Abstract
The basidiomycete fungus Piriformospora indica colonizes roots of a broad range of mono- and dicotyledonous plants. It confers enhanced growth, improves resistance against biotic and tolerance to abiotic stress, and enhances grain yield in barley. To analyze mechanisms underlying P. indica-induced improved grain yield in a crop plant, the influence of different soil nutrient levels and enhanced biotic stress were tested under outdoor conditions. Higher grain yield was induced by the fungus independent of different phosphate and nitrogen fertilization levels. In plants challenged with the root rot-causing fungus Fusarium graminearum, P. indica was able to induce a similar magnitude of yield increase as in unchallenged plants. In contrast to the arbuscular mycorrhiza fungus Glomus mosseae, total phosphate contents of host plant roots and shoots were not significantly affected by P. indica. On the other hand, barley plants colonised with the endophyte developed faster, and were characterized by a higher photosynthetic activity at low light intensities. Together with the increased root formation early in development these factors contribute to faster development of ears as well as the production of more tillers per plant. The results indicate that the positive effect of P. indica on grain yield is due to accelerated growth of barley plants early in development, while improved phosphate supply—a central mechanism of host plant fortification by arbuscular mycorrhizal fungi—was not observed in the P. indica-barley symbiosis.
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References
Achatz B (2006) Untersuchungen zum Einfluss des Wurzelendophyten Piriformospora indica auf das Wachstum von Hordeum vulgare, die Resistenz gegen Blumeria graminis f.sp. hordei und die Genexpression in den Blättern. Philipps-University Marburg, Germany, PhD thesis. http://archiv.ub.uni-marburg.de/diss/z2006/0415
Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel K-H, 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 180:501–10
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
Borgmann F (2000) Ertragsbildung der Kulturpflanzen. In: Entrup NL, Oehmichen J (eds) Lehrbuch des Pflanzenbaus. Verlag Thomas Mann, Gelsenkirchen, pp 337–355
Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82:3057–3068
Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26
Bütehorn B, Rhody D, Franken P (2000) Isolation and characterisation of Pitef1 encoding the translation elongation factor EF-1α of the root Endophyte Piriformospora indica. Plant Biol 2:687–692
Caravaca F, Diaz E, Barea JM, Azcón-Aguilar C, Roldán A (2003) Photosynthetic and transpiration rates of Olea europaea subsp. sylvestris and Rhamnus lycioides as affected by water deficit and mycorrhiza. Biol Plant 46:637–639
Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant-Microbe Interact 11:1017–1028
Dehne HW (1982) Interactions between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathol 72:1115–1119
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
Deshmukh S, Kogel KH (2007) Piriformospora indica protects barley from root rot caused by Fusarium graminearum. J Plant Dis Prot 114:263–268
Druege U, Baltruschat H, Franken P (2007) Piriformospora indica promotes adventitious root formation in cuttings. Scient Horticult 112:422–426
Fay P, Mitchell DT, Osborne BA (1996) Photosynthesis and nutrient-use efficiency of barley in response to low arbuscular mycorrhizal colonization and addition of phosphorus. New Phytol 132:425–433
Gericke S, Kurmies B (1952) Colorimetrische Bestimmung der Phosphorsäure mit Vanadat-Molybdat (Vm-Methode). Fresenius Z f Anal Chem 137:15–22
Gernns H, von Alten H, Poehling HM (2001) Arbuscular mycorrhiza increased the activity of a biotrophic leaf pathogen—is a compensation possible? Mycorrhiza 11:237–243
Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698
Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823
Harrison MJ (2005) Signalling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42
Humbeck K, Kloppstech K, Krupinska K (1994) Expression of early light-inducible proteins in flag leaves of field-grown barley. Plant Physiol 105:1217–1222
Karandashov V, Nagy R, Wegmüller S, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 101:6285–6290
Kormanik PP, McGraw AC (1982) In: Schenck NC (ed) Methods and principles of mycorrhizal research. Am. Phytopathol. Soc., St. Paul, pp 37–45
Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant and Soil 159:89–102
Mathur N, Vyas A (1995) Influence of VA mycorrhizae on net photosynthesis and transpiration of Ziziphus mauritiana. J Plant Physiol 147:328–330
Newman EI, Reddell P (1987) The distribution of mycorrhizas among families of vascular plants. New Phytol 106:745–751
Paradi I, Bratek Z, Lang F (2003) Influence of arbuscular mycorrhiza and phosphorus supply on polyamine content, growth and photosynthesis of Plantago lanceolata. Biol Plantarum 46:563–569
Peskan-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 Plant 122:465–477
Pham GH, Kumari R, Singh A, Malla R, Prasad R, Sachdev M, Kaldorf M, Buscot F, Oelmüller R, Hampp R, Saxena AK, Rexer KH, Kost G, Varma A (2004) Axenic Culture of Symbiotic Fungus Piriformospora indica. In: Varma A, Abbot L, Werner D, Hampp R (eds) Plant Surface Microbiology. Springer-Verlag Berlin, Heidelberg, pp 593–612
Phillips JM, Hayman DS (1970) Improved procedure for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transact Brit Mycol Soc 55:158–161
Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534
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
Reinhardt D (2007) Programming good relations—development of the arbuscular mycorrhizal symbiosis. Curr Op Plant Biol 10:98–105
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
Selosse MA, Le Tacon F (1998) The land flora—a phototroph-fungus partnership. Trends Ecol Evol 13:15–20
Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathol 97:523–531
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
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
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London
Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d'un système radiculaire. Recherche de méthodes d'estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221
Varma A, Verma S, Sudah SN, Franken P (1999) Piriformospora indica, a cultivable plant growth-promoting root endophyte. Appl & Environ Microbiol 65:2741–2744
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
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 indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391
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
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
Wright DP, Scholes JD, Read DJ (1998) Effects of VA mycorrhizal colonisation on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21:209–216
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421
Acknowledgements
We thank D. Biedenkopf and C. Neumann for excellent technical assistance, S. Deshmukh, M. Sharma and H. Baltruschat for providing unpublished HvPht1;8 expression results and two anonymous reviewers for helpful comments. We are grateful for support with photosynthesis measurements by H.-W. Koyro and for support by M. Kolmer at the experimental station Rauischholzhausen. DA was supported by the German Academic Exchange Service (DAAD). This work was supported by Deutsche Forschungsgemeinschaft (DFG) grant FOR666 to KHK and FW.
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Achatz, B., von Rüden, S., Andrade, D. et al. Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil 333, 59–70 (2010). https://doi.org/10.1007/s11104-010-0319-0
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DOI: https://doi.org/10.1007/s11104-010-0319-0