The root endophytes Trametes versicolor and Piriformospora indica increase grain yield and P content in wheat

  • Meysam Taghinasab
  • Jafargholi Imani
  • Diedrich Steffens
  • Stefanie P. Glaeser
  • Karl-Heinz Kogel
Regular Article

Abstract

Background and Aims

Soil phosphorus (P) deficiency occurs in many developing and transition countries. One method of resolving soil P deficiency is a strong application of mineral and organic fertilizers in order to saturate the P binding capacity of soil. Another promising method is the implementation of crop-endophyte symbioses in combination with the application of smaller amount of P fertilizer. This study comparatively examined the effect of the fungal endophytes Trametes versicolor and Piriformospora indica in P-deprived and P-rich conditions on P uptake and yield in wheat (Triticum aestivum L., cv. Bobwhite).

Methods

Three-day-old wheat seedlings were dip-inoculated with mycelia of (a) T. versicolor WC16GW axenically isolated from Galium album, a dicotyledonous plant obtained from grassland in Linden near Giessen, Germany, and (b) axenic cultures of P. indica DSM 11827 freshly re-isolated from surface-sterilized barley roots. Seedlings were subsequently grown in 6 l Mitscherlich pots (eight seedlings per pot) in soil containing mono-calcium phosphate [CP, Ca (H2PO4)2] with 100 mg P kg−1 soil and control (CO) with 6.3 mg CAL-P kg−1 soil P in an open-air pot experiment station for three months.

Results

Colonization of wheat roots by T. versicolor and P. indica increased plant biomass, yield and P content. T. versicolor-colonized plants exhibited a significant increase in grain yield of 37% (CO treatment) and 8.5% (CP treatment), as well as straw yield of 27% (CO treatment) as compared to non-colonized plants. P. indica-colonized plants showed a significant increase in grain yield of 10% under high P (CP treatment) and straw yield of 22% (CO treatment). Moreover, P. indica improved grain P content by 30% (CO treatment), 16% (CP treatment) and straw P content by 33% (CO treatment), while T. versicolor increased grain P content by 16% (CP treatment) and straw by 35% (CP treatment).

Conclusions

Both T. versicolor and P. indica improved wheat P uptake in both P-deprived and P-rich conditions. T. versicolor supported a high grain yield under the CO and CP treatments, suggesting this fungus has a promising potential for P management in cereal crops.

Keywords

Root endophyte Piriformospora indica Trametes versicolor Phosphate Yield parameters 

Abbreviations

P

Phosphorus

RP

Rock phosphate

CP

Mono-calcium phosphate

CO

Control

Notes

Acknowledgements

We are grateful to Ute Micknass, Christina Birkenstock and Lutz Wilming for technical assistance. This research was supported in the project “PrimedPlant” by the German Ministry of Education and Research (BMBF) to K.H.K. We are very grateful to Prof. Dr. Phil Lane, Institute of Phytopathology, Justus Liebig University Giessen, for many excellent advises and comments.

