Going with the Flow: Multiscale Insights into the Composite Nature of Water Transport in Roots

Couvreur, Valentin; Faget, Marc; Lobet, Guillaume; Javaux, Mathieu; Chaumont, François; Draye, Xavier

doi:10.1104/pp.18.01006

Cited by 73 publications

(98 citation statements)

References 74 publications

(109 reference statements)

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“…Therefore, to reduce the number of unknowns, we kept the flow domain as simple as possible, but complex enough to include the two pathways, their exchange and the role of the endodermis. Recently, Couvreur et al 3 www.nature.com/scientificreports www.nature.com/scientificreports/ coefficients did not vary between day and night. However, the diffusion coefficient of the membrane might change in response to varying aquaporin activity.…”

Section: Discussionmentioning

confidence: 98%

Root water uptake and its pathways across the root: quantification at the cellular scale

Zarebanadkouki¹,

Trtik

Hayat³

et al. 2020

Preprint

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The pathways of water across root tissues and their relative contribution to plant water uptake remain debated. This is mainly due to technical challenges in measuring water flux non-invasively at the cellular scale under realistic conditions.&#160; We developed a new method to quantify water fluxes inside roots growing in soils. The method combines spatiotemporal quantification of deuterated water distribution imaged by rapid neutron tomography with an inverse simulation of water transport across root tissues. Using this non-invasive technique, we estimated for the first time the in-situ radial water fluxes [m s-1] in apoplastic and cell-to-cell pathways. The water flux in the apoplast of twelve days-old lupins (Lupinus albus L. cv. Feodora) was seventeen times faster than in the cell-to-cell pathway. Hence, the overall contribution of the apoplast in water flow [m3 s-1] across the cortex is, despite its small volume of 5%, as large as 57&#177;8 % (Mean &#177; SD for n=3) of the total water flow. This method is suitable to non-invasively measure the response of cellular scale root hydraulics and water fluxes to varying soil and climate conditions.

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Section: Discussionmentioning

confidence: 98%

Root water uptake and its pathways across the root: quantification at the cellular scale

Zarebanadkouki¹,

Trtik

Hayat³

et al. 2020

Preprint

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“…Other future applications could be the coupling of our detailed PD level calculations of effective symplasmic permeability with tissue level models, which would allow for investigating the impact of microscopic changes on developmental and physiological processes, e.g., see ( Foster and Miklavcic, 2017 ; Couvreur et al, 2018 ). Depending on the context, it would then be useful or even required to also implement hydrodynamic flow through the PDs.…”

Section: Discussionmentioning

confidence: 99%

“…Computational modelling approaches have been applied to model PD transport but, so far, these have mainly focused on hydrodynamic flow and the specific tissues where that matters ( Blake, 1978 ; Bret-Harte and Silk, 1994 ; Jensen et al, 2012 ; Ross-Elliott et al, 2017 ; Comtet et al, 2017 ; Foster and Miklavcic, 2017 ; Couvreur et al, 2018 ). The few existing studies on diffusive transport do not consider neck constrictions or the approach to PDs from the cytoplasmic bulk.…”

Section: Introductionmentioning

confidence: 99%

“…The few existing studies on diffusive transport do not consider neck constrictions or the approach to PDs from the cytoplasmic bulk. Most models consider PDs as straight channels, with advective/diffusive transport through an unobstructed cytosolic sleeve and typically, but not always, account for reduced diffusivity inside these narrow channels compared to the cytosol ( Bret-Harte and Silk, 1994 ; Liesche and Schulz, 2013 ; Dölger et al, 2014 ; Ross-Elliott et al, 2017 ; Couvreur et al, 2018 ). Only the oldest of this set, Blake ( 1978 ), uses a dilated central region in its calculations, but is entirely focused on hydrodynamics.…”

Section: Introductionmentioning

confidence: 99%

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From plasmodesma geometry to effective symplasmic permeability through biophysical modelling

