Development of arbuscular mycorrhizal fungal colonization of roots and the surrounding soil is the central process of mycorrhizal symbiosis, important for ecosystem functioning and commercial inoculum applications. To improve mechanistic understanding of this highly spatially and temporarily dynamic process, we developed a three-dimensional model taking into account growth of the roots and hyphae. It is for the first time that infection within the root system is simulated dynamically and in a spatially resolved way. Comparison between data measured in a calibration experiment and simulated results showed a good fit. Our simulations showed that the position of the fungal inoculum affects the sensitivity of hyphal growth parameters. Variation in speed of secondary infection and hyphal lifetime had a different effect on root infection and hyphal length, respectively, depending on whether the inoculum was concentrated or dispersed. For other parameters (branching rate, distance between entry points), the relative effect was the same independent of inoculum placement. The model also indicated that maximum root colonization levels well below 100%, often observed experimentally, may be a result of differential spread of roots and hyphae, besides intrinsic plant control, particularly upon localized placement of inoculum and slow secondary infection.

Computational Science Center University of Vienna Oskar Morgenstern Platz 1 1090 Vienna Austria

Department of Microbiology and Ecosystem Science University of Vienna Althanstrasse 14 1090 Vienna Austria

Forschungszentrum Juelich GmbH Institute of Bio and Geosciences IBG 3 Agrosphere 52425 Juelich Germany

Institute of Hydraulics and Rural Water Management BOKU University of Natural Resources and Life Sciences Muthgasse 18 1190 Vienna Austria

Laboratory of Fungal Biology Institute of Microbiology Academy of Sciences of the Czech Republic Vídeňská 1083 Praha 4 Krč 142 20 Czech Republic

Zobrazit více v PubMed

Wyatt GAK, Kiers ET, Gardner A, West SA. 2014. A biological market analysis of the plant–mycorrhizal symbiosis. Evolution 68, 2603–2618. (10.1111/evo.12466) PubMed DOI

Treseder K. 2013. The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil 371, 1–13. (10.1007/s11104-013-1681-5) DOI

Jakobsen I, Abbott LK, Robson AD. 1992. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol. 120, 371–380. (10.1111/j.1469-8137.1992.tb01077.x) DOI

Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I. 2004. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol. 164, 357–364. (10.1111/j.1469-8137.2004.01169.x) PubMed DOI

Jansa J, Smith FA, Smith SE. 2008. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol. 177, 779–789. (10.1111/j.1469-8137.2007.02294.x) PubMed DOI

Lendenmann M, Thonar C, Barnard RL, Salmon Y, Werner RA, Frossard E, Jansa J. 2011. Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza 21, 689–702. (10.1007/s00572-011-0371-5) PubMed DOI

Thonar C, Schnepf A, Frossard E, Roose T, Jansa J. 2011. Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil 339, 231–245. (10.1007/s11104-010-0571-3) DOI

Duke SE, Jackson RB, Caldwell MM. 1994. Local reduction of mycorrhizal arbuscule frequency in enriched soil microsites. Can. J. Bot. 72, 998–1001. (10.1139/b94-125) DOI

Treseder KK, Allen MF. 2002. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol. 155, 507–515. (10.1046/j.1469-8137.2002.00470.x) PubMed DOI

Schroeder MS, Janos DP. 2005. Plant growth, phosphorus nutrition, and root morphological responses to arbuscular mycorrhizas, phosphorus fertilization, and intraspecific density. Mycorrhiza 15, 203–216. (10.1007/s00572-004-0324-3) PubMed DOI

Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P. 2008. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20, 1407–1420. (10.1105/tpc.108.059014) PubMed DOI PMC

Friese C, Allen M. 1991. The spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture. Mycologia 83, 409–418. (10.2307/3760351) DOI

VanDer Heijden MGA, Scheublin TR. 2007. Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol. 174, 244–250. (10.1111/j.1469-8137.2007.02041.x) PubMed DOI

Buwalda JG, Stribley DP, Tinker PB. 1984. The development of endomycorrhizal root systems. V. The detailed patterns of development of infection and the control of infection level by host in young leek plants. New Phytol. 96, 411–427. (10.1111/j.1469-8137.1984.tb03576.x) DOI

Bruce A, Smith SE, Tester M. 1994. The development of mycorrhizal infection in cucumber: effects of P supply on root growth, formation of entry points and growth of infection units. New Phytol. 127, 507–514. (10.1111/j.1469-8137.1994.tb03968.x) DOI

Rosling A, Roose T, Herrmann AM, Davidson FA, Finlay RD, Gadd GM. 2009. Approaches to modelling mineral weathering by fungi. Fungal Biol. Rev. 23, 138–144. (10.1016/j.fbr.2009.09.003) DOI

Hopkins S, Boswell GP. 2012. Mycelial response to spatiotemporal nutrient heterogeneity: a velocity-jump mathematical model. Fungal Ecol. 5, 124–136. (10.1016/j.funeco.2011.06.006) DOI

