Stratégies d'exploration racinaire et cycles des nutriments : Étude du rôle fonctionnel de l'exploration horizontale du sol par les plantes

Plant nutrition depends on complementary mechanisms : the development of root systems, root uptake and plant ability to control nutrient cycling, e.g. through exudation. The aim of this thesis is to link plant-soil feedbacks involving the cycling of nutrients and root foraging strategies. I first review the different mechanisms of plant influence on nutrient cycling within the soil and assess their respective scales. Considering the direct effect of roots on the soil at the scale of the rhizosphere, I hypothesize that the combination of absorption and exudation may lead to synergies between the roots of a plant. At the scale of the whole root system, I propose a second, heuristic hypothesis: the existence of a trade-off between soil exploration and soil occupation (defined as the ability of plants to influence efficiently nutrient cycling). In a first chapter, I develop a general model of nutrient cycling, to determine under which condition plants should limit the exploration of soil by their roots. I show that limited exploration is an efficient strategy under specific conditions, especially nutrient-poor soils and the existence of synergies between roots. In a second chapter, I characterize soil occupation and nitrogen cycling, by the use of isotopes ratios, in the plant-soil system of three perennial grasses of the savanna of Hwange (Zimbabwe). This field study shows a gradient of root heterogeneity among these grass species. Those showing the more heterogeneous root pattern have a slower but potentially more efficient nitrogen cycling. In a last chapter, I develop a numerical mechanistic model at the rhizosphere scale for a plant taking up phosphorus and increasing its availability through exudation of citrate. I show that, depending on the extent of root influence on soil by exudation and nutrient depletion, competition between roots as well as facilitation arise from the combination of root uptake and exudation. By upscaling rhizosphere processes to the root system, I show that phosphorus losses are minimized by a restricted soil exploration, which backs the hypothesis of a trade-off between soil exploration and occupation. Overall, I developed complementary approaches that took into account several mechanisms and scales of plant-soil interactions. Considering that root functions are not limited to nutrient uptake, but also involve their influence on nutrient cycling, lead to two novel results: the potential existence of intra-plant and inter-root facilitation, and limited soil exploration as an efficient foraging strategy. This work underlines the importance of accurately integrating the mechanisms of plant-soil interaction to assess their nutrient strategies and to predict their impact on nutrient cycling within ecosystems.La nutrition minérale des plantes dépend à la fois du développement et du fonctionnement de leur appareil racinaire, incluant l'absorption mais aussi la capacité des plantes à influencer les cycles des nutriments, notamment par l'exsudation. Le but de cette thèse est de lier les rétroactions plantes-sol impliquant les cycles des nutriments aux stratégies d'exploration racinaire. Dans la revue bibliographique, je recense des mécanismes d'interaction plantes-sol et leurs échelles spatiales et temporelles. En considérant, à l'échelle de la rhizosphère, les interactions directes entre racines et sol, je propose que la combinaison entre exsudation et absorption des nutriments mène à des synergies entre racines d'une même plante. Ma seconde hypothèse est celle de l'existence d'un compromis entre l'exploration du sol et son occupation (défini comme la capacité des plantes à influencer efficacement le cycle des nutriments). Dans un premier chapitre, je développe un modèle général de recyclage des nutriments afin de déterminer sous quelles conditions les plantes auraient intérêt à limiter leur exploration du sol. Je montre qu'une exploration limitée est une stratégie de nutrition efficace sous certaines conditions, dont l'existence de synergies entre racines et le fait d'être dans un sol pauvre en nutriment. Dans un deuxième chapitre, je mesure le patron d'exploration racinaire et évalue le recyclage de l'azote à l'aide des outils isotopiques, chez trois espèces de Poacées pérennes de la savane de Hwange (Zimbabwe). Cette étude de terrain montre un gradient d'hétérogénéité racinaire entre ces trois espèces. Les Poacées exprimant le patron d'exploration le plus hétérogène ont un cycle de l'azote plus lent, mais potentiellement plus efficace. Dans un dernier chapitre, je développe un modèle mécaniste à l'échelle de la rhizosphère, pour une plante absorbant le phosphore et contrôlant sa disponibilité par l'exsudation de citrate. Je montre que, selon l'échelle d'influence des racines en terme d'exsudation et d'abaissement de la concentration en phosphore, la combinaison de l'exsudation et de l'absorption mène soit à une compétition, soit à une facilitation entre les racines d'une même plante. En me plaçant à l'échelle du système racinaire, je montre que les pertes en phosphore sont limitées par une exploration limitée du sol. Ce dernier résultat va dans le sens du compromis exploration/occupation. Au cours de cette thèse, j'ai donc développé des approches complémentaires, mettant en jeu différents mécanismes et échelles d'interactions plantes-sol. Le fait que les racines ne se limitent pas à un rôle d'absorption, mais agissent activement sur les cycles de nutriments a mené à deux résultats originaux : la facilitation inter-racinaire et intra-plante, et le fait qu'une exploration limitée puisse être considérée comme une stratégie efficace de nutrition. Enfin, ce travail souligne l'importance d'intégrer les divers mécanismes d'interaction plantes-sol pour comprendre les stratégies de nutrition des plantes et mieux prédire leur impact sur les cycles de nutriments à l'échelle des écosystèmes

