspergillus medium: trace elements and minimum medium salt stock solutions. Fungal Genet Newslett 48:20–21

    Google Scholar 

  • Hirt H, Garcia AV, Oelmüller R (2011) AGC kinase in plant development and defense. Plant Signal Behav 6:1–4

    Article  Google Scholar 

  • Johnson PR, Ecker JR (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annu Rev Genet 22:227–254

    Article  Google Scholar 

  • Johnson JM, Oelmüller R (2009) Mutualism or parasitism: life in an unstable continuum. What can we learn from the mutualistic interaction between Piriformospora indicaand Arabidopsis thaliana. Endocyt Cell Res 19:81–110

    Google Scholar 

  • Kaldorf M, Koch B, Rexer KH, Kost G, Varma A (2005) Patterns of interaction between Populus Esch5 and Piriformospora indica: a transition from mutualism to antagonism. Plant Biol 7:210–218

    Article  PubMed  CAS  Google Scholar 

  • Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol 117:265–286

    Article  Google Scholar 

  • Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790

    Article  PubMed  CAS  Google Scholar 

  • Kumar M, Yadav V, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A Phosphate Transporter from the Root Endophytic Fungus Piriformospora indicaPlays a Role in Phosphate Transport to the Host Plant. J Biol Chem 285:26522–26544.

    Google Scholar 

  • Kumar M, Yadav V, Kumar H, Sharma R, Singh A, Tuteja N, Johri AK (2011) Piriformospora indicaenhances plant growth by transferring phosphate. Plant Signal Behav 6:1–2

    Article  Google Scholar 

  • Kumar V, Sahai V, Bisaria VS (2011) High-density spore production of Piriformospora indica, a plant growth-promoting endophyte, by optimization of nutritional and cultural parameters. Bioresource Technology 102: 3169–3175.

    Article  PubMed  CAS  Google Scholar 

  • Kumari R, Sachdev M, Garg AP, Varma A (2004a) Symbiotic fungi for eco-friendly environment: a perspective. Nat Prod Rad CSIR 2:296–400

    Google Scholar 

  • Kumari R, Pham GH, Prasad R, Sachdev M, Srivastava A, Yadav V, Verma PK, Sharma S, Malla R, Singh A, Maurya AK, Prakash S, Pareek A, Rexer KH, Kost G, Garg AP, Oelmueller R, Sharma MC, Varma A (2004b) Piriformospora indica: fungus of the millennium. In: Podila G, Varma A (eds) Basic research and applications: mycorrhizas. IK International, New Delhi, pp 259–295

    Google Scholar 

  • Kumari R, Sachdev M, Garg AP, Varma A (2004c) Biological hardening of micropropagated plants of horticultural importance. In: Podila G, Varma A (eds) Basic research and applications: mycorrhizas. IK International, New Delhi, pp 229–262

    Google Scholar 

  • Lee Y-C, Michal Johnson J, Chien C-T, Sun C, Cai D, Lou B, Oelmüller R, Yeh K-W (2011) Growth promotion of Chinese cabbage and Arabidopsisby Piriformospora indicais not stimulated by mycelium-synthesized auxin. Mol Plant Microbe Interact 24:421–421

    Article  PubMed  CAS  Google Scholar 

  • Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 210:1180–1182

    Article  Google Scholar 

  • Ludwig-Müller J, Güther M (2007) Auxins as signals in arbuscular mycorrhiza formation. Plant Signal Behav 2:194–196

    Article  PubMed  Google Scholar 

  • Luo ZB, Janz D, Jiang X, Göbel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A (2009) Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol 151:1902–1917

    Article  PubMed  CAS  Google Scholar 

  • Maier W, Peipp H, Schmidt J, Wray V, Strack D (1995) Levels of a terpenoid glycoside (blumenin) and cell wall-bound phenolics in cereal mycorrhizas. Plant Physiol 109:465–470

    Article  PubMed  CAS  Google Scholar 

  • Matsushima R, Fukao Y, Nishimura M, Hara-Nishimura I (2004) NAI1 gene that encodes a basic-helix-loop-helix-type putative transcription factor that regulates the formation of a novel ER-derived structure, the ER body. Plant Cell 16:1526–1549

