Seedling root system adaptation to water availability during maize domestication and global expansion.

The maize root system has been reshaped by indirect selection during global adaptation to new agricultural environments. In this study, we characterized the root systems of more than 9,000 global maize accessions and its wild relatives, defining the geographical signature and genomic basis of variation in seminal root number. We demonstrate that seminal root number has increased during maize domestication followed by a decrease in response to limited water availability in locally adapted varieties. By combining environmental and phenotypic association analyses with linkage mapping, we identified genes linking environmental variation and seminal root number. Functional characterization of the transcription factor ZmHb77 and in silico root modeling provides evidence that reshaping root system architecture by reducing the number of seminal roots and promoting lateral root density is beneficial for the resilience of maize seedlings to drought.

Keep in touch: the soil-root hydraulic continuum and its role in drought resistance in crops.

Drought is a major threat to food security worldwide. Recently, the root-soil interface has emerged as a major site of hydraulic resistance during water stress. Here, we review the impact of soil drying on whole-plant hydraulics and discuss mechanisms by which plants can adapt by modifying the properties of the rhizosphere either directly or through interactions with the soil microbiome.

The effect of root hairs on root water uptake is determined by root-soil contact and root hair shrinkage.

The effect of root hairs on water uptake remains controversial. In particular, the key root hair and soil parameters that determine their importance have been elusive. We grew maize plants (Zea mays) in microcosms and scanned them using synchrotron-based X-ray computed microtomography. By means of image-based modelling, we investigated the parameters determining the effectiveness of root hairs in root water uptake. We explicitly accounted for rhizosphere features (e.g. root-soil contact and pore structure) and took root hair shrinkage of dehydrated root hairs into consideration. Our model suggests that > 85% of the variance in root water uptake is explained by the hair-induced increase in root-soil contact. In dry soil conditions, root hair shrinkage reduces the impact of hairs substantially. We conclude that the effectiveness of root hairs on root water uptake is determined by the hair-induced increase in root-soil contact and root hair shrinkage. Although the latter clearly reduces the effect of hairs on water uptake, our model still indicated facilitation of water uptake by root hairs at soil matric potentials from -1 to -0.1 MPa. Our findings provide new avenues towards a mechanistic understanding of the role of root hairs on water uptake.

Constant hydraulic supply and ABA dynamics facilitate the trade-offs in water and carbon.

Carbon-water trade-offs in plants are adjusted through stomatal regulation. Stomatal opening enables carbon uptake and plant growth, whereas plants circumvent drought by closing stomata. The specific effects of leaf position and age on stomatal behavior remain largely unknown, especially under edaphic and atmospheric drought. Here, we compared stomatal conductance (gs ) across the canopy of tomato during soil drying. We measured gas exchange, foliage ABA level and soil-plant hydraulics under increasing vapor pressure deficit (VPD). Our results indicate a strong effect of canopy position on stomatal behavior, especially under hydrated soil conditions and relatively low VPD. In wet soil (soil water potential > -50 kPa), upper canopy leaves had the highest gs (0.727 ± 0.154 mol m-2 s-1) and assimilation rate (A; 23.4 ± 3.9 µmol m-2 s-1) compared to the leaves at a medium height of the canopy (gs : 0.159 ± 0.060 mol m2 s-1; A: 15.9 ± 3.8 µmol m-2 s-1). Under increasing VPD (from 1.8 to 2.6 kPa), gs , A and transpiration were initially impacted by leaf position rather than leaf age. However, under high VPD (2.6 kPa), age effect outweighed position effect. The soil-leaf hydraulic conductance was similar in all leaves. Foliage ABA levels increased with rising VPD in mature leaves at medium height (217.56 ± 85 ng g-1 FW) compared to upper canopy leaves (85.36 ± 34 ng g-1 FW). Under soil drought (< -50 kPa), stomata closed in all leaves resulting in no differences in gs across the canopy. We conclude that constant hydraulic supply and ABA dynamics facilitate preferential stomatal behavior and carbon-water trade-offs across the canopy. These findings are fundamental in understanding variations within the canopy, which helps in engineering future crops, especially in the face of climate change.

Soil-plant hydraulics explain stomatal efficiency-safety tradeoff.

