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Title: Laser ablation tomography for visualization of root colonization by edaphic organisms

Abstract

Soil biota have important effects on crop productivity, but can be difficult to study in situ. Laser ablation tomography (LAT) is a novel method that allows for rapid, three-dimensional quantitative and qualitative analysis of root anatomy, providing new opportunities to investigate interactions between roots and edaphic organisms. LAT was used for analysis of maize roots colonized by arbuscular mycorrhizal fungi, maize roots herbivorized by western corn rootworm, barley roots parasitized by cereal cyst nematode, and common bean roots damaged by Fusarium. UV excitation of root tissues affected by edaphic organisms resulted in differential autofluorescence emission, facilitating the classification of tissues and anatomical features. Samples were spatially resolved in three dimensions, enabling quantification of the volume and distribution of fungal colonization, western corn rootworm damage, nematode feeding sites, tissue compromised by Fusarium, and as well as root anatomical phenotypes. Owing to its capability for high-throughput sample imaging, LAT serves as an excellent tool to conduct large, quantitative screens to characterize genetic control of root anatomy and interactions with edaphic organisms. Additionally, this technology improves interpretation of root–organism interactions in relatively large, opaque root segments, providing opportunities for novel research investigating the effects of root anatomical phenes on associations with edaphic organisms.

Authors:
ORCiD logo [1];  [1];  [1];  [2];  [3];  [3];  [4];  [4];  [1]; ORCiD logo [1]; ORCiD logo [1]
  1. Pennsylvania State Univ., University Park, PA (United States)
  2. Lasers for Innovative Solutions, LLC, State College, PA (United States)
  3. The Univ. of Adelaide, Glen Osmond (Australia)
  4. Michigan State Univ., East Lansing, MI (United States)
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Advanced Research Projects Agency - Energy (ARPA-E)
Contributing Org.:
Department of Plant Science, Pennsylvania State University, University Park, PA 16802 USA 2 Lasers for Innovative Solutions, LLC, 200 Innovation Blvd. (Suite 214), State College, PA 16803 USA 3 School of Agriculture, Food and Wine, Waite Research Institute, The University of Adelaide, PMB 1, Glen Osmond, SA 5064, Australia 4 Department of Plant, Soil, and Microbial Sciences, Michigan State University, East Lansing, MI 48824, USA
OSTI Identifier:
1572933
Grant/Contract Number:  
AR0000821
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Volume: 70; Journal Issue: 19; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; cereal cyst nematode; Fusarium; mycorrhizae; root anatomy; root phenotyping; western corn rootworm

Citation Formats

Strock, Christopher F., Schneider, Hannah M., Galindo-Castañeda, Tania, Hall, Benjamin T., Van Gansbeke, Bart, Mather, Diane E., Roth, Mitchell G., Chilvers, Martin I., Guo, Xiangrong, Brown, Kathleen, and Lynch, Jonathan P. Laser ablation tomography for visualization of root colonization by edaphic organisms. United States: N. p., 2019. Web. doi:10.1093/jxb/erz271.
Strock, Christopher F., Schneider, Hannah M., Galindo-Castañeda, Tania, Hall, Benjamin T., Van Gansbeke, Bart, Mather, Diane E., Roth, Mitchell G., Chilvers, Martin I., Guo, Xiangrong, Brown, Kathleen, & Lynch, Jonathan P. Laser ablation tomography for visualization of root colonization by edaphic organisms. United States. doi:10.1093/jxb/erz271.
Strock, Christopher F., Schneider, Hannah M., Galindo-Castañeda, Tania, Hall, Benjamin T., Van Gansbeke, Bart, Mather, Diane E., Roth, Mitchell G., Chilvers, Martin I., Guo, Xiangrong, Brown, Kathleen, and Lynch, Jonathan P. Thu . "Laser ablation tomography for visualization of root colonization by edaphic organisms". United States. doi:10.1093/jxb/erz271. https://www.osti.gov/servlets/purl/1572933.
@article{osti_1572933,
title = {Laser ablation tomography for visualization of root colonization by edaphic organisms},
author = {Strock, Christopher F. and Schneider, Hannah M. and Galindo-Castañeda, Tania and Hall, Benjamin T. and Van Gansbeke, Bart and Mather, Diane E. and Roth, Mitchell G. and Chilvers, Martin I. and Guo, Xiangrong and Brown, Kathleen and Lynch, Jonathan P.},
abstractNote = {Soil biota have important effects on crop productivity, but can be difficult to study in situ. Laser ablation tomography (LAT) is a novel method that allows for rapid, three-dimensional quantitative and qualitative analysis of root anatomy, providing new opportunities to investigate interactions between roots and edaphic organisms. LAT was used for analysis of maize roots colonized by arbuscular mycorrhizal fungi, maize roots herbivorized by western corn rootworm, barley roots parasitized by cereal cyst nematode, and common bean roots damaged by Fusarium. UV excitation of root tissues affected by edaphic organisms resulted in differential autofluorescence emission, facilitating the classification of tissues and anatomical features. Samples were spatially resolved in three dimensions, enabling quantification of the volume and distribution of fungal colonization, western corn rootworm damage, nematode feeding sites, tissue compromised by Fusarium, and as well as root anatomical phenotypes. Owing to its capability for high-throughput sample imaging, LAT serves as an excellent tool to conduct large, quantitative screens to characterize genetic control of root anatomy and interactions with edaphic organisms. Additionally, this technology improves interpretation of root–organism interactions in relatively large, opaque root segments, providing opportunities for novel research investigating the effects of root anatomical phenes on associations with edaphic organisms.},
doi = {10.1093/jxb/erz271},
journal = {Journal of Experimental Botany},
number = 19,
volume = 70,
place = {United States},
year = {2019},
month = {6}
}