    Google Scholar 

  • McKendrick SL, Leake JR, Taylor D, Lee RDJ (2002) Symbiotic germination and development of the myco-heterotrophic orchid Neottia nidus-avisin nature and its requirement for locally distributed Sebacinaspp. New Phytol 154:222–247

    Article  Google Scholar 

  • Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobiumin the absence of nodule organogenesis. Science 215:101–104

    Article  Google Scholar 

  • Nitz I, Berkefeld H, Puzio PS, Grundler FM (2001) Pyk10, a seedling and root specific gene and promoter from Arabidopsis thaliana. Plant Sci 161:227–246

    Article  Google Scholar 

  • Oberwinkler F (1964) Intrahymeniale heterobasisiomyceten. Fruchtkorperlose Sebacina- Sippen und ihre systematische Stellung. Nova Hedwigia 7:489–498

    Google Scholar 

  • Oelmüller R, Shahollari B, Peškan-Berghöfer T, Trebicka A, Giong PH, Sherameti I, Oudhoff M, Venus Y, Altschmied L, Varma A (2004) Molecular analyses of the interaction between Arabidopsisroots and the growth-promoting fungus Piriformospora indica. Endocyt Cell Res 15:504–517

    Google Scholar 

  • Oelmüller R, Peškan-Berghöfer T, Shahollari B, Sherameti I, Varma A (2005) MATH domain containing proteins represent a novel gene family in Arabidopsis thalianaand are involved in plant/microbe interactions. Physiol Plant 124:152–166

    Article  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

    Article  Google Scholar 

  • Perrine-Walker F, Doumas P, Lucas M, Vaissayre V, Beauchemin NJ, Band LR, Chopard J, Crabos A, Conejero G, Péret B, King JR, Verdeil JL, Hocher V, Franche C, Bennett MJ, Tisa LS, Laplaze L (2010) Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glaucaactinorhizal nodules. Plant Physiol 154:1272–1280

    Article  Google Scholar 

  • Peškan-Berghöfer T, Shahollari B, Giang PH, Hehl S, Markert C, Blanke V, Varma AK, Oelmüller R (2004) Association of Piriformospora indicawith Arabidopsis thalianaroots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmatic reticulum and at the plasma membrane. Physiol Plant 122:465–477

    Article  Google Scholar 

  • Pham GH, Singh AN, Malla R, Kumari R, Prasad R, Sachdev M, Rexer K-H, Kost G, Luis P, Kaldorf M, Buscot F, Herrmann S, Peškan T, Oelmüller R, Saxena AK, Declerck S, Mittag M, Stabentheiner E, Hehl S, Varma A (2004a) Interaction of Piriformospora indicawith diverse microorganisms and plants. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin Heidelberg New York, pp 227–265

    Google Scholar 

  • Pham GH, Kumari R, Singh AN, Kaldorf M, Buscot F, Oelmüller R, Tatjana P, Weiss M, Hampp R, Varma A (2004b) Axenic cultures of Piriformospora indica. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin Heidelberg New York, pp 592–615

    Google Scholar 

  • Prasad R (2008) Studies on interaction between symbiotic fungus (Piriformospora indica), rhizobacteria and selected plants. PhD thesis, Merrut University, Merrut

    Google Scholar 

  • Pritsch K, Emanuel CP, Churin J-L, Cloutier-Hurteau B, Arif AM, Damon C, Duchemin M, Egli S, Ernst J, Fraissinet-Tachet L, Kuhar F, Legname E, Marmeisse R, Müller A, Nikolova P, Peter M, Plassard C, Richard F, Schloter M, Selosse M-A, Franc A, Garbaye J (2011) Optimized assay and storage conditions for enzyme activity profiling of ectomycorrhizae. Mycorrhiza 21:589–600