Cunniffe NJ, Gilligan CA. 2008. Scaling from mycelial growth to infection dynamics: a reaction diffusion approach. Fungal Ecol. 1, 133–142. (10.1016/j.funeco.2008.10.007) DOI

Boswell GP, Davidson FA. 2012. Modelling hyphal networks. Fungal Biol. Rev. 26, 30–38. (10.1016/j.fbr.2012.02.002) DOI

McGonigle TB. 2001. On the use of non-linear regression with the logistic equation for changes with time of percentage root length colonized by arbuscular mycorrhizal fungi. Mycorrhiza 10, 249–254. (10.1007/s005720000080) DOI

Bever JD. 2015. Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts. New Phytol. 205, 1503–1514. (10.1111/nph.13239) PubMed DOI

Landis FC, Fraser LH. 2008. A new model of carbon and phosphorus transfers in arbuscular mycorrhizas. New Phytol. 177, 466–479. PubMed

Buwalda JG, Ross GJS, Stribley DP, Tinker PB. 1982. The development of endomycorrhizal root systems. III. The mathematical representation of the spread of vesicular–arbuscular mycorrhizal infection in root systems. New Phytol. 91, 669–682. (10.1111/j.1469-8137.1982.tb03346.x) DOI

Buwalda JG, Ross GJS, Stribley DP, Tinker PB. 1982. The development of endomycorrhizal root systems. IV. The mathematical analysis of effects of phosphorus on the spread of vesicular–arbuscular mycorrhizal infection in root systems. New Phytol. 92, 391–399. (10.1111/j.1469-8137.1982.tb03396.x) DOI

Schnepf A, Roose T, Schweiger P. 2008. Growth model for arbuscular mycorrhizal fungi. J. R. Soc. Interface 5, 773–784. (10.1098/rsif.2007.1250) PubMed DOI PMC

Schnepf A, Roose T, Schweiger P. 2008. Impact of growth and uptake patterns of arbuscular mycorrhizal fungi on plant phosphorus uptake—a modelling study. Plant Soil 312, 85–99. (10.1007/s11104-008-9749-3) DOI

Leitner D, Klepsch S, Bodner G, Schnepf A. 2010. A dynamic root system growth model based on L-systems. Plant Soil 332, 177–192. (10.1007/s11104-010-0284-7) DOI

Leitner D, Klepsch S, Knieß A, Schnepf A. 2010. The algorithmic beauty of plant roots—an L-system model for dynamic root growth simulation. Math. Comput. Model. Dyn. Syst. 16, 575–587. (10.1080/13873954.2010.491360) DOI

Hart MM, Reader RJ. 2002. Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol. 153, 335–344. (10.1046/j.0028-646X.2001.00312.x) DOI

Sanders FE, Tinker PB, Black RLB, Palmerley SM. 1977. The development of endymycorrhizal root systems: I. Spread of infection and growth-promoting effects with four species of vesicular-arbuscular endophyte. New Phytol. 78, 257–268. (10.1111/j.1469-8137.1977.tb04829.x) DOI

Smith SE, Walker NA. 1981. A quantitative study of mycorrhizal infection in Trifolium: separate determination of the rates of infection and of mycelial growth. New Phytol. 89, 225–240. (10.1111/j.1469-8137.1981.tb07485.x) DOI

Jakobsen I, Abbott LK, Robson AD. 1992. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytol. 120, 509–516. (10.1111/j.1469-8137.1992.tb01800.x) DOI

Black R, Tinker PB. 1979. The development of endymycorrhizal root systems. II. Effect of agronomic factors and soil conditions on the development of vesicular-arbuscular mycorrhizal infection in barley and on the endophyte spore density. New Phytol. 83, 401–413. (10.1111/j.1469-8137.1979.tb07465.x) DOI

Amijee F, Stribley DP, Tinker PB. 1986. The development of endomycorrhizal root systems. VI. The relationship between development of infection, and intensity of infection in young leak roots. New Phytol. 102, 293–301. (10.1111/j.1469-8137.1986.tb00584.x) DOI

Amijee F, Tinker PB, Stribley DP. 1989. The development of endomycorrhizal root systems. VII. A detailed study of effects of soil phosphorus on colonization. New Phytol. 111, 435–446. (10.1111/j.1469-8137.1989.tb00706.x) PubMed DOI

Amijee F, Stribley DP, Tinker PB. 1993. The development of endomycorrhizal root systems. VIII. Effects of soil phosphorus and fungal colonization on the concentration of soluble carbohydrates in roots. New Phytol. 123, 1469–8137. (10.1111/j.1469-8137.1993.tb03739.x) PubMed DOI

Abbott LK, Robson AD, Jasper DA, Gazey C. 1992. What is the role of VA mycorrhizal hyphae in soil? In Mycorrhizas in ecosystems, Wallingford, UK: CAB International.

