Root morphology and exudate availability are shaped by particle size and chemistry in Brachypodium distachyon

Abstract Root morphology and exudation define a plants’ sphere of influence in soils. In turn, soil characteristics influence plant growth, morphology, root microbiome, and rhizosphere chemistry. Collectively, all these parameters have significant implications on the major biogeochemical cycles, crop yield, and ecosystem health. However, how plants are shaped by the physiochemistry of soil particles is still not well understood. We explored how particle size and chemistry of growth substrates affect root morphology and exudation of a model grass. We grew Brachypodium distachyon in glass beads with various sizes (0.5, 1, 2, 3 mm), as well as in sand (0.005, 0.25, 4 mm) and in clay (4 mm) particles and in particle‐free hydroponic medium. Plant morphology, root weight, and shoot weight were measured. We found that particle size significantly influenced root fresh weight and root length, whereas root number and shoot weight remained constant. Next, plant exudation profiles were analyzed with mass spectrometry imaging and liquid chromatography–mass spectrometry. Mass spectrometry imaging suggested that both, root length and number shape root exudation. Exudate profiles were comparable for plants growing in glass beads or sand with various particles sizes, but distinct for plants growing in clay for in situ exudate collection. Clay particles were found to sorb 20% of compounds exuded by clay‐grown plants, and 70% of compounds from a defined exudate medium. The sorbed compounds belonged to a range of chemical classes, among them nucleosides, organic acids, sugars, and amino acids. Some of the sorbed compounds could be desorbed by a rhizobacterium (Pseudomonas fluorescens WCS415), supporting its growth. This study demonstrates the effect of different characteristics of particles on root morphology, plant exudation and availability of nutrients to microorganisms. These findings further support the critical importance of the physiochemical properties of soils when investigating plant morphology, plant chemistry, and plant–microbe interactions.

[1]  J. Jadaun,et al.  WRKY1-mediated regulation of tryptophan decarboxylase in tryptamine generation for withanamide production in Withania somnifera (Ashwagandha) , 2020, Plant Cell Reports.

[2]  A. Gómez-Cadenas,et al.  Root exudates: from plant to rhizosphere and beyond , 2019, Plant Cell Reports.

[3]  Wolfgang Wanek,et al.  Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli , 2019, Front. Plant Sci..

[4]  C. Broeckling,et al.  Non-Targeted Metabolomics Reveals Sorghum Rhizosphere-Associated Exudates are Influenced by the Belowground Interaction of Substrate and Sorghum Genotype , 2019, International journal of molecular sciences.

[5]  N. Sokol,et al.  Pathways of mineral‐associated soil organic matter formation: Integrating the role of plant carbon source, chemistry, and point of entry , 2018, Global change biology.

[6]  P. Ortet,et al.  Plant Nutrient Resource Use Strategies Shape Active Rhizosphere Microbiota Through Root Exudation , 2018, Front. Plant Sci..

[7]  A. Visel,et al.  Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass , 2018, bioRxiv.

[8]  D. Etalo,et al.  Modulation of plant chemistry by beneficial root microbiota. , 2018, Natural product reports.

[9]  M. Firestone,et al.  Ecosystem Fabrication (EcoFAB) Protocols for The Construction of Laboratory Ecosystems Designed to Study Plant-microbe Interactions , 2018, Journal of visualized experiments : JoVE.

[10]  Eoin L. Brodie,et al.  Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly , 2018, Nature Microbiology.

[11]  Y. Kuzyakov,et al.  Rhizodeposition under drought is controlled by root growth rate and rhizosphere water content , 2018, Plant and Soil.

[12]  R. Chakraborty,et al.  Construction of Viable Soil Defined Media Using Quantitative Metabolomics Analysis of Soil Metabolites , 2017, Front. Microbiol..

[13]  P. Hallett,et al.  Plant exudates improve the mechanical conditions for root penetration through compacted soils , 2017, Plant and Soil.

[14]  A. Aharoni,et al.  Live imaging of root–bacteria interactions in a microfluidics setup , 2017, Proceedings of the National Academy of Sciences.

[15]  Evan Bolton,et al.  ClassyFire: automated chemical classification with a comprehensive, computable taxonomy , 2016, Journal of Cheminformatics.

[16]  M. Watt,et al.  Microbiome and Exudates of the Root and Rhizosphere of Brachypodium distachyon, a Model for Wheat , 2016, PloS one.

[17]  J. Dinneny,et al.  Environmental Control of Root System Biology. , 2016, Annual review of plant biology.

[18]  S. Brink Unlocking the Secrets of the Rhizosphere. , 2016, Trends in plant science.