    Article  PubMed  CAS  Google Scholar 

  • Qiang X, Weiss M, Kogel K-H, Schaefer P (2011) Piriformospora indica- A mutualstic basidiomycete with an exceptionally large plant host range. Mol Plant Pathol. doi:10.1111/J.1364-3703.2011.00764.X

  • Rai M, Varma A (2005) Arbuscular mycorrhiza-like biotechnological potential of Piriformospora indica, which promotes the growth of Adhatoda vasicaNees. Electron J Biotechnol 8:107–112

    Article  Google Scholar 

  • Rai MK, Acharya D, Varma A, Chikhale NJ, Wadegaonkar PA, Thakare PV, Ramteke AP, Kirpan P, Shende S (2001) Arbuscular mycorrhizal fungi in growth promotional of medicinal plants. In: National workshop on conservation of medicinal aromatic plants, CFHRD, Chhindwara, 26–27 Dec 2001, pp 105–110

    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 nonhost Arabidopsis thaliana. Mol Plant Microbe Interact 15:922–928

    Article  Google Scholar 

  • Sahay NS (1999) Interaction of Piriformospora indicawith tissue culture raised plant. PhD thesis, Jawaharlal Nehru University, New Delhi

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sahay NS, Varma A (2000) Biological approach towards increasing the survival rates of micropropogated plants. Curr Sci 78:126–129

    Google Scholar 

  • Sahay NS, Sudha SA, Varma A (1998) Trends in endomycorrhizal research. Indian J Exp Biol NISCOM 26:1069–1086

    Google Scholar 

  • Schäfer P, Kogel KH (2009) The sebacinoid fungus Piriformospora indica: an orchid mycorrhiza which may increase host plant reproduction and fitness. In: Deising HB, Esser K (eds) The Mycota, vol 5, Plant relationships. Springer, Berlin Heidelberg New York, pp 99–112

    Google Scholar 

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

    Article  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 (2009a) Phytohormones in plant root – Piriformospora indica mutualism. Plant Signal Behav 4:669–671

    Article  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 (2009b) 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

    Article  PubMed  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1421–1422

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Shahollari B, Peškan-Berghöfer T, Varma A, Oelmüller R (2004) Receptor kinases with leucine-rich repeats are enriched in Triton X-100 insoluble plasma membrane microdomains from plants. Physiol Plant 122:297–402

    Article  Google Scholar 

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

    Article  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 indicain Arabidopsis thaliana. Plant J 50:1–12

    Article  PubMed  CAS  Google Scholar 

  • Sharma M, Chauhan G, Chandra A, Pushpangadan P, Varma A, Kharkwal H (2011) Piriformospora indicaVarma and Franken mediated enhancement of biomass and diosgenin production in Trigonella foenum-graecum. Medicinal Plants – Int J Phytomed Rel Ind 3:217–226

    Google Scholar 

  • Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller R (2005) The endophytic fungus Piriformospora indicastimulates the expression of Nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsisroots through a homeodomain transcription factor which binds to a conserved motif in their promoters. J Biol Chem 280:2641–2647

    Article  Google Scholar 

  • Sherameti I, Tripathi S, Varma A, Oelmüller R (2008a) The root-colonizing endophyte Piriformospora indicaconfers drought tolerance in Arabidopsisby stimulating the expression of drought stress-related genes in leaves. Mol Plant Microbe Interact 21:799–807

    Article  PubMed  CAS  Google Scholar 

  • Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM, Nitz I, Varma A, Grundler FM, Oelmüller R (2008b) PYK10, a β-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thalianaand the endophytic fungus Piriformospora indica. Plant J 54:428–429

    Article  PubMed  CAS  Google Scholar 

  • Singh A (2004) Immuno-characterization of Piriformospora indicaand other identical root endophytes. PhD thesis, Jawaharlal Nehru University, New Delhi

    Google Scholar 

  • Singh AN, Singh AR, Kumari M, Kumari R, Rai MK, Sharma AP, Varma A (2002a) AMF-like fungus: Piriformospora indica – a boon for plant industry. In: Prasad BN (ed) Biotechnology in sustainable biodiversity and food security. IBH, Oxford, pp 101–124

