Skip to main content
SpringerLink
Log in

Facilitation of plant water uptake by an arbuscular mycorrhizal fungus: a Gordian knot of roots and hyphae

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal (AM) fungi play a positive role in plant water relations, and the AM symbiosis is often cited as beneficial for overcoming drought stress of host plants. Nevertheless, water uptake via mycorrhizal hyphal networks has been little addressed experimentally, especially so through isotope tracing. In a greenhouse study conducted in two-compartment rhizoboxes, Medicago truncatula was planted in the primary compartment (PC), either inoculated with Rhizophagus irregularis or left uninoculated. Plant roots were either allowed to enter the secondary compartment (SC) or were restricted to the PC by root-excluding mesh. Substrate moisture was manipulated in the PC such that the plants were grown either in high moisture (15% of gravimetric water content, GWC) or low moisture (8% GWC). Meanwhile, the SC was maintained at 15% GWC throughout and served as a water source accessible (or not) by roots and/or hyphae. Water in the SC was labeled with deuterium (D) to quantify water uptake by the plants from the SC. Significantly, increased D incorporation into plants indicated higher water uptake by mycorrhizal plants when roots had access to the D source, but this was mainly explained by generally larger mycorrhizal root systems in proximity to the D source. On the other hand, AM fungal hyphae with access to the D source increased D incorporation into plants more than twofold compared to non-mycorrhizal plants. Despite this strong effect, water transport via AM fungal hyphae was low compared to the transpiration demand of the plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allen MF (1982) Influence of vesicular arbuscular mycorrhizae on water-movement through Bouteloua gracilis (H.B.K.) Lag ex Steud. New Phytol 91:191–196

    Google Scholar 

  • Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297

    Google Scholar 

  • Augé RM (1989) Do VA mycorrhizae enhance transpiration by affecting host phosphorus content? J Plant Nutr 12:743–753

    Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Google Scholar 

  • Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations can J. Soil Sci 84:373–381

    Google Scholar 

  • Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24

    PubMed  Google Scholar 

  • Beyer M, Koeniger P, Gaj M, Hamutoko JT, Wanke H, Himmelsbach T (2016) A deuterium-based labeling technique for the investigation of rooting depths, water uptake dynamics and unsaturated zone water transport in semiarid environments. J Hydrol 533:627–643

    CAS  Google Scholar 

  • Bitterlich M, Franken P (2016) Connecting polyphosphate translocation and hyphal water transport points to a key of mycorrhizal functioning. New Phytol 211:1147–1149

    PubMed  Google Scholar 

  • Bitterlich M, Franken P, Graefe J (2018a) Arbuscular mycorrhiza improves substrate hydraulic conductivity in the plant available moisture range under root growth exclusion. Front Plant Sci 9:11

    Google Scholar 

  • Bitterlich M, Sandmann M, Graefe J (2018b) Arbuscular mycorrhiza alleviates restrictions to substrate water flow and delays transpiration limitation to stronger drought in tomato. Front Plant Sci 9:15

    Google Scholar 

  • Bitterlich M, Franken P, Graefe J (2019) Atmospheric drought and low light impede mycorrhizal effects on leaf photosynthesisa glasshouse study on tomato under naturally fluctuating environmental conditions. Mycorrhiza 29:13–28

    PubMed  Google Scholar 

  • Bukovská P, Gryndler M, Gryndlerová H, Püschel D, Jansa J (2016) Organic nitrogen-driven stimulation of arbuscular mycorrhizal fungal hyphae correlates with abundance of ammonia oxidizers. Front Microbiol 7:15

    Google Scholar 

  • Bukovská P, Bonkowski M, Konvalinková T, Beskid O, Hujslová M, Püschel D, Řezáčová V, Gutiérrez-Núñez MS, Gryndler M, Jansa J (2018) Utilization of organic nitrogen by arbuscular mycorrhizal fungi-is there a specific role for protists and ammonia oxidizers? Mycorrhiza 28:269–283

    PubMed  Google Scholar 

  • Couillerot O et al (2013) Comparison of prominent Azospirillum strains in Azospirillum-Pseudomonas-Glomus consortia for promotion of maize growth. Appl Microbiol Biot 97:4639–4649

    CAS  Google Scholar 

  • Drew EA, Murray RS, Smith SE, Jakobsen I (2003) Beyond the rhizosphere: growth and function of arbuscular mycorrhizal external hyphae in sands of varying pore sizes. Plant Soil 251:105–114

    CAS  Google Scholar 

  • Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244:221–230

    CAS  Google Scholar 

  • Faber BA, Zasoski RJ, Munns DN, Shackel K (1991) A method for measuring hyphal nutrient and water-uptake in mycorrhizal plants. Can J Bot 69:87–94

    Google Scholar 

  • Fang YJ, Xiong LZ (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72:673–689

