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Title: Multiseriate cortical sclerenchyma enhance root penetration in compacted soils

Abstract

Mechanical impedance limits soil exploration and resource capture by plant roots. We examine the role of root anatomy in regulating plant adaptation to mechanical impedance and identify a root anatomical phene in maize (Zea mays) and wheat (Triticum aestivum) associated with penetration of hard soil: Multiseriate cortical sclerenchyma (MCS). We characterize this trait and evaluate the utility of MCS for root penetration in compacted soils. Roots with MCS had a greater cell wall-to-lumen ratio and a distinct UV emission spectrum in outer cortical cells. Genome-wide association mapping revealed that MCS is heritable and genetically controlled. We identified a candidate gene associated with MCS. Across all root classes and nodal positions, maize genotypes with MCS had 13% greater root lignin concentration compared to genotypes without MCS. Genotypes without MCS formed MCS upon exogenous ethylene exposure. Genotypes with MCS had greater lignin concentration and bending strength at the root tip. In controlled environments, MCS in maize and wheat was associated improved root tensile strength and increased penetration ability in compacted soils. Maize genotypes with MCS had root systems with 22% greater depth and 49% greater shoot biomass in compacted soils in the field compared to lines without MCS. Of the lines wemore » assessed, MCS was present in 30 to 50% of modern maize, wheat, and barley cultivars but was absent in teosinte and wild and landrace accessions of wheat and barley. MCS merits investigation as a trait for improving plant performance in maize, wheat, and other grasses under edaphic stress.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [4]
  1. Pennsylvania State Univ., University Park, PA (United States). Dept. of Plant Science
  2. Univ. of Nottingham (United Kingdom). School of Biosciences. Division of Agricultural and Environment Sciences; The James Hutton Inst., Invergowrie (United Kingdom)
  3. Univ. of Nottingham (United Kingdom). School of Biosciences. Division of Agricultural and Environment Sciences; Univ. of Nottingham (United Kingdom). Centre for Plant Integrative Biology
  4. Pennsylvania State Univ., University Park, PA (United States). Dept. of Plant Science; Univ. of Nottingham (United Kingdom). School of Biosciences. Division of Agricultural and Environment Sciences; Univ. of Nottingham (United Kingdom). Centre for Plant Integrative Biology
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Advanced Research Projects Agency - Energy (ARPA-E)
OSTI Identifier:
1816762
Grant/Contract Number:  
AR0000821
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 118; Journal Issue: 6; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; root anatomy; soil impedance; phenotype

Citation Formats

Schneider, Hannah M., Strock, Christopher F., Hanlon, Meredith T., Vanhees, Dorien J., Perkins, Alden C., Ajmera, Ishan B., Sidhu, Jagdeep Singh, Mooney, Sacha J., Brown, Kathleen M., and Lynch, Jonathan P. Multiseriate cortical sclerenchyma enhance root penetration in compacted soils. United States: N. p., 2021. Web. doi:10.1073/pnas.2012087118.
Schneider, Hannah M., Strock, Christopher F., Hanlon, Meredith T., Vanhees, Dorien J., Perkins, Alden C., Ajmera, Ishan B., Sidhu, Jagdeep Singh, Mooney, Sacha J., Brown, Kathleen M., & Lynch, Jonathan P. Multiseriate cortical sclerenchyma enhance root penetration in compacted soils. United States. https://doi.org/10.1073/pnas.2012087118
Schneider, Hannah M., Strock, Christopher F., Hanlon, Meredith T., Vanhees, Dorien J., Perkins, Alden C., Ajmera, Ishan B., Sidhu, Jagdeep Singh, Mooney, Sacha J., Brown, Kathleen M., and Lynch, Jonathan P. Wed . "Multiseriate cortical sclerenchyma enhance root penetration in compacted soils". United States. https://doi.org/10.1073/pnas.2012087118. https://www.osti.gov/servlets/purl/1816762.
@article{osti_1816762,
title = {Multiseriate cortical sclerenchyma enhance root penetration in compacted soils},
author = {Schneider, Hannah M. and Strock, Christopher F. and Hanlon, Meredith T. and Vanhees, Dorien J. and Perkins, Alden C. and Ajmera, Ishan B. and Sidhu, Jagdeep Singh and Mooney, Sacha J. and Brown, Kathleen M. and Lynch, Jonathan P.},
abstractNote = {Mechanical impedance limits soil exploration and resource capture by plant roots. We examine the role of root anatomy in regulating plant adaptation to mechanical impedance and identify a root anatomical phene in maize (Zea mays) and wheat (Triticum aestivum) associated with penetration of hard soil: Multiseriate cortical sclerenchyma (MCS). We characterize this trait and evaluate the utility of MCS for root penetration in compacted soils. Roots with MCS had a greater cell wall-to-lumen ratio and a distinct UV emission spectrum in outer cortical cells. Genome-wide association mapping revealed that MCS is heritable and genetically controlled. We identified a candidate gene associated with MCS. Across all root classes and nodal positions, maize genotypes with MCS had 13% greater root lignin concentration compared to genotypes without MCS. Genotypes without MCS formed MCS upon exogenous ethylene exposure. Genotypes with MCS had greater lignin concentration and bending strength at the root tip. In controlled environments, MCS in maize and wheat was associated improved root tensile strength and increased penetration ability in compacted soils. Maize genotypes with MCS had root systems with 22% greater depth and 49% greater shoot biomass in compacted soils in the field compared to lines without MCS. Of the lines we assessed, MCS was present in 30 to 50% of modern maize, wheat, and barley cultivars but was absent in teosinte and wild and landrace accessions of wheat and barley. MCS merits investigation as a trait for improving plant performance in maize, wheat, and other grasses under edaphic stress.},
doi = {10.1073/pnas.2012087118},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 6,
volume = 118,
place = {United States},
year = {Wed Feb 03 00:00:00 EST 2021},
month = {Wed Feb 03 00:00:00 EST 2021}
}