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Cited by: 7 works
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Works referenced in this record:

Ultraviolet-induced autofluorescence of arbuscular mycorrhizal root infections: an alternative to clearing and staining methods for assessing infections
journal, March 1982

  • Ames, Robert N.; Ingham, Elaine R.; Reid, C. P. P.
  • Canadian Journal of Microbiology, Vol. 28, Issue 3
  • DOI: 10.1139/m82-052

New Insights into the Regulation of Aquaporins by the Arbuscular Mycorrhizal Symbiosis in Maize Plants Under Drought Stress and Possible Implications for Plant Performance
journal, April 2014

  • Bárzana, Gloria; Aroca, Ricardo; Bienert, Gerd Patrick
  • Molecular Plant-Microbe Interactions, Vol. 27, Issue 4
  • DOI: 10.1094/MPMI-09-13-0268-R

Biochemical approaches to the study of plant-fungal interactions in arbuscular mycorrhiza
journal, October 1994

  • Bothe, H.; Klingner, A.; Kaldorf, M.
  • Experientia, Vol. 50, Issue 10
  • DOI: 10.1007/BF01923479

Chemical control of the cereal cyst nematode (Heterodera avenae) in the Victorian Mallee
journal, January 1970

  • Brown, Rh; Meagher, Jw; McSwain, Nk
  • Australian Journal of Experimental Agriculture, Vol. 10, Issue 43
  • DOI: 10.1071/EA9700172

A Maize Inbred Exhibits Resistance Against Western Corn Rootwoorm, Diabrotica virgifera virgifera
journal, November 2017

  • Castano-Duque, Lina; Loades, Kenneth W.; Tooker, John F.
  • Journal of Chemical Ecology, Vol. 43, Issue 11-12
  • DOI: 10.1007/s10886-017-0904-2

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

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

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

Chitin Biochemistry: Synthesis and Inhibition
journal, January 1987


Early detection of toxigenic fungi on maize by hyperspectral imaging analysis
journal, November 2010


Imaging and Spectroscopy of Natural Fluorophores in Pine Needles
journal, February 2018


Transparent soil microcosms allow 3D spatial quantification of soil microbiological processes in vivo
journal, October 2014


Parasitic nematodes have two distinct chitin synthases
journal, July 2005


Identification of ergosterol in vesicular-arbuscular mycorrhizae
journal, August 1992

  • Frey, B.; Buser, H. R.; Sch�epp, H.
  • Biology and Fertility of Soils, Vol. 13, Issue 4
  • DOI: 10.1007/BF00340581

Chitin and ergosterol content of extraradical and intraradical mycelium of the vesicular-arbuscular mycorrhizal fungus Glomus intraradices
journal, June 1994