Root foraging strategies and nutrient cycling : study on the functional role of the horizontal exploration of soil by plants

La nutrition minérale des plantes dépend à la fois du développement et du fonctionnement de leur appareil racinaire, incluant l'absorption mais aussi la capacité des plantes à influencer les cycles des nutriments, notamment par l'exsudation. Le but de cette thèse est de lier les rétroactions plantes-sol impliquant les cycles des nutriments aux stratégies d'exploration racinaire. Dans la revue bibliographique, je recense des mécanismes d'interaction plantes-sol et leurs échelles spatiales et temporelles. En considérant, à l'échelle de la rhizosphère, les interactions directes entre racines et sol, je propose que la combinaison entre exsudation et absorption des nutriments mène à des synergies entre racines d'une même plante. Ma seconde hypothèse est celle de l'existence d'un compromis entre l'exploration du sol et son occupation (défini comme la capacité des plantes à influencer efficacement le cycle des nutriments). Dans un premier chapitre, je développe un modèle général de recyclage des nutriments afin de déterminer sous quelles conditions les plantes auraient intérêt à limiter leur exploration du sol. Je montre qu'une exploration limitée est une stratégie de nutrition efficace sous certaines conditions, dont l'existence de synergies entre racines et le fait d'être dans un sol pauvre en nutriment. Dans un deuxième chapitre, je mesure le patron d'exploration racinaire et évalue le recyclage de l'azote à l'aide des outils isotopiques, chez trois espèces de Poacées pérennes de la savane de Hwange (Zimbabwe). Cette étude de terrain montre un gradient d'hétérogénéité racinaire entre ces trois espèces. Les Poacées exprimant le patron d'exploration le plus hétérogène ont un cycle de l'azote plus lent, mais potentiellement plus efficace. Dans un dernier chapitre, je développe un modèle mécaniste à l'échelle de la rhizosphère, pour une plante absorbant le phosphore et contrôlant sa disponibilité par l'exsudation de citrate. Je montre que, selon l'échelle d'influence des racines en terme d'exsudation et d'abaissement de la concentration en phosphore, la combinaison de l'exsudation et de l'absorption mène soit à une compétition, soit à une facilitation entre les racines d'une même plante. En me plaçant à l'échelle du système racinaire, je montre que les pertes en phosphore sont limitées par une exploration limitée du sol. Ce dernier résultat va dans le sens du compromis exploration/occupation. Au cours de cette thèse, j'ai donc développé des approches complémentaires, mettant en jeu différents mécanismes et échelles d'interactions plantes-sol. Le fait que les racines ne se limitent pas à un rôle d'absorption, mais agissent activement sur les cycles de nutriments a mené à deux résultats originaux : la facilitation inter-racinaire et intra-plante, et le fait qu'une exploration limitée puisse être considérée comme une stratégie efficace de nutrition. Enfin, ce travail souligne l'importance d'intégrer les divers mécanismes d'interaction plantes-sol pour comprendre les stratégies de nutrition des plantes et mieux prédire leur impact sur les cycles de nutriments à l'échelle des écosystèmes.Plant nutrition depends on complementary mechanisms : the development of root systems, root uptake and plant ability to control nutrient cycling, e.g. through exudation. The aim of this thesis is to link plant-soil feedbacks involving the cycling of nutrients and root foraging strategies. I first review the different mechanisms of plant influence on nutrient cycling within the soil and assess their respective scales. Considering the direct effect of roots on the soil at the scale of the rhizosphere, I hypothesize that the combination of absorption and exudation may lead to synergies between the roots of a plant. At the scale of the whole root system, I propose a second, heuristic hypothesis: the existence of a trade-off between