    Google Scholar 

  • Singh AN, Singh AR, Kumari M, Rai MK, Varma A (2002b) Biotechnology importance of Piriformospora indica – a novel symbiotic mycorrhiza-like fungus: an overview. Plant biotechnology special issue. Ind J Biotechnol Nat Inst Sci Commun CSIR 2:65–75

    Google Scholar 

  • Soniya B (2011) Micronutrient enhancement in Rice. PhD thesis, Amity University, Uttar Pradesh

    Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-2-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 21:425–448

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sudha (1999) In vitrostudy of endosymbionts associated with tissue culture raised medicinal plants. PhD thesis, Jamia Hamdard University, New Delhi

    Google Scholar 

  • Suman PR, Jain VK, Varma A (2010) Role of nanomaterials in symbiotic fungus growth enhancement. Curr Sci 99:1189–1191

    Google Scholar 

  • Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indicaconfers drought tolerance 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

    Article  PubMed  CAS  Google Scholar 

  • Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 215:104–107

    Article  Google Scholar 

  • Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) Piriformospora indica-mediated growth promotion in Arabidopsisis sensitive to high auxin levels, requires trans-cytokinin biosynthesis and the cytokinin receptor combination CRE1/AHK2. Mol Plant Microbe Interact 21:1271–1282

    Article  Google Scholar 

  • Vadassery J, Ranf S, Drzewiecki C, Mithöfer A, Mazars C, Scheel D, Lee J, Oelmüller R (2009a) A cell wall extract from Piriformospora indicapromotes growth of Arabidopsisseedlings and induces intracellular calcium elevation in roots. Plant J 59:192–206

    Article  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 indicaand Arabidopsis. J Plant Physiol 166:1262–1274

    Article  Google Scholar 

  • Van Rhijn P, Fang Y, Galili S, Shaul O, Atzmon N, Wininger S, Eshed Y, Lum M, Li Y, To Y, Fujishige N, Kapulnik Y, Hirsch AM (1997) Expression of early nodulin genes in alfalfa mycorrhizas indicates that signal transduction pathways used in forming arbuscular mycorrhizas and Rhizobium-induced nodules may be conserved. Proc Natl Acad Sci USA 94:5467–5472

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Varma A, Singh A, Sudha SN, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D, Bharti K, Franken P, Hurek T, Blechert O, Rexer K-H, Kost G, Hahn A, Hock B, Maier W, Walter M, Strack D, Kranner I (2001) Piriformospora indica: a cultivable mycorrhiza-like endosymbiotic fungus. In: Hock B (ed) Mycota IX. Springer, Berlin Heidelberg New York, pp 125–150

    Google Scholar 

  • Varma A, Singh AR, Sudha A, Sahay NS, Kumari M, Bharati K, Sarbhoy AK, Maier W, Walter MH, Strack D, Franken P, Singh AN, Malla R, Hurek T (2002) Piriformospora indica: a plant stimulator and pathogen inhibitor arbuscular mycorrhizalike fungus. In: Markandey DK, Markandey NR (eds) Microorganisms in Bioremediation. Capital Book Company, New Delhi, pp 71–89

    Google Scholar 

  • Varma A, Bakshi M, Lou B, Hartmann A, Oelmueller R (2012a) Piriformospora indica:a novel plant growth-promoting mycorrhizal fungus. Agric Res 1(2):117–131

    Article  Google Scholar 

  • Varma A, Kharkwal A, Agarwal A, Bajaj R, Prasad R (2012b) Piriformospora indica:the model microbe for organic green revolution. Biofertiliser Newsletter 20(1):3–8

    Google Scholar 

  • Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Butehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896–902

    Article  CAS  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 indicareprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:12286–12291

    Article  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 indicaand related Sebacinales species. J Plant Physiol 165:60–70

    Article  PubMed  CAS  Google Scholar 

  • Warcup JH, Talbot PHB (1967) Perfect states of Rhizoctoniaassociated with orchids. New Phytol 66:621–641