The efficiency-safety tradeoff has been thoroughly investigated in plants, especially concerning their capacity to transport water and avoid embolism. Stomatal regulation is a vital plant behaviour to respond to soil and atmospheric water limitation. Recently, a stomatal efficiency-safety tradeoff was reported where plants with higher maximum stomatal conductance (gmax ) exhibited greater sensitivity to stomatal closure during soil drying, that is, less negative leaf water potential at 50% gmax (ψgs50 ). However, the underlying mechanism of this gmax -ψgs50 tradeoff remains unknown. Here, we utilized a soil-plant hydraulic model, in which stomatal closure is triggered by nonlinearity in soil-plant hydraulics, to investigate such tradeoff. Our simulations show that increasing gmax is aligned with less negative ψgs50 . Plants with higher gmax (also higher transpiration) require larger quantities of water to be moved across the rhizosphere, which results in a precipitous decrease in water potential at the soil-root interface, and therefore in the leaves. We demonstrated that the gmax -ψgs50 tradeoff can be predicted based on soil-plant hydraulics, and is impacted by plant hydraulic properties, such as plant hydraulic conductance, active root length and embolism resistance. We conclude that plants may therefore adjust their growth and/or their hydraulic properties to adapt to contrasting habitats and climate conditions.

Quantification of root water uptake and redistribution using neutron imaging: a review and future directions.

Quantifying root water uptake is essential to understanding plant water use and responses to different environmental conditions. However, non-destructive measurement of water transport and related hydraulics in the soil-root system remains a challenge. Neutron imaging, with its high sensitivity to hydrogen, has become an unparalleled tool to visualize and quantify root water uptake in vivo. In combination with isotopes (e.g., deuterated water) and a diffusion-convection model, root water uptake and hydraulic redistribution in root and soil can be quantified. Here, we review recent advances in utilizing neutron imaging to visualize and quantify root water uptake, hydraulic redistribution in roots and soil, and root hydraulic properties of different plant species. Under uniform soil moisture distributions, neutron radiographic studies have shown that water uptake was not uniform along the root and depended on both root type and age. For both tap (e.g., lupine [Lupinus albus L.]) and fibrous (e.g., maize [Zea mays L.]) root systems, water was mainly taken up through lateral roots. In mature maize, the location of water uptake shifted from seminal roots and their laterals to crown/nodal roots and their laterals. Under non-uniform soil moisture distributions, part of the water taken up during the daytime maintained the growth of crown/nodal roots in the upper, drier soil layers. Ultra-fast neutron tomography provides new insights into 3D water movement in soil and roots. We discuss the limitations of using neutron imaging and propose future directions to utilize neutron imaging to advance our understanding of root water uptake and soil-root interactions.

Coupled effects of soil drying and salinity on soil-plant hydraulics.

Salinity and soil drying are expected to induce salt accumulation at the root-soil interface of transpiring plants. However, the consequences of this on the relationship between transpiration rate (E) and leaf xylem water potential (ψleaf-x) are yet to be quantified. Here, we used a noninvasive root pressure chamber to measure the E(ψleaf-x) relationship of tomato (Solanum lycopersicum L.) treated with (saline) or without 100-mM NaCl (nonsaline conditions). The results were reproduced and interpreted with a soil-plant hydraulic model. Under nonsaline conditions, the E(ψleaf-x) relationship became progressively more nonlinear as the soil dried (θ ≤ 0.13 cm3 cm-3, ψsoil = -0.08 MPa or less). Under saline conditions, plants exhibited an earlier nonlinearity in the E(ψleaf-x) relationship (θ ≤ 0.15 cm3 cm-3, ψsoil = -0.05 MPa or less). During soil drying, salinity induced a more negative ψleaf-x at predawn, reduced transpiration rate, and caused a reduction in root hydraulic conductance (from 1.48 × 10-6 to 1.30 × 10-6 cm3 s-1 hPa-1). The model suggested that the marked nonlinearity was caused by salt accumulation at the root surface and the consequential osmotic gradients. In dry soil, most water potential dissipation occurred in the bulk soil and rhizosphere rather than inside the plant. Under saline-dry conditions, the loss in osmotic potential at the root surface was the preeminent component of the total dissipation. The physical model of water flow and solute transport supports the hypothesis that a buildup of osmotic potential at the root-soil interface causes a large drop in ψleaf-x and limits transpiration rate under drought and salinity.

