skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil

Abstract

Maize domestication and breeding have resulted in drastic and well documented changes in aboveground traits, but belowground effects on root system functioning and rhizosphere microbial communities remain poorly understood, despite their critical importance for nutrient and water acquisition. We investigated the rhizosphere microbial community composition and structure of ten Zea mays accessions along an evolutionary transect (two teosinte, three inbred maize lines, and five modern maize hybrids) grown in nutrient depleted soil from a low input agricultural system. Microbial community analysis revealed significant differences in community composition between soil compartments (proximal vs. distal rhizosphere) and between plant genetic groups (teosinte, inbred, and modern hybrid). Only a small portion of the microbial community was differentially selected across plant genetic groups: 3.7% of prokaryotic community members and 4.9% of fungal community members were significantly associated with a specific plant genetic group. Indicator species analysis showed the greatest differentiation between modern hybrids and the other two plant genetic groups. Co-occurrence network analysis revealed that microbial co-occurrence patterns of the inbred maize lines’ rhizosphere were significantly more similar to those of the teosintes than to the modern hybrids. Furthermore, our results suggest that advances in hybrid development significantly impacted rhizosphere microbial communities and networkmore » assembly.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4];  [5]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  2. Univ. of California, Davis, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Davis, CA (United States)
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1577951
Report Number(s):
LLNL-JRNL-776809
Journal ID: ISSN 2045-2322; 969968
Grant/Contract Number:  
AC52-07NA27344; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Brisson, Vanessa L., Schmidt, Jennifer E., Northen, Trent R., Vogel, John P., and Gaudin, Amélie C. M. Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil. United States: N. p., 2019. Web. doi:10.1038/s41598-019-52148-y.
Brisson, Vanessa L., Schmidt, Jennifer E., Northen, Trent R., Vogel, John P., & Gaudin, Amélie C. M. Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil. United States. doi:10.1038/s41598-019-52148-y.
Brisson, Vanessa L., Schmidt, Jennifer E., Northen, Trent R., Vogel, John P., and Gaudin, Amélie C. M. Wed . "Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil". United States. doi:10.1038/s41598-019-52148-y. https://www.osti.gov/servlets/purl/1577951.
@article{osti_1577951,
title = {Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil},
author = {Brisson, Vanessa L. and Schmidt, Jennifer E. and Northen, Trent R. and Vogel, John P. and Gaudin, Amélie C. M.},
abstractNote = {Maize domestication and breeding have resulted in drastic and well documented changes in aboveground traits, but belowground effects on root system functioning and rhizosphere microbial communities remain poorly understood, despite their critical importance for nutrient and water acquisition. We investigated the rhizosphere microbial community composition and structure of ten Zea mays accessions along an evolutionary transect (two teosinte, three inbred maize lines, and five modern maize hybrids) grown in nutrient depleted soil from a low input agricultural system. Microbial community analysis revealed significant differences in community composition between soil compartments (proximal vs. distal rhizosphere) and between plant genetic groups (teosinte, inbred, and modern hybrid). Only a small portion of the microbial community was differentially selected across plant genetic groups: 3.7% of prokaryotic community members and 4.9% of fungal community members were significantly associated with a specific plant genetic group. Indicator species analysis showed the greatest differentiation between modern hybrids and the other two plant genetic groups. Co-occurrence network analysis revealed that microbial co-occurrence patterns of the inbred maize lines’ rhizosphere were significantly more similar to those of the teosintes than to the modern hybrids. Furthermore, our results suggest that advances in hybrid development significantly impacted rhizosphere microbial communities and network assembly.},
doi = {10.1038/s41598-019-52148-y},
journal = {Scientific Reports},
number = 1,
volume = 9,
place = {United States},
year = {2019},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities
journal, December 2010


Plant-Growth-Promoting Rhizobacteria
journal, October 2009


Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011


Associations between species and groups of sites: indices and statistical inference
journal, December 2009

  • Cáceres, Miquel De; Legendre, Pierre
  • Ecology, Vol. 90, Issue 12
  • DOI: 10.1890/08-1823.1

Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota
journal, August 2018


The evolution of apical dominance in maize
journal, April 1997

  • Doebley, John; Stec, Adrian; Hubbard, Lauren
  • Nature, Vol. 386, Issue 6624
  • DOI: 10.1038/386485a0

Evolution of the Crop Rhizosphere: Impact of Domestication on Root Exudates in Tetraploid Wheat (Triticum turgidum L.)
journal, December 2017

  • Iannucci, Anna; Fragasso, Mariagiovanna; Beleggia, Romina
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.02124

Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity
journal, October 2007

  • Nadeem, Sajid Mahmood; Zahir, Zahir Ahmad; Naveed, Muhammad
  • Canadian Journal of Microbiology, Vol. 53, Issue 10
  • DOI: 10.1139/W07-081

The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes
journal, July 2015

  • Hardoim, Pablo R.; van Overbeek, Leonard S.; Berg, Gabriele
  • Microbiology and Molecular Biology Reviews, Vol. 79, Issue 3
  • DOI: 10.1128/MMBR.00050-14

Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018


Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review
journal, January 2015


Simplified and representative bacterial community of maize roots
journal, March 2017

  • Niu, Ben; Paulson, Joseph Nathaniel; Zheng, Xiaoqi
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
  • DOI: 10.1073/pnas.1616148114

Large-scale replicated field study of maize rhizosphere identifies heritable microbes
journal, June 2018

  • Walters, William A.; Jin, Zhao; Youngblut, Nicholas
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
  • DOI: 10.1073/pnas.1800918115

Glomeromycota associated with Mexican native maize landraces in Los Tuxtlas, Mexico
journal, March 2015

