Roots induce hydraulic redistribution to promote nutrient uptake and nutrient cycling in nutrient-rich but dry near-surface layers

Abstract. The rhizosphere is an exclusive passage for water and nutrients from the bulk soil to the whole plant. As such, its importance significantly outweighs the limited volume it represents. Numerous recent experimental and modeling studies have shown that plants invest considerable resources in modifying this region. However, roots must also balance the significant differences in resource availability in the vast soil volume they inhabit. Studies suggest that hydraulic redistribution by roots helps counterbalance the large differences in water status experienced by roots. In addition, experimental evidence suggests that hydraulic redistribution plays a role in mitigating drought effects and aiding nutrient uptake. However, whether hydraulic redistribution is a passive happy accident or a process controlled by plants remains unclear. Here, we present a novel mathematical model that integrates rhizosphere-scale modification of soil hydraulic properties by root exudation with long-distance interaction between roots that occupy disparately resourced soil regions. The model reproduces several known phenomena. First, hydraulic redistribution is proportional to the hydraulic gradient between wet and dry regions. Its magnitude substantially increases with the accumulation of hydrophilic rhizodeposits in the rhizosphere of the dry region. However, its effect on net water uptake by the whole root system is meager, negating the current hypotheses that hydraulic redistribution helps mitigate drought. Second, hydraulic redistribution facilitates nutrient uptake. We observed that periodic rewetting of nutrient-rich but dry soil layers significantly increases the active uptake of soluble nutrients. Moreover, cyclic rewetting of the rhizosphere increases the mineralization of the organic matter, thereby releasing nutrients locked in soil organic matter. The latter is another mechanism that supports the well-known phenomenon of priming of organic matter mineralization by root exudation. Overall, our model supports a hypothesis that roots faced with nutrient and organic matter accumulation in unfavorably dry soil regions facilitate hydraulic redistribution via exudation and benefit from the increased nutrient uptake and mineralization rate. These mechanisms could crucial role in determining whether plants can adapt to shifts in resource distributions under a changing climate.