Evidence that variation in root anatomy contributes to local adaptation in Mexican native maize

Mexican native maize (Zea mays ssp. mays) is adapted to a wide range of climatic and edaphic conditions. Here, we focus specifically on the potential role of root anatomical variation in this adaptation. Given the investment required to characterize root anatomy, we present a machine-learning approach using environmental descriptors to project trait variation from a relatively small training panel onto a larger panel of genotyped and georeferenced Mexican maize accessions. The resulting models defined potential biologically relevant clines across a complex environment that we used subsequently for genotype-environment association. We found evidence of systematic variation in maize root anatomy across Mexico, notably a prevalence of trait combinations favoring a reduction in axial hydraulic conductance in varieties sourced from cooler, drier highland areas. We discuss our results in the context of previously described water-banking strategies and present candidate genes that are associated with both root anatomical and environmental variation. Our strategy is a refinement of standard environmental genome-wide association analysis that is applicable whenever a training set of georeferenced phenotypic data is available

Screening for Staphylococcal Superantigen Genes Shows No Correlation with the Presence or the Severity of Chronic Rhinosinusitis and Nasal Polyposis

BACKGROUND: Staphylococcus aureus secretes numerous exotoxins which may exhibit superantigenic properties. Whereas the virulence of several of them is well documented, their exact biological effects are not fully understood. Exotoxins may influence the immune and inflammatory state of various organs, including the sinonasal mucosa: their possible involvement in chronic rhinosinusitis has been suggested and is one of the main trends in current research. The aim of this study was to investigate whether the presence of any of the 22 currently known staphylococcal exotoxin genes could be correlated with chronic rhinosinusitis. METHODOLOGY/PRINCIPAL FINDINGS: We conducted a prospective, multi-centred European study, analysing 93 Staphylococcus aureus positive swabs taken from the middle meatus of patients suffering from chronic rhinosinusitis, with or without nasal polyposis, and controls. Strains were systematically tested for the presence of the 22 currently known exotoxin genes and genotyped according to their agr groups. No direct correlation was observed between chronic rhinosinusitis, with or without nasal polyposis, and either agr groups or the presence of the most studied exotoxins genes (egc, sea, seb, pvl, exfoliatins or tsst-1). However, genes for enterotoxins P and Q were frequently observed in nasal polyposis for the first time, but absent in the control group. The number of exotoxin genes detected was not statistically different among the 3 patient groups. CONCLUSIONS/SIGNIFICANCE: Unlike many previous studies have been suggesting, we did not find any evident correlation between staphylococcal exotoxin genes and the presence or severity of chronic rhinosinusitis with or without nasal polyposis

In silico analysis of the influence of root hydraulic anatomy on maize (Zea mays) water uptake

For plants and especially for maize (Zea mays), experiencing water deficit at key phenological stages can cause critical yield losses. As such, there is a need to understand the complex plant hydraulic behavior in constraining environments. Within plant diversity, landraces may hold root systems hydraulic architecture that are well fitted to specific pedo-climatic environments. Their sets of traits could be "key" candidates to promote sustainable farming practices and alleviate the consequences of drought episodes. However, due to the difficulties of quantifying the root hydraulic anatomy, there is a knowledge gap in the identification of suitable combinations of root traits. Therefore, developing new ways to explore and evaluate the influence of root hydraulic anatomy on water uptake will be beneficial. In this thesis, we advance our understanding on hydraulic anatomy influence at different scales and for specific soil and environmental constraints. Firstly, we created a new way to estimate root hydraulic properties. Secondly, we developed a method to generate root hydraulic atlases based on a combination of root cross-section images and modeling tools. Then, we investigated in silico the crucial role of root anatomy, subcellular hydraulic properties and maturation stages on water uptake. It showed that the root radii, the contribution of aquaporins to the cell membrane permeability and root maturation rates can create contrasted uptake patterns and influence the cumulative water uptake of in silico maize plants. These exploratory findings inform potential candidate sets of traits which could be investigated furthermore.(AGRO - Sciences agronomiques et ingénierie biologique) -- UCL, 202

GRANAR, a new computational tool to better understand the functional importance of root anatomy

Root hydraulic conductivity is an important determinant of plant water uptake capacity. In particular, the root radial conductivity is often thought to be a limiting factor along the water pathways between the soil and the leaf. The root radial conductivity is itself defined by cell scale hydraulic properties and anatomical features. However, quantifying the influence of anatomical features on the radial conductivity remains challenging due to complex, and time-consuming, experimental procedures. We present a new computation tool, the Generator of Root ANAtomy in R (GRANAR) that can be used to rapidly generate digital versions of root anatomical networks. GRANAR uses a limited set of root anatomical parameters, easily acquired with existing image analysis tools. The generated anatomical network can then be used in combination with hydraulic models to estimate the corresponding hydraulic properties. We used GRANAR to re-analyse large maize (Zea mays) anatomical datasets from the literature. Our model was successful at creating virtual anatomies for each experimental observation. We also used GRANAR to generate anatomies not observed experimentally, over wider ranges of anatomical parameters. The generated anatomies were then used to estimate the corresponding radial conductivities with the hydraulic model MECHA. This enabled us to quantify the effect of individual anatomical features on the root radial conductivity. In particular, our simulations highlight the large importance of the width of the stele and the cortex. GRANAR is an open-source project available here: http://granar.github.io

