The root endophytes Trametes versicolor and Piriformospora indica increase grain yield and P content in wheat
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).
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.
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).
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.
KeywordsRoot endophyte Piriformospora indica Trametes versicolor Phosphate Yield parameters
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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Kogel K-H, Franken P, Hückelhoven R (2006) Endophyte or parasite – what decides? Curr Opin Plant Biol 9(358):363Google Scholar
- 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
- 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
- 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
- Meyberg M (1988) Selective staining of fungal hyphae in parasitic and symbiotic plant-fungus associations. For Hist 88:197–199Google Scholar
- 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
- 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
- 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
- Russell P, Hertz P, McMillan B (2016) Biology: the dynamic science. Cengage Learning US, 3th edn, BelmontGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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