Works referenced in this record:

Lignin Biosynthesis
journal, June 2003


Large Root Cortical Cell Size Improves Drought Tolerance in Maize
journal, October 2014

  • Chimungu, Joseph G.; Brown, Kathleen M.; Lynch, Jonathan P.
  • Plant Physiology, Vol. 166, Issue 4
  • DOI: 10.1104/pp.114.250449

Comparing the defence-related gene expression changes upon root-knot nematode attack in susceptible versus resistant cultivars of rice
journal, March 2016

  • Kumari, Chanchal; Dutta, Tushar K.; Banakar, Prakash
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep22846

Cortical Cell Diameter Is Key To Energy Costs of Root Growth in Wheat
journal, May 2019

  • Colombi, Tino; Herrmann, Anke Marianne; Vallenback, Pernilla
  • Plant Physiology, Vol. 180, Issue 4
  • DOI: 10.1104/pp.19.00262

Phenylalanine ammonia lyase as a precursory enzyme of legume stem lignification
journal, January 1995

  • Bidlack, J. E.; Buxton, D. R.; Shibles, R. M.
  • Canadian Journal of Plant Science, Vol. 75, Issue 1
  • DOI: 10.4141/cjps95-022

The Relation of Cellulose and Lignin Content to the Nutritive Value of Animal Feeds
journal, April 1938

  • Crampton, E. W.; Maynard, L. A.
  • The Journal of Nutrition, Vol. 15, Issue 4
  • DOI: 10.1093/jn/15.4.383

Acetyl Bromide Soluble Lignin (ABSL) Assay for Total Lignin Quantification from Plant Biomass
journal, January 2017


Root cortical aerenchyma improves the drought tolerance of maize ( Zea mays L.)
journal, February 2010


Root cortex: structural and functional variability and responses to environmental stress
journal, January 2004


The nodal roots of Zea : their development in relation to structural features of the stem
journal, November 1986

  • Hoppe, D. C.; McCully, M. E.; Wenzel, C. L.
  • Canadian Journal of Botany, Vol. 64, Issue 11
  • DOI: 10.1139/b86-335

Genotypic Variation for Root Penetration of a Soil Pan
journal, March 1999

  • May, O. Lloyd; Kasperbauer, Michael J.
  • Journal of Sustainable Agriculture, Vol. 13, Issue 4
  • DOI: 10.1300/J064v13n04_08

Plant functional traits and soil carbon sequestration in contrasting biomes
journal, May 2008


Esau's Plant Anatomy
journal, January 2006


Progressive drought alters architectural and anatomical traits of rice roots
journal, December 2018


Sclareol Induces Plant Resistance to Root-Knot Nematode Partially Through Ethylene-Dependent Enhancement of Lignin Accumulation
journal, April 2015