Reduced root cortical burden improves growth and grain yield under low phosphorus availability in maize: Root cortical burden and phosphorus capture
journal, May 2018

  • Galindo-Castañeda, Tania; Brown, Kathleen M.; Lynch, Jonathan P.
  • Plant, Cell & Environment, Vol. 41, Issue 7
  • DOI: 10.1111/pce.13197

A comparison of visualization techniques for recording arbuscular mycorrhizal colonization
journal, April 1999


An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis: Systemic responses in mycorrhizal maize
journal, April 2015

  • Gerlach, Nina; Schmitz, Jessica; Polatajko, Aleksandra
  • Plant, Cell & Environment, Vol. 38, Issue 8
  • DOI: 10.1111/pce.12508

Adaptation and Invasiveness of Western Corn Rootworm: Intensifying Research on a Worsening Pest
journal, January 2009


Root cap influences root colonisation by Pseudomonas fluorescens SBW25 on maize
journal, September 2005


FvSTR1, a striatin orthologue in Fusarium virguliforme, is required for asexual development and virulence
journal, June 2017

  • Islam, Kazi T.; Bond, Jason P.; Fakhoury, Ahmad M.
  • Applied Microbiology and Biotechnology, Vol. 101, Issue 16
  • DOI: 10.1007/s00253-017-8387-1

Variation among Maize Inbred Lines and Detection of Quantitative Trait Loci for Growth at Low Phosphorus and Responsiveness to Arbuscular Mycorrhizal Fungi
journal, January 2000


Multilaboratory Comparison of Quantitative PCR Assays for Detection and Quantification of Fusarium virguliforme from Soybean Roots and Soil
journal, December 2015


Variation in Plant Response to Native and Exotic Arbuscular Mycorrhizal Fungi
journal, September 2003


Suppression of Soybean Yield Potential in the Continental United States by Plant Diseases from 2006 to 2009
journal, January 2010


Nematode feeding sites: unique organs in plant roots
journal, July 2013


Imaging mycorrhizal fungal transformants that express EGFP during ericoid endosymbiosis
journal, June 2007


Real-time PCR for quantification of eleven individual Fusarium species in cereals
journal, March 2009

  • Nicolaisen, Mogens; Supronienė, Skaidrė; Nielsen, Linda Kærgaard
  • Journal of Microbiological Methods, Vol. 76, Issue 3
  • DOI: 10.1016/j.mimet.2008.10.016

Distinguishable staining with neutral red for GFP-marked and GFP-nonmarked Fusarium oxysporum strains simultaneously colonizing root surfaces
journal, February 2003

  • Nonomura, Teruo; Tajima, Hiromi; Kitagawa, Yuko
  • Journal of General Plant Pathology, Vol. 69, Issue 1
  • DOI: 10.1007/s10327-002-0018-7

Bacterial colonization patterns of intact Pinus sylvestris mycorrhizospheres in dry pine forest soil: an electron microscopy study
journal, November 1997

  • Nurmiaho-Lassila, E. -L.; Timonen, S.; Haahtela, K.
  • Canadian Journal of Microbiology, Vol. 43, Issue 11
  • DOI: 10.1139/m97-147

Colonization of Tomato Root by Pathogenic and Nonpathogenic Fusarium oxysporum Strains Inoculated Together and Separately into the Soil
journal, February 2006


Early Events in the Fusarium verticillioides-Maize Interaction Characterized by Using a Green Fluorescent Protein-Expressing Transgenic Isolate
journal, March 2003


Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots
journal, October 2007


Transgenic Rootworm Corn: Assessing Potential Agronomic, Economic, and Environmental Benefits
journal, January 2004


Maize Morphology and Shoot CO Assimilation after Root Damage by Western Corn Rootworm Larvae
journal, January 1999


Autofluorescence of Plant Secreting Cells as a Biosensor and Bioindicator Reaction
journal, September 2003


Vital Autofluorescence: Application to the Study of Plant Living Cells
journal, September 2012

  • Roshchina, Victoria V.
  • International Journal of Spectroscopy, Vol. 2012
  • DOI: 10.1155/2012/124672

Scanning electron microscopy of microorganisms on the roots of wheat
journal, December 1974