[19]  P. Frey-Klett,et al.  The Mineralosphere Concept: Mineralogical Control of the Distribution and Function of Mineral-associated Bacterial Communities. , 2015, Trends in microbiology.

[20]  P. Nico,et al.  Competitive sorption of microbial metabolites on an iron oxide mineral , 2015 .

[21]  Guillaume Lobet,et al.  GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems , 2015, bioRxiv.

[22]  Oliver Ruebel,et al.  Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases , 2015, Metabolites.

[23]  Jennifer Pett-Ridge,et al.  Mineral protection of soil carbon counteracted by root exudates , 2015 .

[24]  T. Northen,et al.  Untargeted soil metabolomics methods for analysis of extractable organic matter , 2015 .

[25]  K. Smalla,et al.  Root exudation and root development of lettuce (Lactuca sativa L. cv. Tizian) as affected by different soils , 2014, Front. Microbiol..

[26]  Johan Six,et al.  Aggregate-associated soil organic matter as an ecosystem property and a measurement tool ☆ , 2014 .

[27]  Oliver Rübel,et al.  OpenMSI: a high-performance web-based platform for mass spectrometry imaging. , 2013, Analytical chemistry.

[28]  H. Bouwmeester,et al.  A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching , 2012, Nature.

[29]  S. Quake,et al.  The RootChip: An Integrated Microfluidic Chip for Plant Science[W][OA] , 2011, Plant Cell.

[30]  Loïc Pagès,et al.  A Novel Image-Analysis Toolbox Enabling Quantitative Analysis of Root System Architecture1[W][OA] , 2011, Plant Physiology.

[31]  A. Parashar,et al.  Plant-in-chip: Microfluidic system for studying root growth and pathogenic interactions in Arabidopsis , 2011 .

[32]  J. Vivanco,et al.  The effect of root exudates on root architecture in Arabidopsis thaliana , 2011, Plant Growth Regulation.

[33]  Benjamin P Bowen,et al.  Dealing with the unknown: Metabolomics and Metabolite Atlases , 2010, Journal of the American Society for Mass Spectrometry.

[34]  Eoin L. Brodie,et al.  Selective progressive response of soil microbial community to wild oat roots , 2009, The ISME Journal.

[35]  Davey L. Jones,et al.  Carbon flow in the rhizosphere: carbon trading at the soil–root interface , 2009, Plant and Soil.

[36]  V. Germain,et al.  Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars: Monosaccharide/proton symporter function in Arabidopsis , 2008 .

[37]  L. Kochian,et al.  Characterization of AtALMT1 Expression in Aluminum-Inducible Malate Release and Its Role for Rhizotoxic Stress Tolerance in Arabidopsis1[W][OA] , 2007, Plant Physiology.

[38]  D. Gleeson,et al.  Altering the mineral composition of soil causes a shift in microbial community structure. , 2007, FEMS microbiology ecology.

[39]  Nigel W. Hardy,et al.  Proposed minimum reporting standards for chemical analysis , 2007, Metabolomics.

[40]  L. V. Kravchenko,et al.  Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. , 2006, Molecular plant-microbe interactions : MPMI.

[41]  B. W. Veen The influence of mechanical impedance on the growth of maize roots , 1982, Plant and Soil.

[42]  A. Kabata-Pendias,et al.  Soil-plant transfer of trace elements—an environmental issue , 2004 .

[43]  J. Six,et al.  A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics , 2004 .

[44]  A. Edwards,et al.  Rock fragments in soil support a different microbial community from the fine earth , 2004 .

[45]  S. Plantureux,et al.  Influence of plant morphology on root exudation of maize subjected to mechanical impedance in hydroponic conditions , 1998, Plant and Soil.

[46]  S. Plantureux,et al.  Influence of mechanical impedance on root exudation of maize seedlings at two development stages , 1995, Plant and Soil.

[47]  G. Neumann,et al.  Cluster roots--an underground adaptation for survival in extreme environments. , 2002, Trends in plant science.

[48]  V. Germain,et al.  Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. , 2000, The Plant journal : for cell and molecular biology.

[49]  J. Baldock,et al.  Role of the soil matrix and minerals in protecting natural organic materials against biological attack , 2000 .

[50]  K. Paustian,et al.  Soil structure and organic matter: I. Distribution of aggregate-size classes and aggregate-associated carbon. , 2000 .

[51]  W. Silk,et al.  A mathematical model for pH patterns in the rhizospheres of growth zones , 1999 .

[52]  N. Peters,et al.  Alfalfa Root Exudates and Compounds which Promote or Inhibit Induction of Rhizobium meliloti Nodulation Genes. , 1988, Plant physiology.

[53]  A. Thomas,et al.  The nucleic acid fractions of a strain of Streptococcus faecalis. , 1953, Journal of general microbiology.