On the path from xylem hydraulic failure to downstream cell death.

Xylem hydraulic failure (HF) has been identified as a ubiquitous factor in triggering drought-induced tree mortality through the damage induced by the progressive dehydration of plant living cells. However, fundamental evidence of the mechanistic link connecting xylem HF to cell death has not been identified yet. The main aim of this study was to evaluate, at the leaf level, the relationship between loss of hydraulic function due to cavitation and cell death under drought conditions and discern how this relationship varied across species with contrasting resistances to cavitation. Drought was induced by withholding water from potted seedlings, and their leaves were sampled to measure their relative water content (RWC) and cell mortality. Vulnerability curves to cavitation at the leaf level were constructed for each species. An increment in cavitation events occurrence precedes the onset of cell mortality. A variation in cells tolerance to dehydration was observed along with the resistance to cavitation. Overall, our results indicate that the onset of cellular mortality occurs at lower RWC than the one for cavitation indicating the role of cavitation in triggering cellular death. They also evidenced a critical RWC for cellular death varying across species with different cavitation resistance.

The spatial distribution of rhizosphere microbial activities under drought: water availability is more important than root-hair-controlled exudation.

Root hairs and soil water content are crucial in controlling the release and diffusion of root exudates and shaping profiles of biochemical properties in the rhizosphere. But whether root hairs can offset the negative impacts of drought on microbial activity remains unknown. Soil zymography, 14 C imaging and neutron radiography were combined to identify how root hairs and soil moisture affect rhizosphere biochemical properties. To achieve this, we cultivated two maize genotypes (wild-type and root-hair-defective rth3 mutant) under ambient and drought conditions. Root hairs and optimal soil moisture increased hotspot area, rhizosphere extent and kinetic parameters (Vmax and Km ) of ß-glucosidase activities. Drought enlarged the rhizosphere extent of root exudates and water content. Colocalization analysis showed that enzymatic hotspots were more colocalized with root exudate hotspots under optimal moisture, whereas they showed higher dependency on water hotspots when soil water and carbon were scarce. We conclude that root hairs are essential in adapting rhizosphere properties under drought to maintain plant nutrition when a continuous mass flow of water transporting nutrients to the root is interrupted. In the rhizosphere, soil water was more important than root exudates for hydrolytic enzyme activities under water and carbon colimitation.

The role of arbuscular mycorrhizal symbiosis in improving plant water status under drought.

Arbuscular mycorrhizal fungi (AMF) have been presumed to ameliorate crop tolerance to drought. Here, we review the role of AMF in maintaining water supply to plants from drying soils and the underlying biophysical mechanisms. We used a soil-plant hydraulic model to illustrate the impact of several AMF mechanisms on plant responses to edaphic drought. The AMF enhance the soil's capability to transport water and extend the effective root length, thereby attenuating the drop in matric potential at the root surface during soil drying. The synthesized evidence and the corresponding simulations demonstrate that symbiosis with AMF postpones the stress onset limit, which is defined as the disproportionality between transpiration rates and leaf water potentials, during soil drying. The symbiosis can thus help crops survive extended intervals of limited water availability. We also provide our perspective on future research needs and call for reconciling the dynamic changes in soil and root hydraulics in order to better understand the role of AMF in plant water relations in the face of climate changes.

Above and belowground traits impacting transpiration decline during soil drying in 48 maize (Zea mays) genotypes.