    CAS  PubMed  Google Scholar 

  • Fitter AH (1985) Functioning of vesicular arbuscular mycorrhizas under field conditions. New Phytol 99:257–265

    Google Scholar 

  • Friese CF, Allen MF (1991) The spread of VA mycorrhizal fungal hyphea in the soil - inoculum types and external hyphal architecture. Mycologia 83:409–418

    Google Scholar 

  • George E, Haussler KU, Vetterlein D, Gorgus E, Marschner H (1992) Water and nutrient translocation by hyphae of Glomus mosseae. Can J Bot 70:2130–2137

    Google Scholar 

  • Graham JH, Syvertsen JP (1984) Influence of vesicular arbuscular mycorrhiza on the hydraulic conductivity of roots of 2 citrus rootstocks. New Phytol 97:277–284

    Google Scholar 

  • Grimoldi AA, Kavanová M, Lattanzi FA, Schäufele R, Schnyder H (2006) Arbuscular mycorrhizal colonization on carbon economy in perennial ryegrass: quantification by 13CO2 / 12CO2 steady-state labelling and gas exchange. New Phytol 172:544–553

    CAS  PubMed  Google Scholar 

  • Hamblin AP (1985) The influence of soil structure on water-movement, crop root-growth, and water-uptake. Adv Agron 38:95–158

    Google Scholar 

  • Harrison MJ, Vanbuuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629

    CAS  PubMed  Google Scholar 

  • Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386:1–19

    CAS  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299

    CAS  PubMed  Google Scholar 

  • Hoeksema JD et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407

    PubMed  Google Scholar 

  • Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hypheafrom roots of mycorrhizal cucumber plants. New Phytol 115:77–83

    Google Scholar 

  • Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91

    PubMed  Google Scholar 

  • Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23:481–488

    CAS  Google Scholar 

  • Jansa J, Mozafar A, Frossard E (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant Soil 276:163–176

    CAS  Google Scholar 

  • Jansa J, Forczek ST, Rozmos M, Püschel D, Bukovská P, Hršelová H (2019) Arbuscular mycorrhiza and soil organic nitrogen: network of players and interactions. Chem Biol Technol Agric 6:10

    Google Scholar 

  • Jansa J et al (2020) Dead Rhizophagus irregularis biomass mysteriously stimulates plant growth. Mycorrhiza

  • Johansen A, Jakobsen I, Jensen ES (1992) Hyphal transport of 15N-labelled nitrogen by a vesicular–arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil N. New Phytol 122:281–288

    CAS  PubMed  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    CAS  PubMed  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586

    Google Scholar 

  • Johnson D, Leake JR, Read DJ (2001) Novel in-growth core system enables functional studies of grassland mycorrhizal mycelial networks. New Phytol 152:555–562

    PubMed  Google Scholar 

  • Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the Law of the Minimum. New Phytol 205:1473–1484

    CAS  PubMed  Google Scholar 

  • Kiers ET et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    CAS  PubMed  Google Scholar 

  • Kikuchi Y et al (2016) Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol 211:1202–1208

    CAS  PubMed  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Google Scholar 

  • Koeniger P, Leibundgut C, Link T, Marshall JD (2010) Stable isotopes applied as water tracers in column and field studies. Org Geochem 41:31–40

    CAS  Google Scholar 

  • Koide RT (1993) Physiology of the mycorrhizal plant advances of. Plant Pathol 9:33–54

    Google Scholar 

  • Koide RT, Li MG (1989) Appropriate controls for vesicular arbuscular mycorrhiza research. New Phytol 111:35–44

    Google Scholar 

  • Konvalinková T, Püschel D, Janoušková M, Gryndler M, Jansa J (2015) Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of Medicago truncatula. Front Plant Sci 6:65

    PubMed  PubMed Central  Google Scholar 

  • Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA-mycorrhizas. Mycol Res 92:486–505

    Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    PubMed  Google Scholar 

  • Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Kapulnik Y, Douds DD Jr (eds) Arbuscular mycorrhizas: physiology and function. Springer, pp 3–18

  • Miller RM, Reinhardt DR, Jastrow JD (1995) External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103:17–23

    CAS  PubMed  Google Scholar 

  • Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364

    PubMed  Google Scholar 

  • Neumann E, George E (2004) Colonisation with the arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) enhanced phosphorus uptake from dry soil in Sorghum bicolor (L.). Plant Soil 261:245–255

    CAS  Google Scholar 

  • Neumann E, Schmid B, Romheld V, George E (2009) Extraradical development and contribution to plant performance of an arbuscular mycorrhizal symbiosis exposed to complete or partial rootzone drying. Mycorrhiza 20:13–23

    PubMed  Google Scholar 

  • Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus is soil extracts using malachite green. Soil Sci Soc Am J 55:892–895