Sanders FE, Sheikh NA. 1983. The development of vesicular–arbuscular mycorrhizal infection in plant root systems. Plant Soil 71, 223–246. (10.1007/BF02182658) DOI

Bourion V, et al. 2014. Unexpectedly low nitrogen acquisition and absence of root architecture adaptation to nitrate supply in a Medicago truncatula highly branched root mutant. J. Exp. Bot. 65, 2365–2380. (10.1093/jxb/eru124) PubMed DOI PMC

Leitner D, Felderer B, Vontobel P, Schnepf A. 2014. Recovering root system traits using image analysis exemplified by two-dimensional neutron radiography images of lupine. Plant Physiol. 164, 24–35. (10.1104/pp.113.227892) PubMed DOI PMC

Dunbabin VM, et al. 2013. Modelling root–soil interactions using three-dimensional models of root growth, architecture and function. Plant Soil 372, 93–124. (10.1007/s11104-013-1769-y) DOI

Hepper CM. 1985. Influence of age of roots on the pattern of vesicular–arbuscular mycorrhizal infection in leek and clover. New Phytol. 101, 685–693. (10.1111/j.1469-8137.1985.tb02874.x) DOI

Ezawa T, Smith SE, Smith FA. 2002. P metabolism and transport in AM fungi. Plant Soil 244, 221–230. (10.1023/A:1020258325010) DOI

Bago B, Azcón-Aguilar C, Goulet A, Piché Y. 1998. Branched absorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. New Phytol. 139, 375–388. (10.1046/j.1469-8137.1998.00199.x) DOI

Bago B, Cano C, Azcón-Aguilar C, Samson J, Coughlan AP, Piché Y. 2004. Differential morphogenesis of the extraradical mycelium of an arbuscular mycorrhizal fungus grown monoxenically on spatially heterogeneous culture media. Mycologia 96, 452–462. (10.2307/3762165) PubMed DOI

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. (10.1111/j.1469-8137.1990.tb00476.x) PubMed DOI

Vierheilig H, Schweiger P, Brundrett M. 2005. An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiol. Plant. 125, 393–404. (10.1111/j.1399-3054.2005.00564.x) DOI

Thonar C, Erb A, Jansa J. 2012. Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities—marker design, verification, calibration and field validation. Mol. Ecol. Resour. 12, 219–232. (10.1111/j.1755-0998.2011.03086.x) PubMed DOI

Jansa J, Erb A, Oberholzer H-R, Šmilauer P, Egli S. 2014. Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol. Ecol. 23, 2118–2135. (10.1111/mec.12706) PubMed DOI

Carver I, Boswell GP. 2008. A lattice-free model of translocation-induced outgrowth in fungal mycelia. IAENG Int. J. Appl. Math. 38, 173–179.

Meškauskas A, McNulty LJ, Moore D. 2004. Concerted regulation of all hyphal tips generates fungal fruit body structures: experiments with computer visualizations produced by a new mathematical model of hyphal growth. Mycol. Res. 108, 341–353. (10.1017/S0953756204009670) PubMed DOI

Snellgrove RC, Splittstoesser WE, Stribley DP, Tinker PB. 1982. The distribution of carbon and the demand of the fungal symbiont in leek plants with vesicular–arbuscular mycorrhizas. New Phytol. 92, 75–87. (10.1111/j.1469-8137.1982.tb03364.x) DOI

Jakobsen I, Rosendahl L. 1990. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol. 115, 77–83. (10.1111/j.1469-8137.1990.tb00924.x) DOI

Schwab SM, Menge JA, Tinker PB. 1991. Regulation of nutrient transfer between host and fungus in vesicular–arbuscular mycorrhizas. New Phytol. 117, 387–398. (10.1111/j.1469-8137.1991.tb00002.x) PubMed DOI

Jones DL, Hodge A, Kuzyakov Y. 2004. Plant and mycorrhizal regulation of rhizodeposition. New Phytol. 163, 459–480. (10.1111/j.1469-8137.2004.01130.x) PubMed DOI

Vierheilig H. 2004. Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. J. Plant Physiol. 161, 339–341. (10.1078/0176-1617-01097) PubMed DOI

Vierheilig H. 2004. Regulatory mechanisms during the plant–arbuscular mycorrhizal fungus interaction. Can. J. Bot. 82, 1166–1176. (10.1139/B04-015) DOI

Berta G, Fusconi A, Trotta A, Scannerini S. 1990. Morphogenetic modifications induced by the mycorrhizal fungus Glomus strain E3 in the root system of Allium porrum L. New Phytol. 114, 207–215. (10.1111/j.1469-8137.1990.tb00392.x) DOI

Felderer B, Jansa J, Schulin R. 2013. Interaction between root growth allocation and mycorrhizal fungi in soil with patchy P distribution. Plant Soil 373, 569–582. (10.1007/s11104-013-1818-6) DOI

Jakobsen I, Chen B, Munkvold L, Lundsgaard T, Zhu Y-G. 2005. Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant Cell Environ. 28, 928–938. (10.1111/j.1365-3040.2005.01345.x) DOI

Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV. 2015. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol. 205, 1537–1551. (10.1111/nph.13138) PubMed DOI PMC