  • Fujimoto, Taketo; Mizukubo, Takayuki; Abe, Hiroshi
  • Molecular Plant-Microbe Interactions®, Vol. 28, Issue 4
  • DOI: 10.1094/MPMI-10-14-0320-R

R/qtl: QTL mapping in experimental crosses
journal, May 2003


Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis
journal, January 2010


Root anatomical traits contribute to deeper rooting of maize under compacted field conditions
journal, May 2020

  • Vanhees, Dorien J.; Loades, Kenneth W.; Bengough, A. Glyn
  • Journal of Experimental Botany, Vol. 71, Issue 14
  • DOI: 10.1093/jxb/eraa165

Lignin biochemistry: Biosynthesis and biodegradation
journal, January 1990


The Morphology and Relationships of Austrobaileya
journal, January 1949

  • Bailey, Irving W.; Swamy, B. G. L.
  • Journal of the Arnold Arboretum., Vol. 30, Issue 3
  • DOI: 10.5962/p.185606

Constricted growth of grass roots through rigid pores
journal, June 1985


Development and application of MIPAR™: a novel software package for two- and three-dimensional microstructural characterization
journal, April 2014

  • Sosa, John M.; Huber, Daniel E.; Welk, Brian
  • Integrating Materials and Manufacturing Innovation, Vol. 3, Issue 1
  • DOI: 10.1186/2193-9772-3-10

QTL mapping and phenotypic variation for root architectural traits in maize (Zea mays L.)
journal, September 2014

  • Burton, Amy L.; Johnson, James M.; Foerster, Jillian M.
  • Theoretical and Applied Genetics, Vol. 127, Issue 11
  • DOI: 10.1007/s00122-014-2353-4

Lignin turnover in arable soil and grassland analysed with two different labelling approaches
journal, June 2007


Ethylene modulates root cortical senescence in barley
journal, April 2018

  • Schneider, Hannah M.; Wojciechowski, Tobias; Postma, Johannes A.
  • Annals of Botany, Vol. 122, Issue 1
  • DOI: 10.1093/aob/mcy059

Effects of soil compaction on root elongation and anatomy of different cereal plant species
journal, May 2012


Quantitative trait loci for root-penetration ability and root thickness in rice: Comparison of genetic backgrounds
journal, February 2000

  • Zheng, Hong-gang; Babu, Md., R. Chandra; Pathan, M. Safiullah
  • Genome, Vol. 43, Issue 1
  • DOI: 10.1139/g99-065

Programmed Proteome Response for Drought Avoidance/Tolerance in the Root of a C3 Xerophyte (Wild Watermelon) Under Water Deficits
journal, December 2007

  • Yoshimura, K.; Masuda, A.; Kuwano, M.
  • Plant and Cell Physiology, Vol. 49, Issue 2
  • DOI: 10.1093/pcp/pcm180

The Influence of Cellulose Content on Tensile Strength in Tree Roots
journal, December 2005


Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids
journal, January 2004


Organic inputs for soil fertility management in tropical agroecosystems: application of an organic resource database
journal, January 2001

  • Palm, Cheryl A.; Gachengo, Catherine N.; Delve, Robert J.
  • Agriculture, Ecosystems & Environment, Vol. 83, Issue 1-2
  • DOI: 10.1016/S0167-8809(00)00267-X

Lignins and lignification: Selected issues
journal, January 2000


Opportunities and challenges in the subsoil: pathways to deeper rooted crops
journal, January 2015

  • Lynch, Jonathan P.; Wojciechowski, Tobias
  • Journal of Experimental Botany, Vol. 66, Issue 8
  • DOI: 10.1093/jxb/eru508

Root cortical aerenchyma inhibits radial nutrient transport in maize (Zea mays)
journal, November 2013

  • Hu, Bo; Henry, Amelia; Brown, Kathleen M.
  • Annals of Botany, Vol. 113, Issue 1
  • DOI: 10.1093/aob/mct259

Laser ablation tomography for visualization of root colonization by edaphic organisms
journal, June 2019

  • Strock, Christopher F.; Schneider, Hannah M.; Galindo-Castañeda, Tania
  • Journal of Experimental Botany, Vol. 70, Issue 19
  • DOI: 10.1093/jxb/erz271

