Abstract
Background and aims
Recent studies indicate the potential of endophytic entomopathogenic fungi to promote plant growth but little is known about the responses of root architecture to fungal endophytism. This study investigates potential adaptations of root architecture upon Metarhizium brunneum endophytism linked to improved plant growth and nutrition.
Methods
Plants (Solanum tuberosum L.) were grown in the presence of M. brunneum applied either as non-formulated mycelium or as mycelium containing beads. After 35 days, fungal growth, root endophytism, plant biomass and nutrition as well as root attributes were determined.
Results
In response to endophytism promoted by bead application, plant P contents and biomass were significantly increased, while N contents and shoot allocation were also significantly increased in plants from the beads without mycelium group. Bead application resulted in a shift from fine to medium-sized roots and in an increase in the number of root forks, while root diameter, surface area and the number of root tips and crossings were independent of either bead or M. brunneum treatment.
Conclusions
M. brunneum containing beads supported endophytism allowing for increases in plant P contents and biomass. However, root architecture was not strongly modulated by M. brunneum endophytism with N provision through bead application being more important than fungal P delivery.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nutr 12:547–562. https://doi.org/10.4067/S0718-95162012005000015
Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250
Behie SW, Bidochka MJ (2014) Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. Appl Environ Microbiol 80:1553–1560. https://doi.org/10.1128/AEM.03338-13
Behie S, Zelisko P, Bidochka M (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577. https://doi.org/10.1126/science.1222289
Behie SW, Jones SJ, Bidochka MJ (2015) Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol 13:112–119. https://doi.org/10.1016/j.funeco.2014.08.001
Behie SW, Moreira CC, Sementchoukova I, Barelli L, Zelisko PM, Bidochka MJ (2017) Carbon translocation from a plant to an insect-pathogenic endophytic fungus. Nat Commun 8:14245. https://doi.org/10.1038/ncomms14245
Bruck DJ (2010) Fungal entomopathogens in the rhizosphere. BioControl 55:103–112. https://doi.org/10.1007/s10526-009-9236-7
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304. https://doi.org/10.1046/j.1469-8137.2002.00397.x
Croft SA, Pitchford JW, Hodge A (2015) Fishing for nutrients in heterogeneous landscapes: modelling plant growth trade-offs in monocultures and mixed communities. AoB Plants 7:plv109. https://doi.org/10.1093/aobpla/plv109
Eissenstat DM, Kucharski JM, Zadworny M, Adams TS, Koide RT (2015) Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytol 208:114–124. https://doi.org/10.1111/nph.13451
Fusconi A (2013) Regulation of root morphogenesis in arbuscular mycorrhizae: what role do fungal exudates, phosphate, sugars and hormones play in lateral root formation? Ann Bot 113:19–33. https://doi.org/10.1093/aob/mct258
García JE, Posadas JB, Perticari A, Lecuona R (2011) Metarhizium anisopliae (Metschnikoff) Sorokin promotes growth and has endophytic activity in tomato plants. Adv Biol Res 5:22–27
Gleeson SK, Tilman D (1990) Allocation and the transient dynamics of succession on poor soils. Ecology 71:1144–1155
Goltapeh EM, Danesh YR, Prasad R, Varma A (2008) Mycorrhizal fungi: what we know and what should we know? In: Varma A (ed) Mycorrhiza. Springer, Heidelberg, pp 3–27
Greenfield M, Gómez-Jiménez MI, Ortiz V, Vega FE, Kramer M, Parsa S (2016) Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biol Control 95:40–48. https://doi.org/10.1016/j.biocontrol.2016.01.002
Gruber BD, Giehl RF, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179. https://doi.org/10.1104/pp.113.218453