Combining cross‐section images and modeling tools to create high‐resolution root system hydraulic atlases in Zea mays

Root hydraulic properties play a central role in the global water cycle, in agricultural systems productivity, and in ecosystem survival as they impact the canopy water supply. However, the existing experimental methods to quantify root hydraulic conductivities, such as the root pressure probing, are particularly challenging, and their applicability to thin roots and small root segments is limited. Therefore, there is a gap in methods enabling easy estimations of root hydraulic conductivities in diverse root types. Here, we present a new pipeline to quickly estimate root hydraulic conductivities across different root types, at high resolution along root axes. Shortly, free-hand root cross-sections were used to extract a selected number of key anatomical traits. We used these traits to parametrize the Generator of Root Anatomy in R (GRANAR) model to simulate root anatomical networks. Finally, we used these generated anatomical networks within the Model of Explicit Cross-section Hydraulic Anatomy (MECHA) to compute an estimation of the root axial and radial hydraulic conductivities (kx and kr, respectively). Using this combination of anatomical data and computational models, we were able to create a root hydraulic conductivity atlas at the root system level, for 14-day-old pot-grown Zea mays (maize) plants of the var. B73. The altas highlights the significant functional variations along and between different root types. For instance, predicted variations of radial conductivity along the root axis were strongly dependent on the maturation stage of hydrophobic barriers. The same was also true for the maturation rates of the metaxylem vessels. Differences in anatomical traits along and across root types generated substantial variations in radial and axial conductivities estimated with our novel approach. Our methodological pipeline combines anatomical data and computational models to turn root cross-section images into a detailed hydraulic atlas. It is an inexpensive, fast, and easily applicable investigation tool for root hydraulics that complements existing complex experimental methods. It opens the way to high-throughput studies on the functional importance of root types in plant hydraulics, especially if combined with novel phenotyping techniques such as laser ablation tomography

Creation of high resolution root system hydraulic atlas from root cross-section images and modelling tools

Root hydraulic properties play a central role in the global water cycle, agricultural systems productivity, and ecosystem survival as they impact the global canopy water supply. However, the available experimental methods to quantify root hydraulic conductivities, such as the root pressure probing, are particularly challenging and their applicability on thin roots and small root segments is limited. There is a gap in methods enabling easy estimations of root hydraulic conductivities across a diversity of root types and at high resolution along root axes. In this case study, we analysed Zea mays (maize) plants of the var. B73 that were grown in pots for 14 days. Root cross-section data were used to extract anatomical measurements. We used the Generator of Root Anatomy in R (GRANAR) model to generate root anatomical networks from anatomical features. Then we used the Model of Explicit Cross-section Hydraulic Anatomy (MECHA) to compute an estimation of the root axial and radial hydraulic conductivities (kx and kr, respectively), based on the generated anatomical networks and cell hydraulic properties from the literature. The root hydraulic conductivity maps obtained from the root cross-sections suggest significant functional variations along and between different root types. Predicted variations of kr along the root axis were strongly dependent on the maturation stage of hydrophobic barriers. The same was also true for the maturation rates of the metaxylem. The different anatomical features, as well as their evolution along the root type add significant variation to the kr estimation in between root type and along the root axe. Under the prism of root types, anatomy, and hydrophobic barriers, our results highlight the diversity of root radial and axial hydraulic conductivities, which may be veiled under low-resolution measurements of the root system hydraulic conductivity. While predictions of our root hydraulic maps match the range and trend of measurements reported in the literature, future studies could focus on the quantitative validation of hydraulic maps. From now on, a novel method, which turns root cross-section images into hydraulic maps will offer an inexpensive and easily applicable investigation tool for root hydraulics, in parallel to root pressure probing experiments

Evidence for a multicellular symplasmic water pumping mechanism across vascular plant roots

With global warming, climate zones are projected to shift poleward, and the frequency and intensity of droughts to increase, driving threats to crop production and ecosystems. Plant hydraulic traits play major roles in coping with such droughts, and process-based plant hydraulics (water flowing along decreasing pressure Ψp or total water potential Ψtot gradients) has newly been implemented in land surface models. An enigma reported for the past 35 years is the observation of water flowing along increasing water potential gradients across roots. By combining the most advanced modelling tool from the emerging field of plant micro-hydrology with pioneering cell solute mapping data, we found that the current paradigm of water flow across roots of all vascular plants is incomplete: it lacks the impact of solute concentration (and thus negative osmotic potential Ψo) gradients across living cells. This gradient acts as a water pump as it reduces water tension without loading solutes in plant vasculature (xylem). Importantly, water tension adjustments in roots may have large impacts in leaves due to the tension-cavitation feedback along stems. Here, we mathematically demonstrate the water pumping mechanism by solving water flow equations analytically on a triple-cell system. Then we show that the simplistic upscaled equations hold in 2- and 3-D maize, grapevine and Arabidopsis complex hydraulic anatomies, and that water may flow “uphill” of water potential gradients toward xylem as observed experimentally. Besides its contribution to the fundamental understanding of plant water relations, this study lays new foundations for future multidisciplinary research encompassing plant physiology and ecohydrology, and has the ambition to mathematically capture a keystone process for the accurate forecasting of plant water status in crop models and LSMs