The buckling of plant roots
journal, March 1982


Genotypic differences in root penetration ability of wheat through thin wax layers in contrasting water regimes and in the field
journal, October 2007


Trade-off between root porosity and mechanical strength in species with different types of aerenchyma
journal, May 2007


Does Morphological and Anatomical Plasticity during the Vegetative Stage Make Wheat More Tolerant of Water Deficit Stress Than Rice?
journal, January 2015

  • Kadam, Niteen N.; Yin, Xinyou; Bindraban, Prem S.
  • Plant Physiology, Vol. 167, Issue 4
  • DOI: 10.1104/pp.114.253328

Temporal Changes in c and n Stocks of Restored Prairie: Implications for c Sequestration Strategies
journal, September 2008

  • Matamala, R.; Jastrow, J. D.; Miller, R. M.
  • Ecological Applications, Vol. 18, Issue 6
  • DOI: 10.1890/07-1609.1

Iterative Usage of Fixed and Random Effect Models for Powerful and Efficient Genome-Wide Association Studies
journal, February 2016


Expanding the genetic map of maize with the intermated B73 × Mo17 (IBM) population
journal, January 2002

  • Lee, Michael; Sharopova, Natalya; Beavis, William D.
  • Plant Molecular Biology, Vol. 48, Issue 5-6, p. 453-461
  • DOI: 10.1023/A:1014893521186

Lignin Biosynthesis.
journal, July 1995


Development and application of MIPAR™: a novel software package for two- and three-dimensional microstructural characterization
journal, April 2014

  • Sosa, John M.; Huber, Daniel E.; Welk, Brian
  • Integrating Materials and Manufacturing Innovation, Vol. 3, Issue 1
  • DOI: 10.1186/2193-9772-3-10

New roots for agriculture: exploiting the root phenome
journal, June 2012

  • Lynch, Jonathan P.; Brown, Kathleen M.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1595
  • DOI: 10.1098/rstb.2011.0243

Rightsizing root phenotypes for drought resistance
journal, February 2018

  • Lynch, Jonathan P.
  • Journal of Experimental Botany, Vol. 69, Issue 13
  • DOI: 10.1093/jxb/ery048

Genotypic Variation of the Ability of Root to Penetrate Hard Soil Layers among Japanese Wheat Cultivars
journal, January 2006

  • Kubo, Katashi; Iwama, Kazuto; Yanagisawa, Akira
  • Plant Production Science, Vol. 9, Issue 1
  • DOI: 10.1626/pps.9.47

Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems
journal, January 2013


Rooting, Water Uptake, and Xylem Structure Adaptation to Drought of Two Sorghum Cultivars
journal, January 1999


Genetic control of root architectural plasticity in maize
journal, February 2020

  • Schneider, Hannah M.; Klein, Stephanie P.; Hanlon, Meredith T.
  • Journal of Experimental Botany
  • DOI: 10.1093/jxb/eraa084

Cortical Cell Diameter Is Key To Energy Costs of Root Growth in Wheat
journal, May 2019

  • Colombi, Tino; Herrmann, Anke Marianne; Vallenback, Pernilla
  • Plant Physiology, Vol. 180, Issue 4
  • DOI: 10.1104/pp.19.00262

Lignin Biosynthesis
journal, June 2003


Development and Structure of the Root Cortex in Caltha palustris L. and Nymphaea odorata Ait.
journal, September 2000


Why fine tree roots are stronger than thicker roots: The role of cellulose and lignin in relation to slope stability
journal, February 2014


Root Phenes for Enhanced Soil Exploration and Phosphorus Acquisition: Tools for Future Crops
journal, May 2011


The C.I.E. colorimetric standards and their use
journal, January 1931


Lignin and cellulose concentrations in roots of Douglas fir and European beech of different diameter classes and soil depths
journal, September 2013


Mixed linear model approach adapted for genome-wide association studies
journal, March 2010

  • Zhang, Zhiwu; Ersoz, Elhan; Lai, Chao-Qiang
  • Nature Genetics, Vol. 42, Issue 4
  • DOI: 10.1038/ng.546

Long-Term Changes in Mollisol Organic Carbon and Nitrogen
journal, January 2009

  • David, Mark B.; McIsaac, Gregory F.; Darmody, Robert G.
  • Journal of Environmental Quality, Vol. 38, Issue 1
  • DOI: 10.2134/jeq2008.0132