Hetrick B (1991) Mycorrhizas and root architecture. Cell Mol Life Sci 47:355–362
Hetrick BD, Kitt DG, Wilson GT (1988) Mycorrhizal dependence and growth habit of warm-season and cool-season tallgrass prairie plants. Can J Bot 66:1376–1380
Hoepfner I, Beyschlag W, Bartelheimer M, Werner C, Unger S (2015) Role of mycorrhization and nutrient availability in competitive interactions between the grassland species Plantago lanceolata and Hieracium pilosella. Plant Ecol 216:887–899. https://doi.org/10.1007/s11258-015-0476-6
Hu G, Leger RJS (2002) Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Appl Environ Microbiol 68:6383–6387. https://doi.org/10.1128/AEM.68.12.6383-6387.2002
Jaber LR, Enkerli J (2016) Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biol Control 103:187–195. https://doi.org/10.1016/j.biocontrol.2016.09.008
Jaber LR, Enkerli J (2017) Fungal entomopathogens as endophytes: can they promote plant growth? Biocontrol Sci Tech 27:28–41. https://doi.org/10.1080/09583157.2016.1243227
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585. https://doi.org/10.1046/j.1469-8137.1997.00729.x
Kabaluk JT, Ericsson JD (2007) Seed treatment increases yield of field corn when applied for wireworm control. Agron J 99:1377–1381. https://doi.org/10.2134/agronj2007.0017N
Koevoets IT, Venema JH, Elzenga JTM, Testerink C (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.01335
Krell V, Jakobs-Schoenwandt D, Vidal S, Patel AV (2017) Encapsulation of Metarhizium brunneum enhances endophytism in tomato plants. Biol Control 116:62–73. https://doi.org/10.1016/j.biocontrol.2017.05.004
Krell V, Jakobs-Schoenwandt D, Vidal S, Patel AV (2018) Cellulase enhances endophytism of encapsulated Metarhizium brunneum in potato plants. Fungal Biol 122:373–378. https://doi.org/10.1016/j.funbio.2018.03.002
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713. https://doi.org/10.1093/aob/mcl114
Liao X, O’Brien TR, Fang W, Leger RJS (2014) The plant beneficial effects of Metarhizium species correlate with their association with roots. Appl Microbiol Biotechnol 98:7089–7096. https://doi.org/10.1007/s00253-014-5788-2
Liao X, Lovett B, Fang W, St Leger RJ (2017) Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiology 163:980–991. https://doi.org/10.1099/mic.0.000494
Linkohr BI, Williamson LC, Fitter AH, Leyser H (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760
Liu S-F et al (2017) Entomopathogen Metarhizium anisopliae promotes the early development of peanut root. Plant Prot Sci 53:101–107. https://doi.org/10.17221/49/2016-PPS
López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256. https://doi.org/10.1104/pp.010934
Marschner H (2011) Mineral nutrition of higher plants. Academic Press, London
Murphy BR, Martin Nieto L, Doohan FM, Hodkinson TR (2015) Profundae diversitas: the uncharted genetic diversity in a newly studied group of fungal root endophytes. Mycology 6:139–150. https://doi.org/10.1080/21501203.2015.1070213
Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00537
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. https://doi.org/10.1038/nrmicro1987
Price N, Roncadori R, Hussey R (1989) Cotton root growth as influenced by phosphorus nutrition and vesicular–arbuscular mycorrhizas. New Phytol 111:61–66
Przyklenk M, Vemmer M, Hanitzsch M, Patel A (2017) A bioencapsulation and drying method increases shelf life and efficacy of Metarhizium brunneum conidia. J Microencapsul 34:498–512. https://doi.org/10.1080/02652048.2017.1354941
Raya-Díaz S, Sánchez-Rodríguez AR, Segura-Fernández JM, del Campillo MC, Quesada-Moraga E (2017) Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates. PLoS One 12:e0185903. https://doi.org/10.1371/journal.pone.0185903
Sasan RK, Bidochka MJ (2012) The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot 99:101–107. https://doi.org/10.3732/ajb.1100136