References

  1. Achatz B, Kogel K-H, Franken P, Waller F (2010) Piriformospora indica mycorrhization increases grain yield by accelerating early development of barley plants. Plant Signal Behav 5:1685–1687.  https://doi.org/10.4161/psb.5.12.14112 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Achatz B, von Rüden S, Andrade D, Neumann E, Pons-Kühnemann J, Kogel K-H, Franken P, Waller F (2010) Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil 333:59–70.  https://doi.org/10.1007/s11104-010-0319-0 CrossRefGoogle Scholar
  3. Akhtar MS, Oki Y, Adachi T (2009) Mobilization and acquisition of sparingly soluble P-sources by Brassica cultivars under P-starved environment I. differential growth response, P-efficiency characteristics and P-remobilization. J Integ Plant Biol 51:1008–1023.  https://doi.org/10.1111/j.1744-7909.2009.00874.x CrossRefGoogle Scholar
  4. Badotti F, de Oliveira FS, Garcia CF, Vaz ABM, Fonseca PLC, Nahum LA, Oliveira G, Góes-Neto A (2017) Effectiveness of ITS and sub-regions as DNA barcode markers for the identification of Basidiomycota (Fungi). BMC Microbiol 17:42.  https://doi.org/10.1186/s12866-017-0958-x CrossRefPubMedPubMedCentralGoogle Scholar
  5. Balzergue C, Chabaud M, Barker DG, Bécard G, Rochange SF (2013) High phosphate reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting root calcium spiking responses to the fungus. Front Plant Sci 4:426CrossRefPubMedPubMedCentralGoogle Scholar
  6. Behie SW, Padilla-Guerrero IE, Bidochka MJ (2013) Nutrient transfer to plants by phylogenetically diverse fungi suggests convergent evolutionary strategies in rhizospheric symbionts. Commun Integr Biol 6:e22321.  https://doi.org/10.4161/cib.22321 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017.  https://doi.org/10.1111/j.1365-313X.2010.04385.x CrossRefPubMedGoogle Scholar
  8. Cheplick GP (2008) Host genotype overrides fungal endophyte infection in influencing tiller and spike production of Lolium perenne (Poaceae) in a common garden experiment. Am J Bot 95:1063–1071.  https://doi.org/10.3732/ajb.0800042 CrossRefPubMedGoogle Scholar
  9. Comby M, Lacoste S, Baillieul F, Profizi C, Dupont J (2016) Spatial and temporal variation of cultivable communities of co-occurring endophytes and pathogens in wheat. Front Microbiol 7:403.  https://doi.org/10.3389/fmicb.2016.00403 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Corradi N, Bonfante P (2012) The arbuscular mycorrhizal symbiosis: origin and evolution of a beneficial plant infection. PLoS Pathog 8:e1002600.  https://doi.org/10.1371/journal.ppat.1002600 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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 Nat Acad Sci USA 103:18450–18457CrossRefPubMedPubMedCentralGoogle Scholar
  12. Ding N, Guo H, Kupper J, McNear D (2016) Shoot specific fungal endophytes alter soil phosphorus (P) fractions and potential acid phosphatase activity but do not increase P uptake in tall fescue. Plant Soil 401:291–305.  https://doi.org/10.1007/s11104-015-2757-1 CrossRefGoogle Scholar
  13. Fidelibus MW, Martin CA, Stutz JC (2001) Geographic isolates of Glomus increase root growth and whole-plant transpiration of citrus seedlings grown with high phosphorus. Mycorrhiza 10:231–236.  https://doi.org/10.1007/s005720000084 CrossRefGoogle Scholar
  14. Franken P (2012) The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl Microbiol Biotechnol 96:1455–1464.  https://doi.org/10.1007/s00253-012-4506-1 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gan H, Churchill ACL, Wickings K (2017) Invisible but consequential: root endophytic fungi have variable effects on belowground plant–insect interactions. Ecosphere 8:e01710-n/a.  https://doi.org/10.1002/ecs2.1710 CrossRefGoogle Scholar