Ethylene-induced changes in lignification and cell wall-degrading enzymes in the roots of mungbean (Vigna radiata) sprouts
journal, December 2013


Variation in Fibre and Parenchyma Wall Thickness in Culms of the Bamboo Sinobambusa Tootsik
journal, January 1988


Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture
journal, March 2019


Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement
journal, April 2014

  • Lynch, Jonathan P.; Chimungu, Joseph G.; Brown, Kathleen M.
  • Journal of Experimental Botany, Vol. 65, Issue 21
  • DOI: 10.1093/jxb/eru162

Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field
journal, November 2010

  • Trachsel, Samuel; Kaeppler, Shawn M.; Brown, Kathleen M.
  • Plant and Soil, Vol. 341, Issue 1-2
  • DOI: 10.1007/s11104-010-0623-8

The Morphology and Relationships of Austrobaileya
journal, January 1949

  • Bailey, Irving W.; Swamy, B. G. L.
  • Journal of the Arnold Arboretum., Vol. 30, Issue 3
  • DOI: 10.5962/p.185606

How do roots elongate in a structured soil?
journal, September 2013

  • Jin, Kemo; Shen, Jianbo; Ashton, Rhys W.
  • Journal of Experimental Botany, Vol. 64, Issue 15
  • DOI: 10.1093/jxb/ert286

Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana
journal, May 2003


Root strength and trampling tolerance in the grass Paspalum dilatatum and the dicot Lotus glaber in flooded soil
journal, February 2006


Erratum: “Three-dimensional analysis of biological systems via a novel laser ablation technique” [J. Laser Appl. 31, 022602 (2019)]
journal, August 2019

  • Hall, Benjamin; Lanba, Asheesh; Lynch, Jonathan P.
  • Journal of Laser Applications, Vol. 31, Issue 3
  • DOI: 10.2351/1.5108633

Adaptation of Root Function by Nutrient-Induced Plasticity of Endodermal Differentiation
journal, January 2016

  • Barberon, Marie; Vermeer, Joop Engelbertus Martinus; De Bellis, Damien
  • Cell, Vol. 164, Issue 3
  • DOI: 10.1016/j.cell.2015.12.021

Trade-off between root porosity and mechanical strength in species with different types of aerenchyma
journal, May 2007


Progressive drought alters architectural and anatomical traits of rice roots
journal, December 2018


Changes in phenolic acid and lignin biosynthesis in response to treatment of root tissue of the Swedish Turnip (Brassica napo-brassica) with ethylene
journal, September 1973

  • Rhodes, M. J. C.; Wooltorton, L. S. C.
  • Qualitas Plantarum Plant Foods for Human Nutrition, Vol. 23, Issue 1-3
  • DOI: 10.1007/BF01092248

R/qtl: QTL mapping in experimental crosses
journal, May 2003


Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis
journal, January 2010


Influence of root diameter on the penetration of seminal roots into a compacted subsoil
journal, August 1992

  • Materechera, S. A.; Alston, A. M.; Kirby, J. M.
  • Plant and Soil, Vol. 144, Issue 2
  • DOI: 10.1007/BF00012888

Laser ablation tomography for visualization of root colonization by edaphic organisms
journal, June 2019

  • Strock, Christopher F.; Schneider, Hannah M.; Galindo-Castañeda, Tania
  • Journal of Experimental Botany, Vol. 70, Issue 19
  • DOI: 10.1093/jxb/erz271

Reduced Root Cortical Cell File Number Improves Drought Tolerance in Maize
journal, October 2014

  • Chimungu, Joseph G.; Brown, Kathleen M.; Lynch, Jonathan P.
  • Plant Physiology, Vol. 166, Issue 4
  • DOI: 10.1104/pp.114.249037

Lignin content and chemical characteristics in maize and wheat vary between plant organs and growth stages: consequences for assessing lignin dynamics in soil
journal, February 2011


The composite water and solute transport of barley (Hordeum vulgare) roots: effect of suberized barriers
journal, January 2017

  • Ranathunge, Kosala; Kim, Yangmin X.; Wassmann, Friedrich
  • Annals of Botany
  • DOI: 10.1093/aob/mcw252

Subsoil compaction effects on crops in Punjab, Pakistan:
journal, July 2001


Effects of a compacted subsoil layer on root and shoot growth, water use and nutrient uptake of winter wheat
journal, April 1988


