Abstract
Aims
The concept of intra-plant, inter-root competition considers the overlap of nutrient depletion zones around roots, but neglects the spatial pattern of root exudates that can increase nutrient availability. We tested the hypothesis that interactions between nutrient accumulation zones due to exudation by different roots can lead to intra-plant inter-root facilitation.
Methods
We used the PARIS model (Raynaud et al. 2008) to simulate phosphorus uptake by a population of roots that are able to increase phosphorus availability by exuding citrate. We carried out several simulations with the same parameters but with increasing root density in order to study out if changes in root densities would alter nutrient uptake per unit root.
Results
Emerging relationships between root uptake efficiency and root length density indicated cases of inter-root competition or facilitation. The sizes of the accumulation and depletion zones were calculated to explain these results. Our simulations showed a continuum between cases of inter-root competition and facilitation. Facilitation occurred at low exudation rates, when phosphorus supply was not saturated within the phosphorus depletion zone surrounding roots. Low exudation systems led to a lower phosphorus uptake per unit root length, but minimized phosphorus losses in the process.
Conclusions
Based on our model, we derived conditions that allowed predicting whether competition, facilitation or no interaction, is the dominant interaction between roots within a root system, based on the different distances to which an isolated root alters P concentration and supply.
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References
Barber SA, Cushman JH (1981) Nutrient uptake model for agronomic crops. In: Iskander IK (ed) Modelling wastewater renovation land treatment. Wiley, New York, pp 382–409
Boudsocq S, Barot S, Loeuille N (2011) Evolution of nutrient acquisition: when adaptation fills the gap between contrasting ecological theories. P Roy Soc B-Biol Sci 278:449–457
Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125
Cahill JF, McNickle GG (2011) The behavioral ecology of nutrient foraging by plants. Annu Rev Ecol Evol Syst 42:289–311
Callaway RM, Brooker R, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET et al (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848
Chapman SK, Langley JA, Hart SC, Koch GW (2006) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169:27–34
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
Craine JM, Fargione JE, Sugita S (2005) Supply pre-emption, not concentration reduction, is the mechanism of competition for nutrients. New Phytol 166:933–940
Dakora F, Phillips D (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47
Dijkstra FA, Cheng W (2007) Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecol Lett 10:1046–1053
Doussan C, Pagès L, Pierret A (2003) Soil exploration and resource acquisition by plant roots: an architectural and modelling point of view. Agronomie 23:419–431
Dunbabin VM, Postma JA, Schnepf A (2013) Modelling root–soil interactions using three–dimensional models of root growth, architecture and function. Plant Soil 372:93–124
Ge Z, Rubio G, Lynch JP (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant Soil 218:159–171
Gignoux J, Davies ID, Hill DRC (2005) 3Worlds: a new platform for simulating ecological systems. 1st open international conference on modelling and simulation, Clermont-Ferrand, pp. 49–64
Gignoux J, Davies ID, Flint SR, Zucker J-D (2011) The ecosystem in practice: interest and problems of an old definition for constructing ecological models. Ecosystems 14:1039–1054
Gruntman M, Novoplansky A (2004) Physiologically mediated self/non-self discrimination in roots. Proc Nat Acad Sci USA 101:3863–3867
Haefner JW (2005) Modeling biological systems: principles and applications, 2nd edn. Springer Science & Business Media, New York, pp 475
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
Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24
Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187
Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257
Kéfi S, Van Baalen M, Rietkerk M, Loreau M (2008) Evolution of local facilitation in arid ecosystems. Am Nat 172:1–17
Kirk GJD, Santos EE, Findenegg GR (1999a) Phosphate solubilization by organic anion excretion from rice (Oryza sativa L.) growing in aerobic soil. Plant Soil 211:11–18
Kirk GJD, Santos EE, Santos MB (1999b) Phosphate solubilization by organic anion excretion from rice growing in aerobic soil: rates of excretion and decomposition, effects on rhizosphere pH and effects on phosphate availability and uptake. New Phytol 142:185–200
Lata J-C, Degrange V, Raynaud X, Maron P-A, Lensi R, Abbadie L (2004) Grass populations control nitrification in savanna soils. Funct Ecol 18:605–611
Li L, Li SM, Sun J-H, Bao X-G, Zhang H-G, Zhang F (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus deficient soils. Proc Nat Acad Sci USA 104:11192–11196
Lin Y, Berger U, Grimm V, Ji Q (2012) Differences between symmetric and asymmetric facilitation matter: exploring the interplay between modes of positive and negative plant interactions. J Ecol 100:1482–1491