The role of root hairs in water uptake: recent advances and future perspectives.

Sufficient water is essential for plant growth and production. Root hairs connect roots to the soil, extend the effective root radius, and greatly enlarge the absorbing surface area. Although the efficacy of root hairs in nutrient uptake, especially phosphorus, has been well recognized, their role in water uptake remains contentious. Here we review recent advances in this field, discuss the factors affecting the role of root hairs in water uptake, and propose future directions. We argue that root hair length and shrinkage, in response to soil drying, explain the apparently contradictory evidence currently available. Our analysis revealed that shorter and vulnerable root hairs (i.e. rice and maize) made little, if any, contribution to root water uptake. In contrast, relatively longer root hairs (i.e. barley) had a clear influence on root water uptake, transpiration, and hence plant response to soil drying. We conclude that the role of root hairs in water uptake is species (and probably soil) specific. We propose that a holistic understanding of the efficacy of root hairs in water uptake will require detailed studies of root hair length, turnover, and shrinkage in different species and contrasting soil textures.

Stomatal closure during water deficit is controlled by below-ground hydraulics.

BACKGROUND AND AIMS: Stomatal closure allows plants to promptly respond to water shortage. Although the coordination between stomatal regulation, leaf and xylem hydraulics has been extensively investigated, the impact of below-ground hydraulics on stomatal regulation remains unknown. METHODS: We used a novel root pressure chamber to measure, during soil drying, the relation between transpiration rate (E) and leaf xylem water pressure (ψleaf-x) in tomato shoots grafted onto two contrasting rootstocks, a long and a short one. In parallel, we also measured the E(ψleaf-x) relation without pressurization. A soil-plant hydraulic model was used to reproduce the measurements. We hypothesize that (1) stomata close when the E(ψleaf-x) relation becomes non-linear and (2) non-linearity occurs at higher soil water contents and lower transpiration rates in short-rooted plants. KEY RESULTS: The E(ψleaf-x) relation was linear in wet conditions and became non-linear as the soil dried. Changing below-ground traits (i.e. root system) significantly affected the E(ψleaf-x) relation during soil drying. Plants with shorter root systems required larger gradients in soil water pressure to sustain the same transpiration rate and exhibited an earlier non-linearity and stomatal closure. CONCLUSIONS: We conclude that, during soil drying, stomatal regulation is controlled by below-ground hydraulics in a predictable way. The model suggests that the loss of hydraulic conductivity occurred in soil. These results prove that stomatal regulation is intimately tied to root and soil hydraulic conductances.

Arbuscular Mycorrhiza Symbiosis Enhances Water Status and Soil-Plant Hydraulic Conductance Under Drought.

Recent studies have identified soil drying as a dominant driver of transpiration reduction at the global scale. Although Arbuscular Mycorrhiza Fungi (AMF) are assumed to play a pivotal role in plant response to soil drying, studies investigating the impact of AMF on plant water status and soil-plant hydraulic conductance are lacking. Thus, the main objective of this study was to investigate the influence of AMF on soil-plant conductance and plant water status of tomato under drought. We hypothesized that AMF limit the drop in matric potential across the rhizosphere, especially in drying soil. The underlying mechanism is that AMF extend the effective root radius and hence reduce the water fluxes at the root-soil interface. The follow-up hypothesis is that AMF enhance soil-plant hydraulic conductance and plant water status during soil drying. To test these hypotheses, we measured the relation between transpiration rate, soil and leaf water potential of tomato with reduced mycorrhiza colonization (RMC) and the corresponding wild type (WT). We inoculated the soil of the WT with Rhizophagus irregularis spores to potentially upsurge symbiosis initiation. During soil drying, leaf water potential of the WT did not drop below -0.8MPa during the first 6days after withholding irrigation, while leaf water potential of RMC dropped below -1MPa already after 4days. Furthermore, AMF enhanced the soil-plant hydraulic conductance of the WT during soil drying. In contrast, soil-plant hydraulic conductance of the RMC declined more abruptly as soil dried. We conclude that AMF maintained the hydraulic continuity between root and soil in drying soils, hereby reducing the drop in matric potential at the root-soil interface and enhancing soil-plant hydraulic conductance of tomato under edaphic stress. Future studies will investigate the role of AMF on soil-plant hydraulic conductance and plant water status among diverse plant species growing in contrasting soil textures.