  16. Gerike S, Kurmies B (1952) Die colorimetrische Phosphorsäurebestimmung mit Ammonium-Vandat-Molybdat und ihre Anwendung in der Pflanzenanalyse. Z Pflanzenernähr Bodenkd 104:235–247Google Scholar
  17. Gerke J (2015) Phytate (inositol Hexakisphosphate) in soil and phosphate acquisition from inositol phosphates by higher plants. A Review. Plants 4:253–266.  https://doi.org/10.3390/plants4020253 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Grace EJ, Cotsaftis O, Tester M, Smith FA, Smith SE (2009) Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytol 181:938–949CrossRefPubMedGoogle Scholar
  19. Grant CA, Flaten DN, Tomasiewicz DJ, Sheppard SC (2001) The importance of early season phosphorus nutrition. Can J Plant Sci 81:211–224.  https://doi.org/10.4141/p00-093 CrossRefGoogle Scholar
  20. Guo H, Glaeser SP, Alabid I, Imani J, Haghighi H, Kampfer P, Kogel KH (2017) The abundance of endofungal bacterium Rhizobium radiobacter (syn. Agrobacterium tumefaciens) increases in its fungal host Piriformospora indica during the tripartite sebacinalean symbiosis with higher plants. Front Microbiol 8:629.  https://doi.org/10.3389/fmicb.2017.00629 PubMedPubMedCentralGoogle Scholar
  21. Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev: MMBR 79:293–320CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195.  https://doi.org/10.1023/a:1013351617532 CrossRefGoogle Scholar
  23. Hiscox J, Savoury M, Muller CT, Lindahl BD, Rogers HJ, Boddy L (2015) Priority effects during fungal community establishment in beech wood. Isme J 9:2246–2260.  https://doi.org/10.1038/ismej.2015.38 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Ijdo M, Cranenbrouck S, Declerck S (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza 21:1–16.  https://doi.org/10.1007/s00572-010-0337-z CrossRefPubMedGoogle Scholar
  25. Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel KH, Schäfer P (2011) Broad spectrum suppression of innate immunity is required for colonization of Arabidopsis thaliana roots by the fungus Piriformospora indica. Plant Physiol 156:726–740CrossRefPubMedPubMedCentralGoogle Scholar
  26. Jiang H, Zhang J, Han Z, Yang J, Ge C, Wu Q (2017) Revealing new insights into different phosphorus-starving responses between two maize (Zea mays) inbred lines by transcriptomic and proteomic studies. Sci Rep 7:44294.  https://doi.org/10.1038/srep44294 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Johri AK, Oelmüller R, Dua M, Yadav V, Kumar M, Tuteja N, Varma A, Bonfante P, Persson BL, Stroud RM (2015) Fungal association and utilization of phosphate by plants: success, limitations, and future prospects. Front Microbiol 6:984.  https://doi.org/10.3389/fmicb.2015.00984 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kammann C, Müller C, Grünhage L, Jäger H-J (2008) Elevated CO2 stimulates N2O emissions in permanent grassland. Soil Biol Biochem 40:2194–2205.  https://doi.org/10.1016/j.soilbio.2008.04.012 CrossRefGoogle Scholar
  29. Kim SJ, Eo J-K, Lee E-H, Park H, Eom A-H (2017) Effects of Arbuscular Mycorrhizal fungi and soil conditions on crop plant growth. Mycobiology 45:20–24.  https://doi.org/10.5941/myco.2017 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kogel K-H, Franken P, Hückelhoven R (2006) Endophyte or parasite – what decides? Curr Opin Plant Biol 9(358):363Google Scholar
  31. Kohler A, Kuo A, Nagy LG et al (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47:410–415.  https://doi.org/10.1038/ng.3223 CrossRefPubMedGoogle Scholar
  32. Kumar M, Yadav V, Kumar H, Sharma R, Singh A, Tuteja N, Johri AK (2011) Piriformospora indica enhances plant growth by transferring phosphate. Plant Signal Behav 6:723–725CrossRefPubMedPubMedCentralGoogle Scholar
  33. Liu W, Zhang Y, Jiang S, Deng Y, Christie P, Murray PJ, Li X, Zhang J (2016) Arbuscular mycorrhizal fungi in soil and roots respond differently to phosphorus inputs in an intensively managed calcareous agricultural soil. Sci Rep 6:24902.  https://doi.org/10.1038/srep24902; https://www.nature.com/articles/srep24902#supplementary-information
