Linking root structure to functionality: the impact of root system architecture on citrate‐enhanced phosphate uptake

Fletcher, Daniel McKay; Ruiz, Siul; Dias, Tiago Gerheim Souza; Petroselli, Chiara; Roose, Tiina

doi:10.1111/nph.16554

Cited by 53 publications

(36 citation statements)

References 52 publications

(116 reference statements)

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“…The fact that we observed HR in a shallowrooted herbaceous plant (tomato) suggests that the mismatch of resources rather than climate and plant type are the primary drivers of HR. Increasing water uptake is not necessarily the primary function of HR, as has been postulated elsewhere (Ghezzehei and Albalasmeh, 2015;Carminati et al, 2016;Meinzer et al, 2004). Indeed, our observations of root zone water dynamics (Fig.…”

Section: Broader Implications Of Findingssupporting

confidence: 63%

“…7d. Decline in HR magnitude has been previously attributed to the loss of hydraulic conductance in soil-plant systems (Meinzer et al, 2004;Prieto et al, 2010;Scholz et al, 2008). At first glance, this observation appears to contradict the commonplace observation of rapid and spontaneous imbibition during infiltration into dry soils.…”

Section: Facilitation Of Hrmentioning

confidence: 88%

“…The magnitude of the HR flux was defined as the water flux released from the root surface to the soil (mm/d). The gain in volumetric water content was calculated by subtracting the minimum daily root zone water content from the subsequent daily maximum values (Meinzer et al, 2004). The volumetric water content was then scaled to an equivalent soil moisture depth by multiplying it by the thickness of the layer where the roots were concentrated.…”

Section: Soil Hydraulic Properties and Fluxesmentioning

confidence: 99%

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Root uptake under mismatched distributions of water and nutrients in the root zone

2020

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Abstract. Most plants derive their water and nutrient needs from soils where the resources are often scarce, patchy, and ephemeral. It is not uncommon for plant roots to encounter mismatched patches of water-rich and nutrient-rich regions in natural environments. Such an uneven distribution of resources necessitates plant reliance on strategies for exploring and acquiring nutrients from relatively dry patches. We conducted a laboratory study that elucidates the biophysical mechanisms that enable this adaptation. The roots of tomato (Solanum lycopersicum) seedlings were laterally split and grown in two adjacent, hydraulically disconnected pots, which permitted precise control of water and nutrient applications to each compartment. We observed that the physical separation of water-rich and nutrient-rich compartments (one received 90 % water and 0 % nutrients and the other received 10 % water and 100 % nutrients) does not significantly stunt plant growth and productivity compared to two control treatments (control 1: 90 % water and 100 % nutrients versus 10 % water and 0 % nutrients; control 2: 50 % water and 50 % nutrients in each compartment). Specifically, we showed that soil dryness does not reduce nutrient uptake, vegetative growth, flowering, and fruiting compared to control treatments. We identified localized root proliferation in nutrient-rich dry soil patches as a critical strategy that enabled nutrient capture. We observed nocturnal rewetting of the nutrient-rich but dry soil zone (10 % water and 100 % nutrients) but not in the nutrient-free and dry zone of the control experiment (90 % water and 100 % nutrients). We interpreted the rewetting as the transfer of water from the wet to dry zones through roots, a process commonly known as hydraulic redistribution (HR). The occurrence of HR likely prevents the nutrient-rich soil from drying due to permanent wilting and the subsequent decline of root functions. Sustaining rhizosphere wetness is also likely to increase nutrient mobility and uptake. Lack of HR in the absence of nutrients suggests that HR is not entirely a passive, water-potential-gradient driven flow. The density and size of root hairs appeared to be higher (qualitative observation) in the nutrient-rich and dry compartments than in the nutrient-free and dry compartments. We also observed organic coating on sand grains in the rhizosphere of the nutrient-rich and dry compartments. The observations are consistent with prior observations that root hairs and rhizodeposition aid rhizosphere wetting. These findings were synthesized in a conceptual model that explains how plants of dry regions may be adapted to mismatched resources. This study also suggests that separating the bulk of applied nutrients from the frequently irrigated soil region can increase nutrient use efficiency and curtail water pollution from intensive agricultural systems.

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Section: Broader Implications Of Findingssupporting

confidence: 63%

Section: Facilitation Of Hrmentioning

confidence: 88%

Section: Soil Hydraulic Properties and Fluxesmentioning

confidence: 99%

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Root uptake under mismatched distributions of water and nutrients in the root zone

2020

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“…One important difference to batch experiments is the MD membrane acting as an additional sink for dissolved P that competes with chelating species, adsorbing surfaces (Barrow, 2017), and microbial uptake (Schneider et al, 2017). In such a far-from equilibrium dynamic, each single interacting citrate molecule can mobilize a phosphate whose fate is determined by the spatial arrangement of sinks and the diffusion speed (McKay Fletcher et al, 2020). The probability of a dissolved P to reach the MD surface decreases by both diffusion time and the number of opportunities to be reimmobilized.…”