Soil textures rather than root hairs dominate water uptake and soil-plant hydraulics under drought.

Although the role of root hairs (RHs) in nutrient uptake is well documented, their role in water uptake and drought tolerance remains controversial. Maize (Zea mays) wild-type and its hair-defective mutant (Mut; roothairless 3) were grown in two contrasting soil textures (sand and loam). We used a root pressure chamber to measure the relation between transpiration rate (E) and leaf xylem water potential (ψleaf_x) during soil drying. Our hypotheses were: (1) RHs extend root-soil contact and reduce the ψleaf_x decline at high E in dry soils; (2) the impact of RHs is more pronounced in sand; and (3) Muts partly compensate for lacking RHs by producing longer and/or thicker roots. The ψleaf_x(E) relation was linear in wet conditions and became nonlinear as the soils dried. This nonlinearity occurred more abruptly and at less negative matric potentials in sand (ca. -10 kPa) than in loam (ca. -100 kPa). At more negative soil matric potentials, soil hydraulic conductance became smaller than root hydraulic conductance in both soils. Both genotypes exhibited 1.7 times longer roots in loam, but 1.6 times thicker roots in sand. No differences were observed in the ψleaf_x(E) relation and active root length between the two genotypes. In maize, RHs had a minor contribution to soil-plant hydraulics in both soils and their putative role in water uptake was smaller than that reported for barley (Hordeum vulgare). These results suggest that the role of RHs cannot be easily generalized across species and soil textures affect the response of root hydraulics to soil drying.

Stomatal closure of tomato under drought is driven by an increase in soil-root hydraulic resistance.

The fundamental question as to what triggers stomatal closure during soil drying remains contentious. Thus, we urgently need to improve our understanding of stomatal response to water deficits in soil and atmosphere. Here, we investigated the role of soil-plant hydraulic conductance (Ksp ) on transpiration (E) and stomatal regulation. We used a root pressure chamber to measure the relation between E, leaf xylem water potential (ψleaf-x ) and soil water potential (ψsoil ) in tomato. Additional measurements of ψleaf-x were performed with unpressurized plants. A soil-plant hydraulic model was used to simulate E(ψleaf-x ) for decreasing ψsoil . In wet soils, E(ψleaf-x ) had a constant slope, while in dry soils, the slope decreased, with ψleaf-x rapidly and nonlinearly decreasing for moderate increases in E. The ψleaf-x measured in pressurized and unpressurized plants matched well, which indicates that the shoot hydraulic conductance did not decrease during soil drying and that the decrease in Ksp is caused by a decrease in soil-root conductance. The decrease of E matched well the onset of hydraulic nonlinearity. Our findings demonstrate that stomatal closure prevents the drop in ψleaf-x caused by a decrease in Ksp and elucidate a strong correlation between stomatal regulation and belowground hydraulic limitation.

Mucilage Polysaccharide Composition and Exudation in Maize From Contrasting Climatic Regions.

Mucilage, a gelatinous substance comprising mostly polysaccharides, is exuded by maize nodal and underground root tips. Although mucilage provides several benefits for rhizosphere functions, studies on the variation in mucilage amounts and its polysaccharide composition between genotypes are still lacking. In this study, eight maize (Zea mays L.) genotypes from different globally distributed agroecological zones were grown under identical abiotic conditions in a randomized field experiment. Mucilage exudation amount, neutral sugars and uronic acids were quantified. Galactose (∼39-42%), fucose (∼22-30%), mannose (∼11-14%), and arabinose (∼8-11%) were the major neutral sugars in nodal root mucilage. Xylose (∼1-4%), and glucose (∼1-4%) occurred only in minor proportions. Glucuronic acid (∼3-5%) was the only uronic acid detected. The polysaccharide composition differed significantly between maize genotypes. Mucilage exudation was 135 and 125% higher in the Indian (900 M Gold) and Kenyan (DH 02) genotypes than in the central European genotypes, respectively. Mucilage exudation was positively associated with the vapor pressure deficit of the genotypes' agroecological zone. The results indicate that selection for environments with high vapor pressure deficit may favor higher mucilage exudation, possibly because mucilage can delay the onset of hydraulic failure during periods of high vapor pressure deficit. Genotypes from semi-arid climates might offer sources of genetic material for beneficial mucilage traits.