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

Characterizing variation in mycorrhiza effect among diverse plant varieties
journal, December 2009

  • Sawers, Ruairidh J. H.; Gebreselassie, Mesfin N.; Janos, David P.
  • Theoretical and Applied Genetics, Vol. 120, Issue 5
  • DOI: 10.1007/s00122-009-1231-y

Recent research on fumonisins: a review
journal, February 2012


Simple Sequence Repeat Markers Developed from Maize Sequences Found in the GENBANK Database: Map Construction
journal, January 1996


Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi?
journal, November 2008


Tansley Review No. 96. Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses
journal, November 1997


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


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

Behaviour and ecology of the western corn rootworm ( Diabrotica virgifera virgifera LeConte)
journal, February 2009


Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition
journal, November 2017

  • Strock, Christopher F.; Morrow de la Riva, Laurie; Lynch, Jonathan P.
  • Plant Physiology, Vol. 176, Issue 1
  • DOI: 10.1104/pp.17.01583

Cereal cyst nematodes: importance, distribution, identification, quantification, and control
journal, June 2017

  • Toumi, Fateh; Waeyenberge, Lieven; Viaene, Nicole
  • European Journal of Plant Pathology, Vol. 150, Issue 1
  • DOI: 10.1007/s10658-017-1263-0

Mycorrhizal ecology and evolution: the past, the present, and the future
journal, February 2015

  • van der Heijden, Marcel G. A.; Martin, Francis M.; Selosse, Marc-André
  • New Phytologist, Vol. 205, Issue 4
  • DOI: 10.1111/nph.13288

Improved Diagnoses and Quantification of Fusarium virguliforme , Causal Agent of Soybean Sudden Death Syndrome
journal, March 2015


Temporal Dynamics of Fusarium virguliforme Colonization of Soybean Roots
journal, January 2019


Detection of external insect infestations in jujube fruit using hyperspectral reflectance imaging
journal, April 2011


Mid-infrared diffuse reflectance spectroscopy for the rapid analysis of plant root composition
journal, November 2011


Sistema de cultivo e doses de nitrogênio na sanidade e no rendimento do milho
journal, February 2013


Precise mapping Fhb5, a major QTL conditioning resistance to Fusarium infection in bread wheat (Triticum aestivum L.)
journal, July 2011


Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply
journal, July 2005

  • Zhu, Jinming; Kaeppler, Shawn M.; Lynch, Jonathan P.
  • Theoretical and Applied Genetics, Vol. 111, Issue 4
  • DOI: 10.1007/s00122-005-2051-3

Chitin Biochemistry: Synthesis And Inhibition
journal, January 1987


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

    Works referencing / citing this record:

    Identification of ergosterol in vesicular-arbuscular mycorrhizae
    journal, August 1992

    • Frey, B.; Buser, H. R.; Sch�epp, H.
    • Biology and Fertility of Soils, Vol. 13, Issue 4
    • DOI: 10.1007/bf00340581

    Biochemical approaches to the study of plant-fungal interactions in arbuscular mycorrhiza
    journal, October 1994

    • Bothe, H.; Klingner, A.; Kaldorf, M.
    • Experientia, Vol. 50, Issue 10
    • DOI: 10.1007/bf01923479

    Scanning electron microscopy of microorganisms on the roots of wheat
    journal, December 1974


    Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply
    journal, July 2005

    • Zhu, Jinming; Kaeppler, Shawn M.; Lynch, Jonathan P.
    • Theoretical and Applied Genetics, Vol. 111, Issue 4
    • DOI: 10.1007/s00122-005-2051-3

    Characterizing variation in mycorrhiza effect among diverse plant varieties
    journal, December 2009

    • Sawers, Ruairidh J. H.; Gebreselassie, Mesfin N.; Janos, David P.
    • Theoretical and Applied Genetics, Vol. 120, Issue 5
    • DOI: 10.1007/s00122-009-1231-y

    Precise mapping Fhb5, a major QTL conditioning resistance to Fusarium infection in bread wheat (Triticum aestivum L.)
    journal, July 2011


    FvSTR1, a striatin orthologue in Fusarium virguliforme, is required for asexual development and virulence
    journal, June 2017