BACKGROUND AND AIMS: Stomatal regulation allows plants to promptly respond to water stress. However, our understanding of the impact of above and belowground hydraulic traits on stomatal regulation remains incomplete. The objective of this study was to investigate how key plant hydraulic traits impact transpiration of maize during soil drying. We hypothesize that the stomatal response to soil drying is related to a loss in soil hydraulic conductivity at the root-soil interface, which in turn depends on plant hydraulic traits. METHODS: We investigate the response of 48 contrasting maize (Zea mays) genotypes to soil drying, utilizing a novel phenotyping facility. In this context, we measure the relationship between leaf water potential, soil water potential, soil water content and transpiration, as well as root, rhizosphere and aboveground plant traits. KEY RESULTS: Genotypes differed in their responsiveness to soil drying. The critical soil water potential at which plants started decreasing transpiration was related to a combination of above and belowground traits: genotypes with a higher maximum transpiration and plant hydraulic conductance as well as a smaller root and rhizosphere system closed stomata at less negative soil water potentials. CONCLUSIONS: Our results demonstrate the importance of belowground hydraulics for stomatal regulation and hence drought responsiveness during soil drying. Furthermore, this finding supports the hypothesis that stomata start to close when soil hydraulic conductivity drops at the root-soil interface.

Root hydraulic phenotypes impacting water uptake in drying soils.

Soil drying is a limiting factor for crop production worldwide. Yet, it is not clear how soil drying impacts water uptake across different soils, species, and root phenotypes. Here we ask (1) what root phenotypes improve the water use from drying soils? and (2) what root hydraulic properties impact water flow across the soil-plant continuum? The main objective is to propose a hydraulic framework to investigate the interplay between soil and root hydraulic properties on water uptake. We collected highly resolved data on transpiration, leaf and soil water potential across 11 crops and 10 contrasting soil textures. In drying soils, the drop in water potential at the soil-root interface resulted in a rapid decrease in soil hydraulic conductance, especially at higher transpiration rates. The analysis reveals that water uptake was limited by soil within a wide range of soil water potential (-6 to -1000 kPa), depending on both soil textures and root hydraulic phenotypes. We propose that a root phenotype with low root hydraulic conductance, long roots and/or long and dense root hairs postpones soil limitation in drying soils. The consequence of these root phenotypes on crop water use is discussed.

Root hairs enable high transpiration rates in drying soils.

Do root hairs help roots take up water from the soil? Despite the well-documented role of root hairs in phosphate uptake, their role in water extraction is controversial. We grew barley (Hordeum vulgare cv Pallas) and its root-hairless mutant brb in a root pressure chamber, whereby the transpiration rate could be varied whilst monitoring the suction in the xylem. The method provides accurate measurements of the dynamic relationship between the transpiration rate and xylem suction. The relationship between the transpiration rate and xylem suction was linear in wet soils and did not differ between genotypes. When the soil dried, the xylem suction increased rapidly and non-linearly at high transpiration rates. This response was much greater with the brb mutant, implying a reduced capacity to take up water. We conclude that root hairs facilitate the uptake of water by substantially reducing the drop in matric potential at the interface between root and soil in rapidly transpiring plants. The experiments also reinforce earlier observations that there is a marked hysteresis in the suction in the xylem when the transpiration rate is rising compared with when it is falling, and possible reasons for this behavior are discussed.

Differences in mucilage properties and stomatal sensitivity of locally adapted Zea mays in relation with precipitation seasonality and vapour pressure deficit regime of their native environment.