Deinum¹,

Benitez‐Alfonso

Mulder

2019

Preprint

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11Regulation of molecular transport via intercellular channels called plasmodesmata (PDs) is 12 important for both coordinating developmental and environmental responses among 13 neighbouring cells, and isolating (groups of) cells to execute distinct programs. Cell-to-cell mobility 14 of fluorescent molecules and PD dimensions (measured from electron micrographs) are both used 15 as methods to predict PD transport capacity (i.e., effective symplasmic permeability), but often yield 16 very different values. Here, we build a theoretical bridge between both experimental approaches 17 by calculating the effective symplasmic permeability from a geometrical description of individual 18 PDs and considering the flow towards them. We find that a dilated central region has the strongest 19 impact in thick cell walls and that clustering of PDs into pit fields strongly reduces predicted 20 permeabilities. Moreover, our open source multi-level model allows to predict PD dimensions 21 matching measured permeabilities and add a functional interpretation to structural differences 22 observed between PDs in different cell walls. 23 24 51 are embryo or seedling lethal, highlighting the importance of these structures for normal plant 52 development (Kim et al., 2002; Benitez-Alfonso et al., 2009; Xu et al., 2012). 53 Small molecules can move via PD by diffusion (non-targeted transport). This is considered to 54 be predominantly symmetrical (Schönknecht et al., 2008; Maule, 2008), while in certain tissues, 55 such as secreting trichomes (Waigmann and Zambryski, 1995; Gunning and Hughes, 1976) and the 56 phloem (Ross-Elliott et al., 2017;Comtet et al., 2017), hydrodynamic flow may create directionality. 57 The maximum size of molecules that can move by this generic "passive" pathway is often referred to 58 2 of 38 Manuscript submitted to eLife as the "size exclusion limit" (SEL), which obviously depends on PD properties and structural features 59 (Dashevskaya et al., 2008). Large molecules can move through PD via an ''active" or "targeted" 60 pathway overriding the defined SEL. This may involve additional factors that temporarily modify 61 these substrates, target them to the PDs, or induce transient modifications of the PDs to allow for 62 the passage of larger molecules in a highly substrate dependent fashion (Zambryski and Crawford, 63 2000; Maule et al., 2011). 64 Computational modelling approaches have been applied to model PD transport but, so far, 65 these have mainly focused on hydrodynamic flow and the specific tissues where that matters (Blake, 66 1978; Bret-Harte and Silk, 1994; Jensen et al., 2012; Ross-Elliott et al., 2017; Comtet et al., 2017; 67 Foster and Miklavcic, 2017; Couvreur et al., 2018). The few existing studies on diffusive transport 68 do not consider neck constrictions or the approach to PDs from the cytoplasmic bulk. Most models 69 consider PDs as straight channels, with advective/diffusive transport through an unobstructed 70 cytosolic sleeve and typically, but not always, accou...

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“…At a finer scale, on the organ level, radial and axial conductivities can also be defined by hydraulic and structural properties. On the hydraulic side, the radial conductivity (k r ) of a root segment is influenced by the expression and location of water channels 5 , the formation of hydrophobic barriers 6 , and the conductivity of plasmodesmata 7 . On the structural side, the k r is known to be influenced by anatomical features, such as the number of cell layers in the cortex 8 , the size of cortex cells 9 , or the presence of aerenchyma 10 .…”

Section: Introductionmentioning

confidence: 99%

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

Heymans

Couvreur

LaRue

et al. 2019

Preprint

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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. Heymans et al. 2019 -GRANAR -A Generator of Root ANAtomy in R -Preprint 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 Keywords Root anatomy, radial conductivity, anatomical model, Zea mays , aerenchyma, reanalysis One-Sentence summary: Generator of Root ANAtomy in R (GRANAR) is a new open-source computational tool that can be used to rapidly generate digital versions of root anatomical networks.

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Going with the Flow: Multiscale Insights into the Composite Nature of Water Transport in Roots

Cited by 73 publications

References 74 publications

Root water uptake and its pathways across the root: quantification at the cellular scale

Root water uptake and its pathways across the root: quantification at the cellular scale

From plasmodesma geometry to effective symplasmic permeability through biophysical modelling

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

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