Differential Genotypic and Root Type Penetration of Compacted Soil Layers
journal, May 1998


Lignin Biosynthesis
journal, July 1995

  • Whetten, Ross; Sederoff, Ron
  • The Plant Cell, Vol. 7, Issue 7
  • DOI: 10.2307/3870053

Root anatomical phenes predict root penetration ability and biomechanical properties in maize (Zea Mays)
journal, April 2015

  • Chimungu, Joseph G.; Loades, Kenneth W.; Lynch, Jonathan P.
  • Journal of Experimental Botany, Vol. 66, Issue 11
  • DOI: 10.1093/jxb/erv121

Development of anatomical structure of roots of Phragmites australis
journal, February 2002


Does Morphological and Anatomical Plasticity during the Vegetative Stage Make Wheat More Tolerant of Water Deficit Stress Than Rice?
journal, January 2015

  • Kadam, Niteen N.; Yin, Xinyou; Bindraban, Prem S.
  • Plant Physiology, Vol. 167, Issue 4
  • DOI: 10.1104/pp.114.253328

An Expanded Maize Gene Expression Atlas based on RNA Sequencing and its Use to Explore Root Development
journal, January 2016


Carbohydrate and lignin contents of plant materials used in animal feeding
journal, August 1997


Agronomic consequences of tractor wheel compaction on a clay soil
journal, August 2006


A combined RFLP and AFLP linkage map of upland rice (Oryza sativa L.) used to identify QTLs for root-penetration ability
journal, January 2000

  • Price, A. H.; Steele, K. A.; Moore, B. J.
  • Theoretical and Applied Genetics, Vol. 100, Issue 1
  • DOI: 10.1007/s001220050007

Genetic control of root anatomical plasticity in maize
journal, March 2020

  • Schneider, Hannah M.; Klein, Stephanie P.; Hanlon, Meredith T.
  • The Plant Genome, Vol. 13, Issue 1
  • DOI: 10.1002/tpg2.20003

Lignin Biosynthesis.
journal, July 1995


Root cortical burden influences drought tolerance in maize
journal, April 2013

  • Jaramillo, Raúl E.; Nord, Eric A.; Chimungu, Joseph G.
  • Annals of Botany, Vol. 112, Issue 2
  • DOI: 10.1093/aob/mct069

Three-dimensional analysis of biological systems via a novel laser ablation technique
journal, May 2019

  • Hall, Benjamin; Lanba, Asheesh
  • Journal of Laser Applications, Vol. 31, Issue 2
  • DOI: 10.2351/1.5096089

Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.)
journal, February 2015

  • Chimungu, Joseph G.; Maliro, Moses F. A.; Nalivata, Patson C.
  • Field Crops Research, Vol. 171
  • DOI: 10.1016/j.fcr.2014.10.009

Root anatomical traits contribute to deeper rooting of maize under compacted field conditions
journal, May 2020

  • Vanhees, Dorien J.; Loades, Kenneth W.; Bengough, A. Glyn
  • Journal of Experimental Botany, Vol. 71, Issue 14
  • DOI: 10.1093/jxb/eraa165

Cell‐Wall Composition of Maize Internodes of Varying Maturity
journal, March 1998


Demystifying roots: A need for clarification and extended concepts in root phenotyping
journal, May 2019


Genotypic variation and nitrogen stress effects on root anatomy in maize are node specific
journal, June 2019

  • Yang, Jennifer T.; Schneider, Hannah M.; Brown, Kathleen M.
  • Journal of Experimental Botany, Vol. 70, Issue 19
  • DOI: 10.1093/jxb/erz293

Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement
journal, April 2014

  • Lynch, Jonathan P.; Chimungu, Joseph G.; Brown, Kathleen M.
  • Journal of Experimental Botany, Vol. 65, Issue 21
  • DOI: 10.1093/jxb/eru162

Root Cortical Aerenchyma Enhances Nitrogen Acquisition from Low-Nitrogen Soils in Maize
journal, June 2014

  • Saengwilai, P.; Nord, E. A.; Chimungu, J. G.
  • PLANT PHYSIOLOGY, Vol. 166, Issue 2
  • DOI: 10.1104/pp.114.241711

Use of Wax‐Petrolatum Layers for Screening Rice Root Penetration
journal, May 1995


RootScan: Software for high-throughput analysis of root anatomical traits
journal, February 2012