soil exploration and soil occupation (defined as the ability of plants to influence efficiently nutrient cycling). In a first chapter, I develop a general model of nutrient cycling, to determine under which condition plants should limit the exploration of soil by their roots. I show that limited exploration is an efficient strategy under specific conditions, especially nutrient-poor soils and the existence of synergies between roots. In a second chapter, I characterize soil occupation and nitrogen cycling, by the use of isotopes ratios, in the plant-soil system of three perennial grasses of the savanna of Hwange (Zimbabwe). This field study shows a gradient of root heterogeneity among these grass species. Those showing the more heterogeneous root pattern have a slower but potentially more efficient nitrogen cycling. In a last chapter, I develop a numerical mechanistic model at the rhizosphere scale for a plant taking up phosphorus and increasing its availability through exudation of citrate. I show that, depending on the extent of root influence on soil by exudation and nutrient depletion, competition between roots as well as facilitation arise from the combination of root uptake and exudation. By upscaling rhizosphere processes to the root system, I show that phosphorus losses are minimized by a restricted soil exploration, which backs the hypothesis of a trade-off between soil exploration and occupation. Overall, I developed complementary approaches that took into account several mechanisms and scales of plant-soil interactions. Considering that root functions are not limited to nutrient uptake, but also involve their influence on nutrient cycling, lead to two novel results: the potential existence of intra-plant and inter-root facilitation, and limited soil exploration as an efficient foraging strategy. This work underlines the importance of accurately integrating the mechanisms of plant-soil interaction to assess their nutrient strategies and to predict their impact on nutrient cycling within ecosystems

Modelling facilitation or competition within a root system: importance of the overlap of root depletion and accumulation zones

International audienceAims: 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

Explore less to control more: why and when should plants limit the horizontal exploration of soil by their roots?

International audienceIn ecosystems limited by soil nutrients, some plants show a restricted horizontaldistribution of their roots. We explored the hypothesis that this particular pattern is aforaging strategy emerging from trade-offs between soil exploration (that increases the poolof nutrients available for plants) and the local control of nutrient cycling within the soil thatwe call soil occupation. We developed two general analytical models of the cycling of alimiting nutrient in a plant population that is not limited by water. They allowed to explorehow plant productivity is affected when roots do not exploit the whole soil available and todetermine the conditions for which plant nutrient stock is maximized when plants limittheir exploration of soil. We predict that a restricted exploration strategy can be beneficialwhen (1) there is at least one trade-off between a nutrient cycling parameter and soilexploration, (2) nutrient availability in the unexplored soil is poor and (3) the area of soilexplored by plants is stable over time. The exploration limitation strategy results inspatially heterogeneous and nutrient-conservative ecosystems. Our results should applywell to perennial tussock grasses within tropical nutrient-limited ecosystems and raisesinteresting cues for the construction of more sustainable agro-ecosystems. Overall, ourstudy underlines the importance of considering the multiplicity of root-soil interactions andof their scales when considering root foraging strategies

Explore less to control more: why and when should plants limit the horizontal exploration of soil by their roots?