    • Islam, Kazi T.; Bond, Jason P.; Fakhoury, Ahmad M.
    • Applied Microbiology and Biotechnology, Vol. 101, Issue 16
    • DOI: 10.1007/s00253-017-8387-1

    Imaging mycorrhizal fungal transformants that express EGFP during ericoid endosymbiosis
    journal, June 2007


    Nematode feeding sites: unique organs in plant roots
    journal, July 2013


    Distinguishable staining with neutral red for GFP-marked and GFP-nonmarked Fusarium oxysporum strains simultaneously colonizing root surfaces
    journal, February 2003

    • Nonomura, Teruo; Tajima, Hiromi; Kitagawa, Yuko
    • Journal of General Plant Pathology, Vol. 69, Issue 1
    • DOI: 10.1007/s10327-002-0018-7

    Cereal cyst nematodes: importance, distribution, identification, quantification, and control
    journal, June 2017

    • Toumi, Fateh; Waeyenberge, Lieven; Viaene, Nicole
    • European Journal of Plant Pathology, Vol. 150, Issue 1
    • DOI: 10.1007/s10658-017-1263-0

    A Maize Inbred Exhibits Resistance Against Western Corn Rootwoorm, Diabrotica virgifera virgifera
    journal, November 2017

    • Castano-Duque, Lina; Loades, Kenneth W.; Tooker, John F.
    • Journal of Chemical Ecology, Vol. 43, Issue 11-12
    • DOI: 10.1007/s10886-017-0904-2

    Chitin and ergosterol content of extraradical and intraradical mycelium of the vesicular-arbuscular mycorrhizal fungus Glomus intraradices
    journal, June 1994


    Detection of external insect infestations in jujube fruit using hyperspectral reflectance imaging
    journal, April 2011


    Root cap influences root colonisation by Pseudomonas fluorescens SBW25 on maize
    journal, September 2005


    Mid-infrared diffuse reflectance spectroscopy for the rapid analysis of plant root composition
    journal, November 2011


    Early detection of toxigenic fungi on maize by hyperspectral imaging analysis
    journal, November 2010


    Real-time PCR for quantification of eleven individual Fusarium species in cereals
    journal, March 2009

    • Nicolaisen, Mogens; Supronienė, Skaidrė; Nielsen, Linda Kærgaard
    • Journal of Microbiological Methods, Vol. 76, Issue 3
    • DOI: 10.1016/j.mimet.2008.10.016

    Parasitic nematodes have two distinct chitin synthases
    journal, July 2005


    Autofluorescence of Plant Secreting Cells as a Biosensor and Bioindicator Reaction
    journal, September 2003


    Tansley Review No. 96. Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses
    journal, November 1997


    A comparison of visualization techniques for recording arbuscular mycorrhizal colonization
    journal, April 1999


    Chemical control of the cereal cyst nematode (Heterodera avenae) in the Victorian Mallee
    journal, January 1970

    • Brown, Rh; Meagher, Jw; McSwain, Nk
    • Australian Journal of Experimental Agriculture, Vol. 10, Issue 43
    • DOI: 10.1071/ea9700172

    Recent research on fumonisins: a review
    journal, February 2012


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


    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

    New Insights into the Regulation of Aquaporins by the Arbuscular Mycorrhizal Symbiosis in Maize Plants Under Drought Stress and Possible Implications for Plant Performance
    journal, April 2014

    • Bárzana, Gloria; Aroca, Ricardo; Bienert, Gerd Patrick
    • Molecular Plant-Microbe Interactions, Vol. 27, Issue 4
    • DOI: 10.1094/mpmi-09-13-0268-r

    Temporal Dynamics of Fusarium virguliforme Colonization of Soybean Roots
    journal, January 2019


    Transgenic Rootworm Corn: Assessing Potential Agronomic, Economic, and Environmental Benefits
    journal, January 2004


    Suppression of Soybean Yield Potential in the Continental United States by Plant Diseases from 2006 to 2009
    journal, January 2010


    Multilaboratory Comparison of Quantitative PCR Assays for Detection and Quantification of Fusarium virguliforme from Soybean Roots and Soil
    journal, December 2015


    Improved Diagnoses and Quantification of Fusarium virguliforme , Causal Agent of Soybean Sudden Death Syndrome
    journal, March 2015