Section: Phosphate Mobilizationmentioning

confidence: 99%

The Cumulative Amount of Exuded Citrate Controls Its Efficiency to Mobilize Soil Phosphorus

Schack‐Kirchner

Loew

Lang

2020

Front. For. Glob. Change

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Root exudation of citrate is discussed as mechanism to mobilize P from the soils' solid phase. Microbial processes can mitigate the mobilization efficiency of citrate. Due to higher microbial activity in topsoils compared to subsoils, we hypothesized a lower mobilization efficiency of exuded citrate in topsoils than in the subsoils. As a model system we used microdialysis (MD) probes and we followed diffusive fluxes of citrate from the perfusate into the soil and of phosphate from the soil into the dialysate in three soil horizons (Oa, Ah, Bw) of a Fagus sylvatica L. stand Cambisol. Three different MD perfusates with a KCl background concentration have been used: control, 1, and 3 mmol L−1 citric acid. Fluxes have been measured after 24, 48, and 144 h. The high-citrate perfusate increased the cumulative 144 h P-influx by a factor of 8, 13, and 113 in the Oa, Ah, and Bw horizon, respectively. With the high-citrate treatment, P mobilization efficiency decreased over time, whereas for the low citrate, P mobilization efficiency had a maximum at day 2. Minimum P mobilization efficiency of citrate was 1:25,000 mol phosphate per mol citrate in the Oa horizon between days 2 and 6, and maximum was 1:286 in the Bw-horizon during day 2. An increasing citrate efflux over time indicated an increasing sink term for citrate in the soil due to microbial decay or immobilization processes. Cumulative phosphate influx could be fitted to cumulative citrate efflux and soil horizon in a logarithmic model explaining 87% of the variability. For the first time, we could follow the localized P-uptake with citrate exudation over several days. Cumulative citrate efflux as the main control of P-mobilization has been barely discussed yet, however, it could explain some gaps in the role of carboxylates in the rhizosphere. Batch experiments are not capable to elucidate microscale dynamic competition for phosphate and carboxylates. MD is a promising tool for spatially explicit investigation of phosphate–citrate exchange, since such detailed insights in are not possible with batch experiments. In combination with the analysis of microbial properties, this technique has a huge potential to identify mobilization processes in soils as induced by citrate.

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“…In general, the model‐based characterization of ARZ processes exists in a fragmented form. Previously, high‐resolution models described root behavior in detail, as is the case with many root architecture models (Godin, 2000; McKay Fletcher et al., 2020), or roots were either crudely represented or are represented as nondynamic factors in global‐scale models (Finzi et al., 2015), as is the case with many ecohydrologic models (Perveen et al., 2014). ARZ processes, such as microbially mediated N cycling, soil C turnover, and respiration, are important components in global climate and landscape‐scale geochemical models, and inaccuracy therein has been at least partly attributed to the absence of or limited or simplified characterization of ARZ components, such as root exudation (Ficken & Warren, 2019; Hinsinger et al., 2011).…”

Section: Introductionmentioning

confidence: 99%

Modeling the Role of Root Exudation in Critical Zone Nutrient Dynamics

Roque‐Malo

Woo

2020

Water Resources Research

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The multifaceted interface of plant roots, microbes, water, and soil can be considered a critical zone within the Critical Zone as it is host to many important dynamically linked processes, including the promotion of nutrient cycling through absorption and rhizodeposition, interaction and feedbacks with microorganisms and fungi, root‐facilitated hydraulic redistribution, and soil carbon dynamics. Such important processes in the Critical Zone have not been fully characterized and modeled in an ecohydrologic framework linking above‐ground natural and/or anthropogenic processes to below‐ground biogeochemical cycling. Specifically, the relation between root exudates and nutrient cycling remains an open challenge. Here we present the model REWT (Root Exudation in Watershed‐scale Transport) to demonstrate the systematic modeling of root exudation in an interconnected ecohydrologic framework. REWT incorporates an explicit dynamic root exudation transport model, nutrient absorption, and coupled microbial processes within the framework of a validated ecohydrologic model. Model simulations demonstrate the influence of root exudation of glucose, a polysaccharide that serves as fuel for microbes, and flavonoids, which can act as a biological nitrification inhibitor on microbial processes linked to soil carbon and nitrogen cycling. To demonstrate the capabilities of this theoretical framework, we parameterize REWT for corn and soybean crops in the Midwestern United States, and simulations indicate that rates of nitrification and respiration were substantially altered compared to model simulations in which root exudation was not explicitly included. This work demonstrates the importance of systematically incorporating root exudates into hydrobiogeochemical models and can serve to inform experimental design for active root zone processes.

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Linking root structure to functionality: the impact of root system architecture on citrate‐enhanced phosphate uptake

Cited by 53 publications

References 52 publications

Root uptake under mismatched distributions of water and nutrients in the root zone

Root uptake under mismatched distributions of water and nutrients in the root zone

The Cumulative Amount of Exuded Citrate Controls Its Efficiency to Mobilize Soil Phosphorus

Modeling the Role of Root Exudation in Critical Zone Nutrient Dynamics

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