International audienceIn ecosystems limited by soil nutrients, some plants show a restricted horizontaldistribution of their roots. We explored the hypothesis that this particular pattern is aforaging strategy emerging from trade-offs between soil exploration (that increases the poolof nutrients available for plants) and the local control of nutrient cycling within the soil thatwe call soil occupation. We developed two general analytical models of the cycling of alimiting nutrient in a plant population that is not limited by water. They allowed to explorehow plant productivity is affected when roots do not exploit the whole soil available and todetermine the conditions for which plant nutrient stock is maximized when plants limittheir exploration of soil. We predict that a restricted exploration strategy can be beneficialwhen (1) there is at least one trade-off between a nutrient cycling parameter and soilexploration, (2) nutrient availability in the unexplored soil is poor and (3) the area of soilexplored by plants is stable over time. The exploration limitation strategy results inspatially heterogeneous and nutrient-conservative ecosystems. Our results should applywell to perennial tussock grasses within tropical nutrient-limited ecosystems and raisesinteresting cues for the construction of more sustainable agro-ecosystems. Overall, ourstudy underlines the importance of considering the multiplicity of root-soil interactions andof their scales when considering root foraging strategies

Contrasting impacts of grass species on nitrogen cycling in a grazed Sudanian savanna

International audienceWe investigated the impact of perennial and annuals grass species on nitrogen cycling in a Sudanian savanna of Burkina Faso. We also analysed how the local context in terms of grazing and soil properties modifies these impacts. We selected four plots differing both by the intensity of grazing by cattle and soil depth, and used soil and grass biomass 15N as integrative indicators of N cycle. If perennials are able to foster a more efficient nitrogen cycling there should be lower 15N abundances in their biomass and soil. If soil depth and cattle pressure significantly modify nitrogen fluxes, soil depth and cattle pressure should influence 15N signatures. Our results suggest that perennial grasses are more conservative for nitrogen (inhibition of nitrification, less leaching via a perennial root system, slower cycling). The increase in leaf δ15N with N concentration is steeper in Loudetia togoensis than in the three other grasses. No significant difference was found between the 15N signatures of the four plots. Our results on 15N signatures and the fact that perennial grasses are much more abundant in the plots that are less grazed and have deeper soils, confirm that the switch from perennial to annual grasses is linked to a degradation in soil fertility and pasture quality. This suggests that 15N signatures can be used as indicators of fertility

Contrasting impacts of grass species on nitrogen cycling in a grazed Sudanian savanna

International audienceWe investigated the impact of perennial and annuals grass species on nitrogen cycling in a Sudanian savanna of Burkina Faso. We also analysed how the local context in terms of grazing and soil properties modifies these impacts. We selected four plots differing both by the intensity of grazing by cattle and soil depth, and used soil and grass biomass 15N as integrative indicators of N cycle. If perennials are able to foster a more efficient nitrogen cycling there should be lower 15N abundances in their biomass and soil. If soil depth and cattle pressure significantly modify nitrogen fluxes, soil depth and cattle pressure should influence 15N signatures. Our results suggest that perennial grasses are more conservative for nitrogen (inhibition of nitrification, less leaching via a perennial root system, slower cycling). The increase in leaf δ15N with N concentration is steeper in Loudetia togoensis than in the three other grasses. No significant difference was found between the 15N signatures of the four plots. Our results on 15N signatures and the fact that perennial grasses are much more abundant in the plots that are less grazed and have deeper soils, confirm that the switch from perennial to annual grasses is linked to a degradation in soil fertility and pasture quality. This suggests that 15N signatures can be used as indicators of fertility