Drying of mucilage causes water repellency in the rhizosphere of maize: measurements and modelling

Background and AimsAlthough maize roots have been extensively studied, there is limited information on the effect of root exudates on the hydraulic properties of maize rhizosphere. Recent experiments suggested that the mucilaginous fraction of root exudates may cause water repellency of the rhizosphere. Our objectives were: 1) to investigate whether maize rhizosphere turns hydrophobic after drying and subsequent rewetting; 2) to test whether maize mucilage is hydrophobic; and 3) to find a quantitative relation between rhizosphere rewetting, particle size, soil matric potential and mucilage concentration.MethodsMaize plants were grown in aluminum containers filled with a sandy soil. When the plants were 3-weeks-old, the soil was let dry and then it was irrigated. The soil water content during irrigation was imaged using neutron radiography. In a parallel experiment, ten maize plants were grown in sandy soil for 5 weeks. Mucilage was collected from young brace roots growing above the soil. Mucilage was placed on glass slides and let dry. The contact angle was measured with the sessile drop method for varying mucilage concentration. Additionally, capillary rise experiments were performed in soils of varying particle size mixed with maize mucilage. We then used a pore-network model in which mucilage was randomly distributed in a cubic lattice. The general idea was that rewetting of a pore is impeded when the concentration of mucilage on the pore surface (g cm−2) is higher than a given threshold value. The threshold value depended on soil matric potential, pore radius and contract angle. Then, we randomly distributed mucilage in the pore network and we calculated the percolation of water across a cubic lattice for varying soil particle size, mucilage concentration and matric potential.ResultsOur results showed that: 1) the rhizosphere of maize stayed temporarily dry after irrigation; 2) mucilage became water repellent after drying. Mucilage contact angle increased with mucilage surface concentration (gram of dry mucilage per surface area); 3) Water could easily cross the rhizosphere when the mucilage concentration was below a given threshold. In contrast, above a critical mucilage concentration water could not flow through the rhizosphere. The critical mucilage concentration decreased with increasing particle size and decreasing matric potential.ConclusionsThese results show the importance of mucilage exudation for the water fluxes across the root-soil interface. Our percolation model predicts at what mucilage concentration the rhizosphere turns hydrophobic depending on soil texture and matric potential. Further studies are needed to extend these results to varying soil conditions and to upscale them to the entire root system.

[1]  Anders Kaestner,et al.  Measurements of water uptake of maize roots: the key function of lateral roots , 2015, Plant and Soil.

[2]  H. Vereecken,et al.  Modelling the impact of heterogeneous rootzone water distribution on the regulation of transpiration by hormone transport and/or hydraulic pressures , 2014, Plant and Soil.

[3]  Hydraulic conductivity of the root-soil interface of lupin in sandy soil after drying and rewetting , 2015, Plant and Soil.

[4]  Tobias Wojciechowski,et al.  Opportunities and challenges in the subsoil: pathways to deeper rooted crops. , 2015, Journal of experimental botany.

[5]  S. Redner,et al.  Introduction To Percolation Theory , 2018 .

[6]  R. Richards,et al.  Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. , 2012, Journal of experimental botany.

[7]  J. Parlange,et al.  Assessment of the application of percolation theory to a water repellent soil , 2005 .

[8]  T. Ghezzehei,et al.  Interplay between soil drying and root exudation in rhizosheath development , 2013, Plant and Soil.

[9]  J. Lynch,et al.  New roots for agriculture: exploiting the root phenome , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[10]  D. Vetterlein,et al.  Plasticity of rhizosphere hydraulic properties as a key for efficient utilization of scarce resources. , 2013, Annals of botany.

[11]  Brian Berkowitz,et al.  PERCOLATION THEORY AND ITS APPLICATION TO GROUNDWATER HYDROLOGY , 1993 .

[12]  Isaac Balberg,et al.  Recent developments in continuum percolation , 1987 .

