Piriformospora indica: A Novel Plant Growth-Promoting Mycorrhizal Fungus

Agricultural Research

Volumn 1, Issue 2, 2012, Pages 117-131

  Varma, Ajit ^a   Bakshi, Madhunita ^a   Lou, Binggan ^b   Hartmann, Anton ^c   Oelmueller, Ralf ^d  

^a AMITY UNIVERSITY   (India)

^b ZHEJIANG UNIVERSITY   (China)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

PGPF; Piriformospora indica; Plant growth promoting mycorrhizal fungus

Indexed keywords

AGRICULTURAL ROBOTS; CELL DEATH; CROPS; METABOLITES; PLANTS (BOTANY);

EARLY-FLOWERING; HORTICULTURAL CROPS; MYCORRHIZAL FUNGUS; PGPF; PIRIFORMOSPORA INDICA; PLANT GROWTH PROMOTING; ROOT COLONIZATION; SECONDARY METABOLITES;

SEED;

COLONIZATION; CROP IMPROVEMENT; CROP PLANT; CROP PRODUCTION; ECOSYSTEM RESPONSE; FUNGUS; GENOME; GROWTH; HORTICULTURE; MYCORRHIZA; ROOT; SECONDARY METABOLITE;

BRYOPHYTES; FUNGI; GYMNOSPERMAE; HEXAPODA; MAGNOLIOPHYTA; PIRIFORMOSPORA INDICA; PTERIDOPHYTA; SEBACINALES;

EID: 84964264015     PISSN: 2249720X     EISSN: 22497218     Source Type: Journal    
DOI: 10.1007/s40003-012-0019-5     Document Type: Review

References (58)