    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

    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

    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

    Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition
    journal, November 2017

    • Strock, Christopher F.; Morrow de la Riva, Laurie; Lynch, Jonathan P.
    • Plant Physiology, Vol. 176, Issue 1
    • DOI: 10.1104/pp.17.01583

    Behaviour and ecology of the western corn rootworm ( Diabrotica virgifera virgifera LeConte)
    journal, February 2009


    Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots
    journal, October 2007


    Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi?
    journal, November 2008


    Mycorrhizal ecology and evolution: the past, the present, and the future
    journal, February 2015

    • van der Heijden, Marcel G. A.; Martin, Francis M.; Selosse, Marc-André
    • New Phytologist, Vol. 205, Issue 4
    • DOI: 10.1111/nph.13288

    An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis: Systemic responses in mycorrhizal maize
    journal, April 2015

    • Gerlach, Nina; Schmitz, Jessica; Polatajko, Aleksandra
    • Plant, Cell & Environment, Vol. 38, Issue 8
    • DOI: 10.1111/pce.12508

    Reduced root cortical burden improves growth and grain yield under low phosphorus availability in maize: Root cortical burden and phosphorus capture
    journal, May 2018

    • Galindo-Castañeda, Tania; Brown, Kathleen M.; Lynch, Jonathan P.
    • Plant, Cell & Environment, Vol. 41, Issue 7
    • DOI: 10.1111/pce.13197

    Early Events in the Fusarium verticillioides-Maize Interaction Characterized by Using a Green Fluorescent Protein-Expressing Transgenic Isolate
    journal, March 2003


    Colonization of Tomato Root by Pathogenic and Nonpathogenic Fusarium oxysporum Strains Inoculated Together and Separately into the Soil
    journal, February 2006


    Ultraviolet-induced autofluorescence of arbuscular mycorrhizal root infections: an alternative to clearing and staining methods for assessing infections
    journal, March 1982

    • Ames, Robert N.; Ingham, Elaine R.; Reid, C. P. P.
    • Canadian Journal of Microbiology, Vol. 28, Issue 3
    • DOI: 10.1139/m82-052

    Bacterial colonization patterns of intact Pinus sylvestris mycorrhizospheres in dry pine forest soil: an electron microscopy study
    journal, November 1997

    • Nurmiaho-Lassila, E. -L.; Timonen, S.; Haahtela, K.
    • Canadian Journal of Microbiology, Vol. 43, Issue 11
    • DOI: 10.1139/m97-147

    Chitin Biochemistry: Synthesis and Inhibition
    journal, January 1987


    Adaptation and Invasiveness of Western Corn Rootworm: Intensifying Research on a Worsening Pest
    journal, January 2009


    Vital Autofluorescence: Application to the Study of Plant Living Cells
    journal, September 2012

    • Roshchina, Victoria V.
    • International Journal of Spectroscopy, Vol. 2012
    • DOI: 10.1155/2012/124672

    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

    Sistema de cultivo e doses de nitrogênio na sanidade e no rendimento do milho
    journal, February 2013


    Variation in Plant Response to Native and Exotic Arbuscular Mycorrhizal Fungi
    journal, September 2003


    Simple Sequence Repeat Markers Developed from Maize Sequences Found in the GENBANK Database: Map Construction
    journal, January 1996


    Maize Morphology and Shoot CO Assimilation after Root Damage by Western Corn Rootworm Larvae
    journal, January 1999


    Variation among Maize Inbred Lines and Detection of Quantitative Trait Loci for Growth at Low Phosphorus and Responsiveness to Arbuscular Mycorrhizal Fungi
    journal, January 2000


    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

    Imaging and Spectroscopy of Natural Fluorophores in Pine Needles
    journal, February 2018


    Transparent soil microcosms allow 3D spatial quantification of soil microbiological processes in vivo
    journal, October 2014


    Genetic components of root architecture and anatomy adjustments to water‐deficit stress in spring barley
    journal, December 2019

    • Oyiga, Benedict C.; Palczak, Janina; Wojciechowski, Tobias
    • Plant, Cell & Environment, Vol. 43, Issue 3
    • DOI: 10.1111/pce.13683