    Article  Google Scholar 

  • Weiß M, Oberwinkler F (2001) Phylogenetic relationships in Auricularialesand related groups-hypotheses derived from nuclear ribosomal DNA sequences. Mycol Res 105:402–415

    Article  Google Scholar 

  • Weiß M, Selosse MA, Rexer KH, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1002–1010

    Google Scholar 

  • Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285(34):26532–26544

    Article  PubMed  CAS  Google Scholar 

  • Zuccaro A, Basiewicz M, Zurawska M, Biedenkopf D, Kogel K-H (2009) Karyotype analysis, genome organization, and stable genetic transformation of the root colonizing fungus Piriformospora indica. Fungal Genet Biol 46:542–550

    Article  Google Scholar 

  • Zuccaro A, Lahrmann U, Güldener 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors from Amity University are thankful to DBT, ICAR and DRDO, India for partial financial funding.

Author information

Authors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, 201303, India

    A. Varma, S. Tripathi, R. Prasad, A. Das, M. Sharma, M. Bakshi, S. Bhardwaj, M. Arora, K. Rastogi, A. Agrawal, A. C. Kharkwal, S. Talukdar & K. S. Sree

  2. Institut für Allgemeine Botanik und Pflanzenphysiologie, Friedrich-Schiller Universität Jena, Dornburger Str. 159, 07743, Jena, Germany

    I. Sherameti, J. M. Johnson & R. Oelmüller

  3. Applied Microbiology Laboratory, Department of Life Sciences, University of Mumbai, Mumbai, Maharashtra, 400098, India

    U. S. Bagde

  4. Department of Biochemical Engineering and Biotechnology, Indian Institute of Technology, New Delhi, India

    V. S. Bisaria

  5. Department of Botany, Guru Ghasidas Central University, Koni, Bilaspur, 495009, Chattisgarh, India

    C. P. Upadhyaya

  6. Department of Molecular Biotechnology, Konkuk University, Seoul, 143701, South Korea

    P. S. Won

  7. Institute of Biotechnology, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Y. Chen, J. Ma & B. Lou

  8. Division of Biotechnology and Forensic Sciences, School of Contemporary Sciences, University of Abertay, Bell Street, Dundee, DD1 1HG, UK

    A. Adya

  9. Institute of Microbiology, Chinese Academy of Sciences, 8 Belertio Zhongguancun, Beijing, 100190, People’s Republic of China

    L. Zhang

  10. Research and Development, Defence Research Development Organization, 2, Tezpur, 784001, Assam, India

    M. K. Meghvansi

  11. College of Basic Science and Humanities, Punjab Agriculture University, Ludhiana Punjab, India

    S. K. Gosal

  12. Research and Development, Defence Institute of Higher Altitude Research, Defence Research Development Organization, Leh-Ladakh, India

    R. B. Srivastava

  13. School of Life Sciences, Jawaharlal Nehru University, New Delhi, 110067, India

    A. K. Johri, M. Kumar & M. Dua

  14. Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campus Grande Block C-2, Piso-5, Sala 03, 1749-016, Lisbon, Portugal

    C. Cruz (Faculty of Sciences)

Authors
  1. A. Varma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. Sherameti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Tripathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Bakshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. J. M. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. S. Bhardwaj
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. M. Arora
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. K. Rastogi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. A. Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. A. C. Kharkwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. S. Talukdar
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. U. S. Bagde
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. V. S. Bisaria
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. C. P. Upadhyaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. P. S. Won
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Y. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. J. Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. B. Lou
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. A. Adya
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. L. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. M. K. Meghvansi
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. K. S. Sree
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. S. K. Gosal
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. R. B. Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. A. K. Johri
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. M. Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. M. Dua
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. C. Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  32. R. Oelmüller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Varma .

Editor information

Editors and Affiliations

  1. Technical University of Munich, Alte Akademie 6, Freising, 85354, Bayern, Germany

    Bertold Hock

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Varma, A. et al. (2012). 13 The Symbiotic Fungus Piriformospora indica: Review. In: Hock, B. (eds) Fungal Associations. The Mycota, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30826-0_13

Download citation

Publish with us

Policies and ethics

Search

Navigation