  34. López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123.  https://doi.org/10.1146/annurev-arplant-050213-035949 CrossRefPubMedGoogle Scholar
  35. Mäder P, Edenhofer S, Boller T, Wiemken A, Niggli U (2000) Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol Fertil Soils 31:150–156.  https://doi.org/10.1007/s003740050638 CrossRefGoogle Scholar
  36. Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189.  https://doi.org/10.3114/sim.53.1.173 CrossRefGoogle Scholar
  37. Mehra P, Pandey BK, Giri J (2017) Improvement in phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnol J 15:1054–1067.  https://doi.org/10.1111/pbi.12699 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Meyberg M (1988) Selective staining of fungal hyphae in parasitic and symbiotic plant-fungus associations. For Hist 88:197–199Google Scholar
  39. Mongon J, Chaiwong N, Bouain N, Prom UTC, Secco D, Rouached H (2017) Phosphorus and iron deficiencies influences rice shoot growth in an oxygen dependent manner: insight from upland and lowland rice. Int J Mol Sci 18.  https://doi.org/10.3390/ijms18030607
  40. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ngwene B, Boukail S, Söllner L, Franken P, Andrade-Linares DR (2016) Phosphate utilization by the fungal root endophyte Piriformospora indica. Plant Soil 405:231–241.  https://doi.org/10.1007/s11104-015-2779-8 CrossRefGoogle Scholar
  42. Ortiz R, Navarrete J, Oviedo C, Parraga M, Carrasco I, de la Vega E, Ortiz M, Blanchette RA (2013) White rot Basidiomycetes isolated from Chiloe National Park in Los Lagos region, Chile. Antonie Van Leeuwenhoek 104:1193–1203.  https://doi.org/10.1007/s10482-013-0041-z CrossRefPubMedGoogle Scholar
  43. 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 496:533–536.  https://doi.org/10.1038/nature12042 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Wees SCMV, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375.  https://doi.org/10.1146/annurev-phyto-082712-102340 CrossRefPubMedGoogle Scholar
  45. Porras-Alfaro A, Bayman P (2011) Hidden Fungi, emergent properties: Endophytes and Microbiomes. Annu Rev Phytopathol 49:291–315.  https://doi.org/10.1146/annurev-phyto-080508-081831 CrossRefPubMedGoogle Scholar
  46. Pinruan U, Rungjindamai N, Choeyklin R, Lumyong S, Hyde KD, Jones EBG (2010) Occurrence and diversity of basidiomycetous endophytes from the oil palm, Elaeis guineensis in Thailand. Fungal Divers 41:71–88.  https://doi.org/10.1007/s13225-010-0029-1 CrossRefGoogle Scholar
  47. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693.  https://doi.org/10.1146/annurev.arplant.50.1.665 CrossRefPubMedGoogle Scholar
  48. Raja HA, Miller AN, Pearce CJ, Oberlies NH (2017) Fungal identification using molecular tools: a primer for the natural products research community. J Nat Prod 80:756–770.  https://doi.org/10.1021/acs.jnatprod.6b01085 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Rédou V, Navarri M, Meslet-Cladière L, Barbier G, Burgaud G (2015) Species richness and adaptation of marine fungi from deep-subseafloor sediments. Appl Environ Microbiol 81:3571–3583.  https://doi.org/10.1128/aem.04064-14 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Rodríguez D, Andrade FH, Goudriaan J (1999) Effects of phosphorus nutrition on tiller emergence in wheat. Plant Soil 209:283–295.  https://doi.org/10.1023/a:1004690404870 CrossRefGoogle Scholar
  51. Russell P, Hertz P, McMillan B (2016) Biology: the dynamic science. Cengage Learning US, 3th edn, BelmontGoogle Scholar
  52. Ruttenberg KC (2003) Treatise Geochem. In: Schlesinger WH (ed) The global phosphorus cycle, vol 8. Elsevier ISBN 0-08-043751-6, pp 585–643Google Scholar
