Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens

Mycorrhiza

Volumn 20, Issue 3, 2010, Pages 191-200

  Fakhro, Ahmad ^a,b   Andrade Linares, Diana Rocío ^a   von Bargen, Susanne ^b   Bandte, Martina ^b   Büttner, Carmen ^b   Grosch, Rita ^a   Schwarz, Dietmar ^a   Franken, Philipp ^a  

^a LEIBNIZ INSTITUTE OF VEGETABLE AND ORNAMENTAL CROPS   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Hydroponic cultures; Lycopersicon esculentum; Pepino mosaic virus; Verticillium dahliae

Indexed keywords

DISEASE SEVERITY; ENDOPHYTE; EXPERIMENTAL STUDY; FRUIT PRODUCTION; FUNGUS; GROWTH RATE; HYDROPONICS; INOCULATION; LIGHT INTENSITY; PATHOGEN; ROOT COLONIZATION; VIRUS;

ARTICLE; BASIDIOMYCETES; BIOMASS; EUROPE; FRUIT; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOGENICITY; PLANT; PLANT DISEASE; POTEXVIRUS; TOMATO; VIROLOGY;

BASIDIOMYCOTA; BIOMASS; EUROPE; FRUIT; LYCOPERSICON ESCULENTUM; PLANT DISEASES; PLANT SHOOTS; POTEXVIRUS;

ARABIDOPSIS; FUNGI; HORDEUM; LYCOPERSICON ESCULENTUM; PEPINO MOSAIC VIRUS; PIRIFORMOSPORA INDICA; TRITICUM AESTIVUM; VERTICILLIUM DAHLIAE;

EID: 77349097766     PISSN: 09406360     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00572-009-0279-5     Document Type: Article

References (58)

1. Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180: 501-510.
2. 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.
3. Barazani O, Von Dahl CC, Baldwin IT (2007) Sebacina vermifera promotes the growth and fitness of Nicotiana attenuata by inhibiting ethylene signaling. Plant Physiol 144: 1223-1232.
4. Chen P, Lee B, Robb J (2004) Tolerance to a non-host isolate of Verticillium dahliae in tomato. Physiol Mol Plant Pathol 64: 283-291.
5. Clark MF, Adams AN (1977) Characteristics of microplate method of enzyme-linked immunosorbent assay for detection of plant viruses. J Gen Virol 34: 475-483.
6. Cordoba-Selles MC, García-Rández A, Alfaro-Fernández A, Jordá-Gutiérrez C (2007) Seed transmission of Pepino mosaic virus and efficacy of tomato seed disinfection treatments. Plant Dis 91: 1250-1254.
7. De Kreij C, Voogt W, van den Bos AL, Baas R (1997) Voedingsoplossingen voor de teelt van tomaat in gesloten teeltsystemen. Brochure VG Tomaat, The Netherlands.
8. Dehne HW (1982) Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72: 1115-1119.
9. Deshmukh SD, Kogel KH (2007) Piriformospora indica protects barley from root rot caused by Fusarium graminearum. J Plant Dis Prot 114: 263-268.
10. Deshmukh SD, Hueckelhoven R, Schaefer 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.
11. Dobinson KF, Tenuta GK, Lazarovits G (1996) Occurrence of race 2 of Verticillium dahliae in processing tomato fields in southwestern Ontario. Can J Plant Pathol 18: 55-58.
12. Drüge U, Baltruschat H, Franken P (2007) Piriformospora indica promotes adventitious root formation in cuttings. Sci Hortic 112: 422-426.
13. Feller C, Bleiholder H, Buhr L, Hack H, Hess M, Klose R, Meier U, Stauss R, van den Boom T, Weber E (1995) Phänologische Entwicklungsstadien von Gemüsepflanzen: II. Fruchtgemüse und Hülsenfrüchte. Nachr bl Dtsch Pflanzenschutzd 47: 217-232.
14. Franken P, Requena N, Bütehorn B, Krajinski F, Kuhn G, Lapopin L, Mann P, Rhody D, Stommel M (2000) Molecular analysis of the arbuscular mycorrhiza symbiosis. Arch Agron Soil Sci 45: 271-286.
15. French CJ, Dubeau C, Bunckle A, Ferguson G, Haesevoets R, Bouthillier M, Bernardy MG (2008) Overview of Pepino mosaic virus research. Can J Plant Pathol 30: 373-374.
16. Gold J, Lee B, Robb J (1996) Colonization of tomatoes by Verticillium dahliae: determinative phase II. Can J Bot 74: 1279-1288.
17. Hanssen IM, Paeleman A, Vandewoestijne E, van Bergen L, Bragard C, Lievens B, Vanachter ACRC, Thomma BPHJ (2009) Pepino mosaic virus isolates and differential symptomatology in tomato. Plant Pathol 58: 450-460.
18. Harrington MA, Dobinson KF (2000) Influences of cropping practices on Verticillium dahliae populations in commercial processing tomato fields in Ontario. Phytopathology 90: 1017.
19. Huisman OC, Ashworth LJ Jr (1976) Influence of crop rotation on survival of Verticillium albo-atrum in soils. Phytopathology 66: 978-981.
20. Jetiyanon K, Kloepper JW (2002) Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol Control 24: 285-291.
21. Jones RAC, Koenig R, Lesemann DE (1980) Pepino mosaic virus, a new potexvirus from pepino (Solanum muricatum). Ann Appl Biol 94: 61-68.
22. Jordá C, Lázaro Pérez A, Martínez-Culebras PV (2001) First report of Pepino mosaic virus on natural hosts. Plant Dis Notes 85: 1292.
23. 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.
24. Ligoxigakis EK, Vakalounakis DJ (1994) The incidence and distribution of races of Verticillium dahliae in Crete. Plant Pathol 43: 755-758.
25. Mansoori B, Milton JM, Smith CJ (1995) Isolation and partial purification of a phytotoxin related to pathogenic Verticillium species. J Phytopathol 143: 33-36.
26. Pegg GF (1974) Verticillium diseases. Rev Plant Pathol 53: 157-182.
27. Pegg GF, Brady BL (2002) Verticillium wilts. Oxford, UK.
28. Peskan-Berghöfer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, Oelmuller 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. Rai M, Acharya D, Singh A, Varma A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11: 123-128.
30. Raupach GS, Liu L, Murphy JF, Tuzun S, Kloepper JW (1996) Induced systemic resistance in cucumber and tomato against Cucumber mosaic cucumovirus using plant growth-promoting rhizobacteria (PGPR). Plant Dis 80: 891-894.
31. Sahay N, Varma A (1999) Piriformospora indica, a new biological hardening tool for micropropagated plants. FEMS Letters 181: 297-302.
32. Savvas D (2003) Hydroponics: a modern technology supporting the application of integrated crop management in greenhouse. J Food Agric Environ 1: 80-86.
33. Schwarz D, Beuch U, Fakhro A, Bandte M, Büttner C, Obermeier C (2009) Spread and interaction of Pepino mosaic virus (PepMV) and Pythium aphanidermatum in a closed nutrient solution recirculation system: effects on tomato growth and yield. Plant Pathol, accepted.
34. 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.
35. Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97: 523-531.
36. Shahollari B, Varma A, Oelmuller 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.
37. Shahollari B, Vadassery J, Varma A, Oelmuller 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.
38. Sharma M, Schmid M, Rothballer M, Hause G, Zuccaro A, Imani J, Kampfer P, Domann E, Schäfer P, Hartmann A, Kogel KH (2008) Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiol 10: 2235-2246.
39. Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves. Mol Plant Microbe Interact 12: 1000-1007.
40. 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.
41. Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM, Nitz I, Varma A, Grundler FM, Oelmuller R (2008) PYK10, a beta-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.
42. Shittu HO, Castroverde DCM, Nazar RN, Robb J (2009) Plant-endophyte interplay protects tomato against a virulent Verticillium. Planta 229: 415-426.
43. Sinha AK, Wood RKS (1968) Studies on nature of resistance in tomato plants to Verticillium albo-artrum. Ann Appl Biol 62: 319-327.
44. 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.
45. Soler-Aleixandre S, Lopez C, Diez MJ, de Castro AP, Nuez F (2005) Association of Pepino mosaic virus with tomato collapse. J Phytopathol 153: 464-469.
46. Spence NJ, Basham J, Mumford RA, Hayman G, Edmondson R, Jones DR (2006) Effect of Pepino mosaic virus on the yield and quality of glasshouse-grown tomatoes in the UK. Plant Pathol 55: 595-606.
47. Stanghellini ME, Rasmussen SL (1994) Hydroponics-a solution for zoosporic pathogens. Plant Dis 78: 1129-1138.
48. 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.
49. Talboys PW (1984) Chemical control of verticillium wilts. Phytopathol Mediterr 23: 163-175.
50. Ton J, van Pelt JA, van Loon LC, Pieterse CMJ (2002) Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol Plant Microbe Interact 15: 27-34.
51. Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novak O, Strnad M, Ludwig-Muller J, Oelmuller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe Interact 21: 1371-1383.
52. van der Vlugt RAA, Cuperus C, Vimk J, Stijger CCMM, Naaldwijk AA, Lesemann DE, Verhoeven JTJ, Roenhorst JW (2002) Identification and characterization of Pepino mosaic potexvirus in tomato. EPPO Bull 32: 503-508.
53. van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103: 753-765.
54. Varma A, Verma S, Sudah SN, Franken P (1999) Piriformospora indica, a cultivable plant growth-promoting root endophyte. Appl Environ Microbiol 65: 2741-2744.
55. Verma S, Varma A, Rexer K-H, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. nov. sp. nov., a new root-colonizing fungus. Mycologia 90: 896-903.
56. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102: 13386-13391.
57. 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.
58. 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.