1. Achatz B, Rüden SV, Andrade D, Neumann E, Kühnemann JP, Kogel KH, Philipp F, Waller F (2010) Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil 33: 7-59.
2. Adya AK, Gautam A, Lixing Z, Varma A (2012) Characterisation of Piriformospora indica culture filtrate: protocol. In: Oelmueller R, Tripathy S, Kost G, Varma A (eds) Sebacinales. Springer, Germany, in press.
3. Basiewicz M, Weiss M, Kogel KH, 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.
4. Bagde US, Prasad R, Varma A (2010) Mass cultivation of Piriformospora indica in new Brumswick fermentor and its formulation as biofertilizer. Asian J Microb Biotechnol 12: 911-916.
5. Bagde US, Prasad R, Varma A (2011) Influence of culture filtrate of Piriformospora indica on growth and yield of seed oil in Helianthus annuus. Symbiosis 53: 83-88.
6. 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.
7. Chen XH, Vater J, Piel J, Franke P, Scholz R, Schneider K, Koumoutsi A, Hitzeroth G, Grammel N, Strittmatter AW, Gottschalk G, Süssmuth RD, Borriss R (2007) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB42. J Bacteriol 188: 4024-4036.
8. Chordia P (2011) Salt stress on axenic growth of Piriformospora indica. M. Phil Thesis, Amity University, Uttar Pradesh.
9. Das A, Prasad R, Srivastava A, Pham HG, Bhatnagar K, Varma A (2007) Microbial siderophores. In: Varma A, Chincholkar SB (eds) Fungal siderophores: structure, functions and regulation. Springer, Heidelberg, pp 1-35.
10. Das A, Sheramati I, Varma A (2012) Contaminated soils: physical, chemical and biological components. In: Varma A, Kothe E (eds) Bio-geo interactions in metal-contaminated soils. Springer, Heidelberg, pp 1-16.
11. Das A, Kamal S, Shakil Najam A, Sherameti I, Oelmüller R, Dua M, Tuteja N, Johri Atul K, Varma A (2012) The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii. Plant Signal Behav 7: 1-10.
12. Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Büttner C, Grosch R, Schwarz D, Franken P (2009) Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20: 191-200.
13. Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321: 35-59.
14. Fuchs R, Budzikiewicz H (2000) Structural studies of pyoverdines with cyclopeptidic substructures by electrospray ionization and collision induced fragmentation. Spectroscopy 14: 229-246.
15. Fuchs R, Budzikiewicz H (2001) Structural studies of pyoverdines by mass spectrometry. Curr Org Chem 5: 265-288.
16. Goltapeh ME, Danesh YR (2006) Pathogenic interactions between Trichoderma species and Agaricus bisporus. J Agric Technol 2: 29-37.
17. Gosal SK, Karlupia A, Gosal SS, Chhibba IM, Varma A (2010) Biotization with Piriformospora indica and Pseudomonas fluorescens improves survival rate, nutrient acquisition, field performance and saponin content of micropropagated Chlorophytum sp. Indian J Biotechnol 9: 289-297.
18. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch HT, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüßler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao Y-J, Zhang N (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111: 509-547.
19. Hill TW, Käfer E (2001) Improved protocols for aspergillus medium: trace elements and minimum medium salt stock solutions. Fungal Genet News Lett 48: 20-21.
20. Jha B, Thakur MC, Gontia I, Albrecht V, Stoffels M, Schmid M, Hartmann A (2009) Isolation, partial identification and application of diazotrophic rhizobacteria from traditional Indian rice cultivars. Eur J Soil Biol 45: 62-72.
21. Johnson JM, Sherameti I, Ludwig A, Nongbri PL, Sun C, Lou B, Varma A, Oelmüller R (2011) Protocols for Arabidopsis thaliana and Piriformospora indica co-cultivation-a model system to study plant beneficial traits. J Endocytobiosis Cell Res 101-113.
22. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298.
23. Koumoutsi A, Chen X-H, Vater J, Borriss R (2007) DegU and YczE positively regulate the synthesis of Bacillomycin D by Bacillus amyloliquefaciens strain FZB42. Appl Environ Microbiol 73: 6953-6964.
24. Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155: 780-790.
25. Kumar M, Sharma R, Jogawat A, Singh P, Dua M, Gill SS, Trivedi DK, Tuteja N, Varma AK, Oelmueller R, Johri AK (2012) Piriformospora indica, a root endophytic fungus, enhances abiotic stress tolerance of the host plant. In: Tuteja N, Gill SS, Tiburcio AF, Tuteja R (eds) Improving crop resistance to abiotic stress. Wiley-Blackwell, Weinheim, pp 543-548.
26. Murugan P (2011) Enhancing winter vegetable production in greenhouse of cold arid desert of Ladakh by inoculation of Piriformospora indica. DRDO Technology Spectrum, pp 164-170.
27. Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49: 1-17.
28. Peškan-Berghöfer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanked 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 Plant 122: 465-477.
29. Pham GH, Kumari R, Singh A, Sachdev M, Prasad R, Kaldorf M et al (2004) Axenic cultures of Piriformospora indica. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Germany, pp 593-616.
30. Pham HG, Kumari R, Singh A, Malla R, Prasad R, Sachdev M, Kaldorf M, Buscot F, Oelmueller R, Hampp R, Saxena AK, Rexer K-H, Kost G, Varma A (2004) Axenic cultures of Piriformospora indica. In: Varma A, Abbott LK, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Germany, pp 593-613.
31. Prasad RP (2008) Studies on interaction between symbiotic fungus (Piriformospora indica), rhizobacteria and selected plants. PhD Thesis, Merrut University, India.
32. Prasad RP, Bagde US, Pushpangadan P, Varma A (2008) Bacopa monniera L. Pharmological aspects and case study involving P. indica. Int J Integr Biol 3: 100-110.
33. Qiang X, Weiss M, Kogel KH, Schäfer P (2012) Piriformospora indica-a mutualistic basidiomycete with an exceptionally large plant host range. Mol Plant Pathol. doi: 10. 1111/J. 1364-3703. 2011. 00764. X.
34. Raajimakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere. A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321: 341-361.
35. Sahay NS, Varma A (1999) Piriformospora indica: a new biological hardening tool for micropropagated plants. FEMS Microbiol Lett 181: 297-302.
36. Sarma MVRK, Kumar V, Saharan K, Srivastava R, Sharma AK, Prakash A, Sahai V, Bisaria VS (2011) Application of inorganic carrier-based formulations of fluorescent pseudomonads and Piriformospora indica on tomato plants and evaluation of their efficacy. J Appl Microbiol 111: 456-466.
37. 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.
38. 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.
39. 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: 26241-26247.
40. 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 21: 799-807.
41. 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 endoplasmic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 54: 428-439.
42. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
43. Strasser RJ, Tsimilli-Michael M, Dangre D, Rai M (2007) Biophysical phenomics reveals functional building blocks of plant system biology: a case study for the evaluation of the impact of mycorrhization with Piriformospora Indica. In: Varma, Oelmueller (eds) Advanced techniques in soil microbiology. Springer, Heidelberg, pp 319-338.
44. Sun C, Johnson JM, 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.
45. Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novak O, Strnad M, Ludwig-Muller J, Oelmüller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe 21: 1371-1383.
46. Vadassery J, Ranf S, Drzewiecki C, Mithöfer A, Mazars C, Scheel D, Lee J, Oelmüller R (2009) A cell wall extract from Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59: 193-206.
47. Vadassery J, Tripathi S, Prasad R, Varma A, Oelmüller R (2009) Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J Plant Physiol 166: 1263-1274.
48. Varma A, Verma S, Sudha, Sahay N, Buttehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65: 2741-2744.
49. Varma A, Singh A, Sudha M, Sahay NS, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D, Bharti K, Hurek T, Blechert O, Rexer KH, Kost G, Hahn A, Maier W, Walter M, Strack D, Kranner I (2001) Piriformospora indica: a cultivable mycorrhiza-like endosymbiotic fungus. In: Hock B (ed) The Mycota IX. Springer-Verlag, Berlin, Germany, pp 125-150.
50. Varma A, Tripathi S, Prasad R, Das A, Sharma M, Bakshi M, Arora M, Rastogi K, Agrawal A, Kharkwal AC, Tsimilli-Michael M, Strasser RJ, Bagde US, Bisaria VS, Upadhyaya CP, Malla R, Kost G, Joy K, Sherameti I, Chen Y, Ma J, Lou B, Oelmüller R (2012) The symbiotic fungus Piriformospora indica: update. In: Hock B (ed) The Mycota XXL. Springer, Berlin, in press.
51. Varma A, Fekete A, Srivastava A, Saxena AK, Frommberger M, Li D, Gschwendter S, Sheramati I, Oelmueller R, Kopplin PS, Tripathi S, Hartmann A (2012) Inhibitory interactions of rhizobacteria with the symbiotic fungus Piriformospora indica. In: Varma A, Oelmueller R (eds) Sebacinales. Springer, Berlin, in press.
52. Verma S, Varma A, Rexer K, 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: 896-903.
53. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D et al (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.
54. 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.
55. Weiss M, Sýkorová 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.
56. 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.
57. 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.
58. Zuccaro A, Lahrmann U, Ldener UG, 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.