Schneider S, Rehner S, Widmer F, Enkerli J (2011) A PCR-based tool for cultivation-independent detection and quantification of Metarhizium clade 1. J Invertebr Pathol 108:106–114. https://doi.org/10.1016/j.jip.2011.07.005
Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686. https://doi.org/10.1017/S095375620500273X
Shipley B, Meziane D (2002) The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Funct Ecol 16:326–331. https://doi.org/10.1046/j.1365-2435.2002.00626.x
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, London
Strasser H, Forer A, Schinner F (1996) Development of media for the selective isolation and maintenance of virulence of Beauveria brongniartii. In: Jackson TA, Glare TR (eds) Proc. 3rd internat. workshop on microbial control of soil dwelling pest, Lincoln. Ag Research, pp 125–130
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677. https://doi.org/10.1038/nature01014
Unger S, Friede M, Hundacker J, Volkmar K, Beyschlag W (2016) Allocation trade-off between root and mycorrhizal surface defines nitrogen and phosphorus relations in 13 grassland species. Plant Soil 407:279–292. https://doi.org/10.1007/s11104-016-2994-y
Unger S, Friede M, Volkmar K, Hundacker J, Beyschlag W (2017) Relationship between mycorrhizal responsiveness and root traits in European sand dune species. Rhizosphere 3:160–169. https://doi.org/10.1016/j.rhisph.2017.04.008
Vemmer M, Patel AV (2013) Review of encapsulation methods suitable for microbial biological control agents. Biol Control 67:380–389. https://doi.org/10.1016/j.biocontrol.2013.09.003
Veresoglou SD, Menexes G, Rillig MC (2012) Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22:227–235. https://doi.org/10.1007/s00572-011-0398-7
Wachsman G, Sparks EE, Benfey PN (2015) Genes and networks regulating root anatomy and architecture. New Phytol 208:26–38. https://doi.org/10.1111/nph.13469
Watanabe F, Olsen S (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Sci Soc Am J 29:677–678
Williamson LC, Ribrioux SP, Fitter AH, Leyser HO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882
Wu Q-S, Liu C-Y, Zhang D-J, Zou Y-N, He X-H, Wu Q-H (2016) Mycorrhiza alters the profile of root hairs in trifoliate orange. Mycorrhiza 26:237–247. https://doi.org/10.1007/s00572-015-0666-z
Yan B, Ji Z, Fan B, Wang X, He G, Shi L, Liu G (2016) Plants adapted to nutrient limitation allocate less biomass into stems in an arid-hot grassland. New Phytol 211:1232–1240. https://doi.org/10.1111/nph.13970
Zangaro W, Nishidate FR, Camargo FRS, Romagnoli GG, Vandressen J (2005) Relationships among arbuscular mycorrhizas, root morphology and seedling growth of tropical native woody species in southern Brazil. J Trop Ecol 21:529–540. https://doi.org/10.1017/S0266467405002555
Acknowledgements
The research conducted in this study was funded by the German Federal Environmental Foundation (31421/01). We would like to thank Prof. Dr. Stefan Vidal (Agricultural Entomology, Department for Crop Science, Georg-August-University Goettingen, Germany) for providing Metarhizium brunneum strain CB15. Special thanks to Herbstreith & Fox KG (Neuenbuerg/Wuertt, Germany) for providing the amidated pectins and to the WG Microbial Genomics and Biotechnology (Center for Biotechnology, Bielefeld, Germany) for providing access to the real-time PCR equipment. Finally, we would like to thank Elke Furlkroeger, Christine Schlueter and Barbara Teichner for their support during plant harvest and laboratory work.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Katharina Pawlowski.
Rights and permissions
About this article
Cite this article
Krell, V., Unger, S., Jakobs-Schoenwandt, D. et al. Importance of phosphorus supply through endophytic Metarhizium brunneum for root:shoot allocation and root architecture in potato plants. Plant Soil 430, 87–97 (2018). https://doi.org/10.1007/s11104-018-3718-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-018-3718-2