[13]  Hans-Jörg Vogel,et al.  Quantitative morphology and network representation of soil pore structure , 2001 .

[14]  D. C. Gordon,et al.  Plant influence on rhizosphere hydraulic properties: direct measurements using a miniaturized infiltrometer. , 2003, The New phytologist.

[15]  G. Sposito Green Water and Global Food Security , 2013 .

[16]  Brian Berkowitz,et al.  Percolation Theory and Network Modeling Applications in Soil Physics , 1998 .

[17]  A. Carminati,et al.  A Model of Root Water Uptake Coupled with Rhizosphere Dynamics , 2012 .

[18]  Hans-Jörg Vogel,et al.  When Roots Lose Contact , 2009 .

[19]  Hans-Jörg Vogel,et al.  Dynamics of soil water content in the rhizosphere , 2010, Plant and Soil.

[20]  M. Zarebanadkouki,et al.  Mucilage exudation facilitates root water uptake in dry soils. , 2014, Functional plant biology : FPB.

[21]  J. Boyer,et al.  The expansion of maize root‐cap mucilage during hydration. 3. Changes in water potential and water content , 1997 .

[22]  Rainer Schulin,et al.  Quantitative Imaging of Infiltration, Root Growth, and Root Water Uptake via Neutron Radiography , 2008 .

[23]  T. Ghezzehei,et al.  Water for Carbon, Carbon for Water , 2015 .

[24]  Luca Ridolfi,et al.  Can diversity in root architecture explain plant water use efficiency? A modeling study , 2015, Ecological modelling.

[25]  T. Ghezzehei,et al.  Effects of root-induced compaction on rhizosphere hydraulic properties--X-ray microtomography imaging and numerical simulations. , 2011, Environmental science & technology.

[26]  Peter J. Gregory,et al.  Plant roots release phospholipid surfactants that modify the physical and chemical properties of soil. , 2003, The New phytologist.

[27]  M. Zarebanadkouki,et al.  Nonequilibrium water dynamics in the rhizosphere: How mucilage affects water flow in soils , 2014 .

[28]  A. Carminati,et al.  Effect of soil drying on mucilage exudation and its water repellency: a new method to collect mucilage , 2015 .

[29]  Hans-Jörg Vogel,et al.  Three-dimensional visualization and quantification of water content in the rhizosphere. , 2011, The New phytologist.

[30]  M. Watt,et al.  Formation and Stabilization of Rhizosheaths of Zea mays L. (Effect of Soil Water Content) , 1994, Plant physiology.

[31]  H. Vogel,et al.  Is the Rhizosphere Temporarily Water Repellent? , 2012 .

[32]  A. Carminati,et al.  Roots at the percolation threshold. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  I. Young Variation in moisture contents between bulk soil and the rhizosheath of wheat (Triticum aestivum L. cv. Wembley) , 1995 .

[34]  Brian Berkowitz,et al.  Percolation approach to the problem of hydraulic conductivity in porous media , 1992 .

[35]  H. Vogel,et al.  How the Rhizosphere May Favor Water Availability to Roots , 2011 .

[36]  Anders Kaestner,et al.  Neutron radiography as a tool for revealing root development in soil: capabilities and limitations , 2009, Plant and Soil.

[37]  C. Grünzweig,et al.  The ICON beamline – A facility for cold neutron imaging at SINQ , 2011 .

[38]  P. M. Abraham,et al.  Water repellency enhances the deposition of negatively charged hydrophilic colloids in a water-saturated sand matrix , 2013 .

[39]  M. Mccully,et al.  How Do Real Roots Work? (Some New Views of Root Structure) , 1995, Plant physiology.

[40]  X. Draye,et al.  Plant Water Uptake in Drying Soils1 , 2014, Plant Physiology.

[41]  A. Hunt Continuum percolation theory for water retention and hydraulic conductivity of fractal soils: estimation of the critical volume fraction for percolation , 2004 .