Transpiration Reduction in Maize (Zea mays L) in Response to Soil Drying.

The relationship between leaf water potential, soil water potential, and transpiration depends on soil and plant hydraulics and stomata regulation. Recent concepts of stomatal response to soil drying relate stomatal regulation to plant hydraulics, neglecting the loss of soil hydraulic conductance around the roots. Our objective was to measure the effect of soil drying on the soil-plant hydraulic conductance of maize and to test whether stomatal regulation avoids a loss of soil-plant hydraulic conductance in drying soils. We combined a root pressure chamber, in which the soil-root system is pressurized to maintain the leaf xylem at atmospheric pressure, with sap flow sensors to measure transpiration rate. The method provides accurate and high temporal resolution measurements of the relationship between transpiration rate and xylem leaf water potential. A simple soil-plant hydraulic model describing the flow of water across the soil, root, and xylem was used to simulate the relationship between leaf water potential and transpiration rate. The experiments were carried out with 5-week-old maize grown in cylinders of 9 cm diameter and 30 cm height filled with silty soil. The measurements were performed at four different soil water contents (WC). The results showed that the relationship between transpiration and leaf water potential was linear in wet soils, but as the soil dried, the xylem tension increased, and nonlinearities were observed at high transpiration rates. Nonlinearity in the relationship between transpiration and leaf water potential indicated a decrease in the soil-plant hydraulic conductance, which was explained by the loss of hydraulic conductivity around the roots. The hydraulic model well reproduced the observed leaf water potential. Parallel experiments performed with plants not being pressurized showed that plants closed stomata when the soil-plant hydraulic conductance decreased, maintaining the linearity between leaf water potential and transpiration rate. We conclude that stomata closure during soil drying is caused by the loss of soil hydraulic conductivity in a predictable way.

Hydraulic processes in roots and the rhizosphere pertinent to increasing yield of water-limited grain crops: a critical review.

HIGHLIGHT: A review of the role of roots in extracting water from the soil with regard to amount and timing leading to maximal grain yield, and of the various mechanisms underlying this.

Root type matters: measurement of water uptake by seminal, crown, and lateral roots in maize.

The ability of plants to take up water from the soil depends on both the root architecture and the distribution and evolution of the hydraulic conductivities among root types and along the root length. The mature maize (Zea mays L.) root system is composed of primary, seminal, and crown roots together with their respective laterals. Our understanding of root water uptake of maize is largely based on measurements of primary and seminal roots. Crown roots might have a different ability to extract water from the soil, but their hydraulic function remains unknown. The aim of this study was to measure the location of water uptake in mature maize and investigate differences between seminal, crown, and lateral roots. Neutron radiography and injections of deuterated water were used to visualize the root architecture and water transport in 5-week-old maize root systems. Water was mainly taken up by crown roots. Seminal roots and their laterals, which were the main location of water uptake in younger plants, made a minor contribution to water uptake. In contrast to younger seminal roots, crown roots were also able to take up water from their most distal segments. The greater uptake of crown roots compared with seminal roots is explained by their higher axial conductivity in the proximal parts and by the fact that they are connected to the shoot above the seminal roots, which favors the propagation of xylem tension along the crown roots. The deeper water uptake of crown roots is explained by their shorter and fewer laterals, which decreases the dissipation of water potential along the roots.

Roots at the percolation threshold.

The rhizosphere is the layer of soil around the roots where complex and dynamic interactions between plants and soil affect the capacity of plants to take up water. The physical properties of the rhizosphere are affected by mucilage, a gel exuded by roots. Mucilage can absorb large volumes of water, but it becomes hydrophobic after drying. We use a percolation model to describe the rewetting of dry rhizosphere. We find that at a critical mucilage concentration the rhizosphere becomes impermeable. The critical mucilage concentration depends on the radius of the soil particle size. Capillary rise experiments with neutron radiography prove that for concentrations below the critical mucilage concentration water could easily cross the rhizosphere, while above the critical concentration water could no longer percolate through it. Our studies, together with former observations of water dynamics in the rhizosphere, suggest that the rhizosphere is near the percolation threshold, where small variations in mucilage concentration sensitively alter the soil hydraulic conductivity. Is mucilage exudation a plant mechanism to efficiently control the rhizosphere conductivity and the access to water?