Evidence for a multicellular water pump fueled by symplastic osmotic potential gradients in vascular plant ro

The current paradigm of root radial water flow assumes that water only flows “downhill” of water potential gradients, so that the only way to pump water without lowering xylem relative pressure is by lowering xylem total water potential through solute loading. However, numerous studies report that crops and woody species roots may absorb water despite higher xylem pressure and lower xylem solute concentration, as compared to the root direct environment (i.e. water would flow “uphill” of water potential gradients). This contradicts the current paradigm of root water acquisition, and seemingly goes against the second law of thermodynamics. We recently found a physiological mechanism solving this enigma with a micro-hydrological model of water flow across roots, called MECHA. Osmotic gradients between living cells generate pressure gradients driving water through plasmodesmata, with a surprising result: subcellular flow “downhill” of local water potential gradients may translate into flow “uphill” of both total and pressure potential gradients between root surface and xylem. This water pumping mechanism means any vascular plant may reduce its xylem water tension and increase its water availability beyond predictions of the current theory. Here, we demonstrate of the water pumping mechanism mathematically by solving water flow equations analytically on a triple-cell system. Then we show that the associated upscaled equations hold in 2- and 3-D maize and Arabidopsis hydraulic anatomies, and that water flows “uphill” of water potential gradients toward xylem as observed experimentall

The plant water pump: why water flows uphill of water potential gradients in a root hydraulic anatomy model

Guttation is the exudation of xylem sap from vascular plant leaves. This process is particularly interesting because in its configuration root water uptake occurs against the hydrostatic pressure driving force. Hence, it emphasizes the contribution of another driving force that lifts water in plants: the osmotic potential gradient. The current paradigm of root water uptake explains that, due to the endodermal apoplastic barrier, water flows across root radius from the same principles as through selective membranes: driven by the total water potential gradient. This theory relies on the idea that during guttation, osmolites loaded in xylem vessels decrease xylem total water potential, making it more negative than the total soil water potential, and generating water inflow by osmosis as in an osmometer. However, this theory fails at explaining experiments in which guttation occurs without sufficient solute loading in root xylem of maize (Enns et al., 1998; Enns et al., 2000) and arrowleaf saltbush (Bai et al., 2007) among others; studies concluding that experimental observations “could not be explained with the current theories in plant physiology”. Such flow rates towards combined increasing pressure potentials and increasing osmotic potentials between separate apoplastic compartments would necessitate an effective root radial conductivity that is negative; a mind bender. What piece of hydraulic network would make it possible for water to flow against the total water potential driving force? We implemented Steudle’s composite water transport model in the explicit root cross-section anatomical hydraulic network MECHA (Couvreur et al., 2018). All apoplastic, transmembrane and symplastic pathways are interconnected in the network. The results show that while root radial conductivity is particularly sensitive to cell membrane permeability, the combination of conductive plasmodesmata and increased dilution of protoplast osmotic potentials inwards is a key to explain root water flow towards increasing total potentials. A triple cell theory is suggested as new paradigm of root radial flow

Theoretical evidence for a multicellular water pump fueled by symplastic osmotic potential gradients in vascular plant roots

The current paradigm of root radial water flow assumes that water only flows of water potential gradients, so that the only way to pump water without lowering xylem relative pressure is by lowering xylem total water potential through solute loading. However, numerous studies report that crops and woody species roots may absorb water despite higher xylem pressure and lower xylem solute concentration, as compared to the root direct environment (i.e. water would flow of water potential gradients). This contradicts the current paradigm of root water acquisition, and seemingly goes against the second law of thermodynamics. We recently found a physiological mechanism solving this enigma with a microhydrological model of water flow across roots, called MECHA. Osmotic gradients between living cells generate pressure gradients driving water through plasmodesmata, with a surprising result: subcellular flow of local water potential gradients may translate into flow of both total and pressure potential gradients between root surface and xylem. This water pumping mechanism means any vascular plant may reduce its xylem water tension and increase its water availability beyond predictions of the current theory. Here, we analyse the water pumping mechanism across a simple cell triplet, then show that the associated upscaled equations hold in 2- and 3-D maize and Arabidopsis hydraulic anatomies, and finally draw perspectives on the implications of such a mechanism on cell-to- cell communication across plasmodesmata