Piriformospora indica: a versatile root endophytic symbiont

Anthony RG, Henriques R, Helfer A, Mészáros T, Rios G, Testerink C, Munnik T, Deák M, Koncz C, Bögre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581

Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983

Aslam SN, Erbs G, Morrissey KL, Newman MA, Chinchilla D, Boller T, Molinaro A, Jackson RW, Cooper RM (2009) Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: influences on perception or mobility and host defence responses. Mol Plant Pathol 10:375–387

Baltruschat H, Fodor J, Borbala H, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel K-H, Schafer 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

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

Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 2:101–106

Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant pathogen relations? Ecology 82:3057–3068

Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464:418–422

Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2010) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci U S A 107:14502–14507

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 beneficial and non-beneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol 185:1062–1073

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:e1002051

Camehl I, Sherameti I, Seebald E, Johnson JM, Oelmueller R (2013) Role of defense compounds in the beneficial interaction between Arabidopsis thaliana and Piriformospora indica. In: Varma A, Kost G, Oelmueller R (eds) Piriformospora indica—Sebacinales and their biotechnological applications. Springer, Germany, pp 239–250

Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544

Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 2:95–101

Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226

Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiß M, Waller F, Kogel K-H (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci U S A 103:18450–18457

Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276

Felle HH, Waller F, Molitor A, Kogel KH (2009) The mycorrhiza fungus Piriformospora indica induces fast root-surface pH signaling and primes systemic alkalinization of the leaf apoplast upon powdery mildew infection. Mol Plant Microbe Interact 9:1179–1185

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

Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011

Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 3:277–284

Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333

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

Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271

Hua J, Chang C, Sun Q, Meyerowitz EM (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269:1712–1714

Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel K-H, Schäfer 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

Jacobs S, Kogel K-H, Schaefer P (2013) Root based innate immunity and its suppression by the mutualistic fungus Piriformospora indica. In: Varma A, Kost G, Oelmueller R (eds) Piriformospora indica—Sebacinales and their biotechnological applications. Springer, Germany, pp 223–238

Jones JD, Dangl JL (2006) The plant immune system. Nature 16:323–329

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

Kost G, Rexer K-H (2013) Morphology and ultrastructure of Piriformospora indica. In: Varma A, Kost G, Oelmueller R (eds) Piriformospora indica—Sebacinales and their biotechnological applications. Springer, Germany, pp 25–36

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

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 Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol Plant Microbe Interact 24:421–431

Liu Y, Schiff M, Dinesh-Kumar SP (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J 38:800–809

Matsushima R, Hayashi Y, Kondo M, Shimada T, Nishimura M, Hara-Nishimura I (2002) An endoplasmic reticulum-derived structure that is induced under stress conditions in Arabidopsis. Plant Physiol 130:1807–1814

Miya A, Albert P, Shiny T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 104:19613–19618

Nagano AJ, Matsushima R, Hara-Nishimura I (2005) Activation of an ER-body-localized β-glucosidasevia a cytosolic binding partner in damaged tissues of Arabidopsis thaliana. Plant Cell Physiol 46:1140–1148

Nitz I, Berkefeld H, Puzio PS, Grundler FMW (1999) Pyk10, a seedling and root specific gene and promoter from Arabidopsis thaliana. Plant Sci 161:337–346

Oelmueller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica: a novel multifunctional symbiotic fungus. Symbiosis 49:1–18

Pedersen BP, Kumar H, Waight AB, Risenmay AJ, Roe-Zurz Z, Chau BH, Schlessinger A, Bonomi M, Harries W, Sali A, Johri AK, Stroud RM (2013) Crystal structure of a eukaryotic phosphate transporter. Nature. doi: 10.1038/nature12042

Pham GH, Kumari R, Singh A, Malla R, Prasad R, Sachdev M, Kaldorf M, Buscot F, Oelmüller R, Hampp R, Saxena AK, Rexer K-H, Kost G, Varma A (2004) Axenic cultures of Piriformospora indica. In: Plant surface microbiology. Springer-Verlag, Germany, pp 593–613

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

Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861

Sakai H, Hua J, Chen G, Chang C, Medrano LJ, Blecker AB, Meyerowitz EM (1998) ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proc Natl Acad Sci U S A 95:5812–5817

Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, Scholz U, Kühnemann JP, Sonnewald S, Sonnewald U, Kogel KH (2009) Phytohormones in plant root-Piriformospora indica mutualism. Plant Signal Behav 4:669–671

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

Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmuller 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

Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM, Nitz I, Varma A, Grundler FM, Oelmüller R (2008) PYK10, a β-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 50:1–17

Sirrenberg A, Goebel 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 Plant 131:581–589

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

Sun C, Michal Johnson J, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers 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

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 Arabidopsis is sensitive to high auxin levels, requires trans-cytokinin biosynthesis and the cytokinin receptor combination CRE1/AHK2. Mol Plant Microbe Interact 21:1371–1383

Varma A, Verma S, Sudha N, Sahay S, Butehorn B, Franken P (1999) Piriformospora indica, a cultivable plant growth promoting root endophyte. Appl Environ Microbiol 65:2741–2744

Varma A, Singh A, Sudha Sahay N, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D, Bharti K, Franken P, Hurek T, Blechert O, Rexer KH, Kost G, Hahn A, Hock B, Maier W, Walter M, Strack D, Kranner I (2001) Piriformospora indica: an axenically culturable mycorrhiza-like endosymbiotic fungus. In: Hock B (ed) The Mycota IX, Fungal Associations. Springer, Germany, pp 123–150

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

Varma A, Sherameti I, Tripathi S, Prasad R, Das A, Sharma M, Bakshi M, Johnson JM, Bhardwaj S, Arora M, Rastogi K, Agrawal A, Kharakwal AC, Talukdar S, Bagde US, Bisaria VS, Upadhyay CP, Won PS, Chen Y, Ma J, Kumar M, Dua M, Lou B, Adya A, Zhong L, Meghvansi MK, Sree KS, Gosal SK, Srivastava RB, Johri AK, Cruz C, Oelmueller R (2012b) The symbiotic fungus Piriformospora indica: review. In: B Hock (ed) The Mycota IX, Fungal Associations. Springer-Verlag, Germany, Chapter 13, pp 231–254

Varma A, Bajaj R, Agarwal A, Asthana S, Rajpal K, Das A, Prasad R, Kharkwal AC (2013a) Memoirs of ‘Rootonic’—the magic fungus. Amity University Press, India

Varma A, Kost G, Oelmueller R (2013b) Piriformospora indica—sebacinales and their biotechnological applications. Springer, Germany

Verma SA, Varma A, Rexer K-H, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:898–905

Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Von Wettstein D, Franken P, Kogel K-H (2005) The endophytic fungus reprograms barley to salt-stress tolerance, disease resistance and higher yield. Proc Natl Acad Sci U S A 102:13386–13391

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 108:1003–1010

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 285:26532–26544

Yamada K, Hara-Nishimura I, Nishimura M (2011) Unique defense strategy by the endoplasmic reticulum body in plants. Plant Cell Physiol 52:2039–2049

Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou JM (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–185

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 K-H (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7:1–26