  53. Sattari SZ, Bouwman AF, Giller KE, van Ittersum MK (2012) Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proc Natl Acad Sci U S A 109(6348):6353Google Scholar
  54. Schachtman DP, Reid RJ, Ayling S (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453CrossRefPubMedPubMedCentralGoogle Scholar
  55. Schäfer P, Kogel KH (eds) (2009) The secacinoid fungus Piriformospora indica: an orchid mycorrhiza fungus which may increase host plant reproduction and fitness. Springer, Berlin, pp 99–122Google Scholar
  56. Scarpari M, Bello C, Pietricola C, Zaccaria M, Bertocchi L, Angelucci A, Ricciardi MR, Scala V, Parroni A, Fabbri AA, Reverberi M, Zjalic S, Fanelli C (2014) Aflatoxin control in maize by Trametes versicolor. Toxins (Basel) 6:3426–3437.  https://doi.org/10.3390/toxins6123426 CrossRefGoogle Scholar
  57. Schouten A (2016) Mechanisms involved in nematode control by endophytic fungi. Annu Rev Phytopathol 54:121–142.  https://doi.org/10.1146/annurev-phyto-080615-100114 CrossRefPubMedGoogle Scholar
  58. Serfling A, Wirsel SG, Lind V, Deising HD (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531.  https://doi.org/10.1094/phyto-97-4-0523 CrossRefPubMedGoogle Scholar
  59. 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 162:945–958CrossRefPubMedGoogle Scholar
  60. Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156(997):1005Google Scholar
  61. 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.  https://doi.org/10.1074/jbc.M500447200 CrossRefPubMedGoogle Scholar
  62. Shikano I, Rosa C, Tan C-W, Felton GW (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol 55:313–331.  https://doi.org/10.1146/annurev-phyto-080516-035319 CrossRefPubMedGoogle Scholar
  63. Singh A, Rajpal K, Singh M, Kharkwal AC, Arora M, Varma A (2013) Mass cultivation of Piriformospora indica and Sebacina species. In: Varma A, Kost G, Oelmüller R (eds) Piriformospora indica: Sebacinales and their biotechnological applications. Springer, Berlin Heidelberg, BerlinGoogle Scholar
  64. Varma A, Savita V, Sudha SN, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744PubMedPubMedCentralGoogle Scholar
  65. Vazquez P, Holguin G, Puente ME, Lopez-Cortes A, Bashan Y (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468.  https://doi.org/10.1007/s003740050024 CrossRefGoogle Scholar
  66. Veiga RSL, Jansa J, Frossard E, van der Heijden MGA (2011) Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PLoS One 6:e27825CrossRefPubMedPubMedCentralGoogle Scholar
  67. Verma S, 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 90:896–903.  https://doi.org/10.2307/3761331 CrossRefGoogle Scholar
  68. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt stress tolerance, disease resistance and higher yield. Proc Nat Acad Sci USA 102:13386–13391CrossRefPubMedPubMedCentralGoogle Scholar
  69. Weiss M, Waller F, Zuccaro A, Selosse MA (2016) Sebacinales - one thousand and one interactions with land plants. New Phytol 211:20–40.  https://doi.org/10.1111/nph.13977 CrossRefPubMedGoogle Scholar
  70. White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Gelfand D, Shinsky J, White T (eds) M Innis. A Guide to Methods and Applications. Academic Press, PCR ProtocolsGoogle Scholar
  71. 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 285:26532–26544CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Meysam Taghinasab
    • 1
  • Jafargholi Imani
    • 1
  • Diedrich Steffens
    • 3
  • Stefanie P. Glaeser
    • 2
  • Karl-Heinz Kogel
    • 1
  1. 1.Institute of Phytopathology, Research Centre for BioSystemsJustus Liebig UniversityGiessenGermany
  2. 2.Institute of Applied Microbiology, Research Centre for BioSystemsJustus Liebig UniversityGiessenGermany
  3. 3.Institute for Plant Nutrition, Research Centre for BioSystemsJustus Liebig UniversityGiessenGermany

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