Loague K (1992) Soil water content at R-5. Part 1. Spatial and temporal variability. J Hydrol 139:233–251
Loeuille N, Barot S, Georgelin E, Kylafis G, Lavigne C (2013) Eco-evolutionary dynamics of agricultural networks: implications for sustainable management. Adv Ecol Res 49:339–435
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56
McNickle GG, St Clair CC, Cahill JF (2009) Focusing the metaphor: plant root foraging behaviour. Trends Ecol Evol 24:419–426
Nielsen KL, Lynch JP, Jablokow AG, Curtis PS (1994) Carbon cost of root systems: an architectural approach. Plant Soil 165:161–169
O’Brien EE, Brown JS (2008) Games roots play: effects of soil volume and nutrients. J Ecol 96:438–446
O’Reilly RC, Beck JM (2006) A family of large-stencil discrete Laplacian approximations in three dimensions. Int J Numer Meth Engineer:1–16
Oburger E, Jones DL, Wenzel WW (2011) Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil. Plant Soil 341:363–382
Olesen T, Moldrup P, Yamaguchi T, Rolston DE (2001) Constant slope impedance factor model for predicting the solute diffusion coefficient in unsaturated soil. Soil Sci 166:89–96
Pagès L (2011) Links between root developmental traits and foraging performance. Plant Cell Environ 34:1749–1760
de Parseval H, Abbadie L, Barot S, Gignoux J, Lata J-C, Raynaud X (2016) Explore less to control more: why and when should plants limit the horizontal exploration of soil by their roots? Oikos 125:1110–1120
Press WH, Teukoisky SA, Vetterling WT, Flannery BP, Teukolsky S (2007) Numerical Recipes. The Art ofScientific Computing. 3rd edn. Cambridge University Press, New York, pp 1235
Ptashnyk M, Roose T, Jones DL, Kirk GJD (2011) Enhanced zinc uptake by rice through phytosiderophore secretion: a modelling study. Plant Cell Environ 34:2038–2046
Raynaud X (2010) Soil properties are key determinants for the development of exudate gradients in a rhizosphere simulation model. Soil Biol Biochem 42:210–219
Raynaud X, Leadley PW (2004) Soil characteristics play a key role in modelling nutrient competition in plant communities. Ecology 85:2200–2214
Raynaud X, Lata J-C, Leadley PW (2006) Soil microbial loop and nutrient uptake by plants: a test using a coupled C:N model of plant–microbial interactions. Plant Soil 287:95–116
Raynaud X, Jaillard B, Leadley PW (2008) Plants may alter competition by modifying nutrient bioavailability in rhizosphere: a modeling approach. Am Nat 171:44–58
van Rees KCJ, Comerford NB, Rao PSC (1990) Defining soil buffer power: implications for ion diffusion and nutrient uptake modelling. Soil Sci Soc Am J 54:1505–1507
Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301
Robinson D, Hodge A, Griffiths BS, Fitter AH (1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proc Roy Soc B-Biol Sci 266:431–435
Rubio G, Walk T, Ge Z, Yan X, Liao H, Lynch JP (2001) Root gravitropism and below-ground competition among neighbouring plants: a modelling approach. Ann Bot 88:929–940
Schnepf A, Leitner D, Klepsch S (2012) Modeling phosphorus uptake by a growing and exuding root system. Vadose Zone J. doi:10.2136/vzj2012.0001
Shahzad T, Chenu C, Genet P, Barot S, Perveen N, Mougin C, Fontaine S (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155
Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125
Shane MW, Cawthray GR, Cramer MD, Kuo J, Lambers H (2006) Specialized “dauciform” roots of Cyperaceae are structurally distinct, but functionally analogous with “cluster” roots. Plant Cell Environ 29:1989–1999
Subbarao GV, Rondon M, Ito O, Ishikawa T, Rao IM, Nakahara KI, Lascano CE, Berry WL (2006) Biological nitrification inhibition (BNI) - is it a widespread phenomenon? Plant Soil 294:5–18
Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, Oxford, p 444
Vanysek P (2000) Ionic conductivity and diffusion at infinite dilution. In: Lide DR (ed) CRC handbook of chemistry and physics (90th edition). Taylor and Francis, Boca Raton, pp 1–3
Williams M, Yanai RD (1996) Multi-dimensional sensitivity analysis and ecological implication of a nutrient uptake model. Plant Soil 180:311–324
York LM, Carminati A, Mooney SJ, Ritz K, Bennett MJ (2016) The holistic rhizosphere: integrating zones, processes, and semantics in the soil influenced by roots. J Exp Bot 67:3629–3643
Zygalakis KC, Roose T (2012) A simple mathematical model for investigating the effect of cluster roots on plant nutrient uptake. Eur Phys J-Spec Top 204:103–118
Acknowledgements
We thank Shayne Flint and Ian Davies for their help in designing the model on 3Worlds. We thank Eric Lateltin and reviewers for constructive comments on earlier versions of the manuscript. This work was supported by the French Agence Nationale de la Recherche, grant number ANR-07-CIS7-001 (3Worlds project).
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de Parseval, H., Barot, S., Gignoux, J. et al. Modelling facilitation or competition within a root system: importance of the overlap of root depletion and accumulation zones. Plant Soil 419, 97–111 (2017). https://doi.org/10.1007/s11104-017-3321-y
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DOI: https://doi.org/10.1007/s11104-017-3321-y