    CAS  Google Scholar 

  • Püschel D, Janoušková M, Hujslová M, Slavíková R, Gryndlerová H, Jansa J (2016) Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecol Evol 6:4332–4346

    PubMed  PubMed Central  Google Scholar 

  • Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J (2017) Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp. through improved phosphorus acquisition. Front Plant Sci 8:12

    Google Scholar 

  • Raven JA, Edwards D (2001) Roots: evolutionary origins and biogeochemical significance. J Exp Bot 52:381–401

    CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plantarum 95:472–478

    CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcon R, Gomez M (1995) Effects of arbuscular-mycorrhizal Glomus species on drought tolerance - physiological and nutritional plant-responses. Appl Environ Microb 61:456–460

    CAS  Google Scholar 

  • Santander C, Aroca R, Ruiz-Lozano JM, Olave J, Cartes P, Borie F, Cornejo P (2017) Arbuscular mycorrhiza effects on plant performance under osmotic stress. Mycorrhiza 27:639–657

    CAS  PubMed  Google Scholar 

  • Schwendenmann L, Dierick D, Kohler M, Holscher D (2010) Can deuterium tracing be used for reliably estimating water use of tropical trees and bamboo? Tree Physiol 30:886–900

    CAS  PubMed  Google Scholar 

  • Slavíková R et al (2017) Monitoring CO2 emissions to gain a dynamic view of carbon allocation to arbuscular mycorrhizal fungi. Mycorrhiza 27:35–51

    PubMed  Google Scholar 

  • Smart DR, Carlisle E, Goebel M, Nunez BA (2005) Transverse hydraulic redistribution by a grapevine. Plant Cell Environ 28:157–166

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, Cambridge

    Google Scholar 

  • Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20

    CAS  Google Scholar 

  • Smith SE, Jakobsen I, Gronlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    CAS  PubMed  PubMed Central  Google Scholar 

  • Somasegaran P, Hoben HJ (1994) Handbook for rhizobia: methods in legume-rhizobium technology. Springer, New York

    Google Scholar 

  • Subramanian KS, Charest C, Dwyer LM, Hamilton RI (1995) Arbuscular mycorrhizas and water relations in maize under drought stress at tasselling. New Phytol 129:643–650

    Google Scholar 

  • Thonar C, Erb A, Jansa J (2012) Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communitiesumarker design, verification, calibration and field validation. Mol Ecol Resour 12:219–232

    CAS  PubMed  Google Scholar 

  • Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, New York

  • van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578

    Google Scholar 

  • Voříšková A, Jansa J, Püschel D, Vosátka M, Šmilauer P, Janoušková M (2019) Abiotic contexts consistently influence mycorrhiza functioning independently of the composition of synthetic arbuscular mycorrhizal fungal communities. Mycorrhiza 29:127–139

    PubMed  Google Scholar 

  • Wagg C, Jansa J, Schmid B, van der Heijden MGA (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009

    PubMed  Google Scholar 

  • Whiteside MD et al (2019) Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks. Curr Biol 29:2043

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Jan Rydlo for technical assistance with the experiment, including the precise and time-consuming measurement of substrate moisture. Further, the authors would like to thank two anonymous reviewers for their critical and inspiring comments on an earlier version of the manuscript. Finally, the role of Dave Janos, the editor of Mycorrhiza, and his helpful suggestions considerably improved this manuscript and are gratefully acknowledged.

Funding

The study was supported by the Czech Science Foundation (project 17-12166S) and by the Czech Academy of Sciences within the long-term research development programs RVO 67985939 and RVO 61388971. The work related to the Leibniz Institute of Vegetable and Ornamental Crops e.V. (IGZ) has received funding from the Ministry of Consumer Protection, Food and Agriculture of the Federal Republic of Germany and from the Ministry for Science, Research and Culture of the State of Brandenburg.

Author information

Authors and Affiliations

  1. Department of Mycorrhizal Symbioses, Institute of Botany of the Czech Academy of Sciences, Průhonice, Czech Republic

    David Püschel & Jana Rydlová

  2. Laboratory of Fungal Biology, Institute of Microbiology of the Czech Academy of Sciences, Prague, Czech Republic

    David Püschel & Jan Jansa

  3. Leibniz Institute of Vegetable and Ornamental Crops e.V. (IGZ), Grossbeeren, Germany

    Michael Bitterlich

Authors
  1. David Püschel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Bitterlich
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jana Rydlová
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jan Jansa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David Püschel.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary materials

ESM 1

(PDF 819 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Püschel, D., Bitterlich, M., Rydlová, J. et al. Facilitation of plant water uptake by an arbuscular mycorrhizal fungus: a Gordian knot of roots and hyphae. Mycorrhiza 30, 299–313 (2020). https://doi.org/10.1007/s00572-020-00949-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-020-00949-9

Keywords

Search

Navigation