With ongoing climate change and the increase in extreme weather events, especially droughts, the challenge of maintaining food security is becoming ever greater. Locally adapted landraces of crops represent a valuable source of adaptation to stressful environments. In the light of future droughts-both by altered soil water supply and increasing atmospheric water demand (vapor pressure deficit [VPD])-plants need to improve their water efficiency. To do so, plants can enhance their access to soil water by improving rhizosphere hydraulic conductivity via the exudation of mucilage. Furthermore, plants can reduce transpirational water loss via stomatal regulation. Although the role of mucilage and stomata regulation on plant water management have been extensively studied, little is known about a possible coordination between root mucilage properties and stomatal sensitivity as well as abiotic drivers shaping the development of drought resistant trait suits within landraces. Mucilage properties and stomatal sensitivity of eight Mexican landraces of Zea mays in contrast with one inbred line were first quantified under controlled conditions and second related to water demand and supply at their respective site of origin. Mucilage physical properties-namely, viscosity, contact angle, and surface tension-differed between the investigated maize varieties. We found strong influences of precipitation seasonality, thus plant water availability, on mucilage production (R 2 = .88, p < .01) and mucilage viscosity (R 2 = .93, p < .01). Further, stomatal sensitivity to increased atmospheric water demand was related to mucilage viscosity and contact angle, both of which are crucial in determining mucilage's water repellent, thus maladaptive, behavior upon soil drying. The identification of landraces with pre-adapted suitable trait sets with regard to drought resistance is of utmost importance, for example, trait combinations such as exhibited in one of the here investigated landraces. Our results suggest a strong environmental selective force of seasonality in plant water availability on mucilage properties as well as regulatory stomatal effects to avoid mucilage's maladaptive potential upon drying and likely delay critical levels of hydraulic dysfunction. By this, landraces from highly seasonal climates may exhibit beneficial mucilage and stomatal traits to prolong plant functioning under edaphic drought. These findings may help breeders to efficiently screen for local landraces with pre-adaptations to drought to ultimately increase crop yield resistance under future climatic variability.

Hydraulic conductivity of soil-grown lupine and maize unbranched roots and maize root-shoot junctions.

Improving or maintaining crop productivity under conditions of long term change of soil water availability and atmosphere demand for water is one the big challenges of this century. It requires a deep understanding of crop water acquisition properties, i.e. root system architecture and root hydraulic properties among other characteristics of the soil-plant-atmosphere continuum. A root pressure probe technique was used to measure the root hydraulic conductances of seven-week old maize and lupine plants grown in sandy soil. Unbranched root segments were excised in lateral, seminal, crown and brace roots of maize, and in lateral roots of lupine. Their total hydraulic conductance was quantified under steady-state hydrostatic gradient for progressively shorter segments. Furthermore, the axial conductance of proximal root regions removed at each step of root shortening was measured as well. Analytical solutions of the water flow equations in unbranched roots developed recently and relating root total conductance profiles to axial and radial conductivities were used to retrieve the root radial hydraulic conductivity profile along each root type, and quantify its uncertainty. Interestingly, the optimized root radial conductivities and measured axial conductances displayed significant differences across root types and species. However, the measured root total conductances did not differ significantly. As compared to measurements reported in the literature, our axial and radial conductivities concentrate in the lower range of herbaceous species hydraulic properties. In a final experiment, the hydraulic conductances of root junctions to maize stem were observed to highly depend on root type. Surprisingly maize brace root junctions were an order of magnitude more conductive than the other crown and seminal roots, suggesting potential regulation mechanism for root water uptake location and a potential role of the maize brace roots for water uptake more important than reported in the literature.

Mucilage exudation facilitates root water uptake in dry soils.

As plant roots take up water and the soil dries, water depletion is expected to occur in the rhizosphere. However, recent experiments showed that the rhizosphere was wetter than the bulk soil during root water uptake. We hypothesise that the increased water content in the rhizosphere was caused by mucilage exuded by roots. It is probably that the higher water content in the rhizosphere results in higher hydraulic conductivity of the root-soil interface. In this case, mucilage exudation would favour the uptake of water in dry soils. To test this hypothesis, we covered a suction cup, referred to as an artificial root, with mucilage. We placed it in soil with a water content of 0.03cm3cm-3, and used the root pressure probe technique to measure the hydraulic conductivity of the root-soil continuum. The results were compared with measurements with roots not covered with mucilage. The root pressure relaxation curves were fitted with a model of root water uptake including rhizosphere dynamics. The results demonstrated that when mucilage is added to the root surface, it keeps the soil near the roots wet and hydraulically well conductive, facilitating the water flow from dry soils towards the root surface. Mucilage exudation seems to be an optimal plant trait that favours the capture of water when water is scarce.