  • Sangabriel-Conde, Wendy; Maldonado-Mendoza, Ignacio E.; Mancera-López, Maria Elena
  • Applied Soil Ecology, Vol. 87
  • DOI: 10.1016/j.apsoil.2014.10.017

The Role of Host Genetic Signatures on Root–Microbe Interactions in the Rhizosphere and Endosphere
journal, December 2018


Impact of plant domestication on rhizosphere microbiome assembly and functions
journal, June 2015

  • Pérez-Jaramillo, Juan E.; Mendes, Rodrigo; Raaijmakers, Jos M.
  • Plant Molecular Biology, Vol. 90, Issue 6
  • DOI: 10.1007/s11103-015-0337-7

Comparison of root system architecture and rhizosphere microbial communities of Balsas teosinte and domesticated corn cultivars
journal, January 2015


Abiotic Stress Responses and Microbe-Mediated Mitigation in Plants: The Omics Strategies
journal, February 2017

  • Meena, Kamlesh K.; Sorty, Ajay M.; Bitla, Utkarsh M.
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.00172

Synthesis of Phytohormones by Plant-Associated Bacteria
journal, January 1995


Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton
journal, June 2015

  • Apprill, A.; McNally, S.; Parsons, R.
  • Aquatic Microbial Ecology, Vol. 75, Issue 2
  • DOI: 10.3354/ame01753

Defining the core Arabidopsis thaliana root microbiome
journal, August 2012

  • Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11237

Taxonomy annotation and guide tree errors in 16S rRNA databases
journal, January 2018


New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities
journal, July 2012


Ribosomal Database Project: data and tools for high throughput rRNA analysis
journal, November 2013

  • Cole, James R.; Wang, Qiong; Fish, Jordan A.
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1244

Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower, Helianthus annuus
journal, November 2016

  • Leff, Jonathan W.; Lynch, Ryan C.; Kane, Nolan C.
  • New Phytologist, Vol. 214, Issue 1
  • DOI: 10.1111/nph.14323

Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China
journal, January 2016


A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system
journal, June 2012

  • Barillot, Cindy D. C.; Sarde, Claude-Olivier; Bert, Valerie
  • Annals of Microbiology, Vol. 63, Issue 2
  • DOI: 10.1007/s13213-012-0491-y

Root microbiome relates to plant host evolution in maize and other Poaceae: Poaceae evolution and root bacteria
journal, April 2014

  • Bouffaud, Marie-Lara; Poirier, Marie-Andrée; Muller, Daniel
  • Environmental Microbiology, Vol. 16, Issue 9
  • DOI: 10.1111/1462-2920.12442

phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013


Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress
journal, March 2015

  • York, L. M.; Galindo-Castaneda, T.; Schussler, J. R.
  • Journal of Experimental Botany, Vol. 66, Issue 8
  • DOI: 10.1093/jxb/erv074

Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants
journal, March 2014

  • Marques, Joana M.; da Silva, Thais F.; Vollu, Renata E.
  • FEMS Microbiology Ecology, Vol. 88, Issue 2
  • DOI: 10.1111/1574-6941.12313

Towards a unified paradigm for sequence-based identification of fungi
journal, September 2013

  • Kõljalg, Urmas; Nilsson, R. Henrik; Abarenkov, Kessy
  • Molecular Ecology, Vol. 22, Issue 21
  • DOI: 10.1111/mec.12481

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

The century experiment: the first twenty years of UC Davis' Mediterranean agroecological experiment
journal, January 2018

  • Wolf, Kristina M.; Torbert, Emma E.; Bryant, Dennis
  • Ecology, Vol. 99, Issue 2
  • DOI: 10.1002/ecy.2105

The Nitrogen Adaptation Strategy of the Wild Teosinte Ancestor of Modern Maize, subsp.
journal, January 2011


Fungal Communities in Rhizosphere Soil under Conservation Tillage Shift in Response to Plant Growth
journal, July 2017


The ecology of the microbiome: Networks, competition, and stability
journal, November 2015


Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley
journal, March 2015

  • Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C.
  • Cell Host & Microbe, Vol. 17, Issue 3
  • DOI: 10.1016/j.chom.2015.01.011

Eighty years of maize breeding alters plant nitrogen acquisition but not rhizosphere bacterial community composition
journal, July 2018

  • Emmett, Bryan D.; Buckley, Daniel H.; Smith, Margaret E.
  • Plant and Soil, Vol. 431, Issue 1-2
  • DOI: 10.1007/s11104-018-3744-0

The rhizosphere microbiome and plant health
journal, August 2012

  • Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M.
  • Trends in Plant Science, Vol. 17, Issue 8
  • DOI: 10.1016/j.tplants.2012.04.001

Phylogenetic diversity of Mesorhizobium in chickpea
journal, April 2014

  • Kim, Dong Hyun; Kaashyap, Mayank; Rathore, Abhishek
  • Journal of Biosciences, Vol. 39, Issue 3
  • DOI: 10.1007/s12038-014-9429-9

The effect of altered dosage of a mutant allele of Teosinte branched 1 (tb1-ref) on the root system of modern maize
journal, January 2014

  • Gaudin, Amelie CM; McClymont, Sarah A.; Soliman, Sameh SM
  • BMC Genetics, Vol. 15, Issue 1
  • DOI: 10.1186/1471-2156-15-23

Global maize production, utilization, and consumption: Maize production, utilization, and consumption
journal, March 2014

  • Ranum, Peter; Peña-Rosas, Juan Pablo; Garcia-Casal, Maria Nieves
  • Annals of the New York Academy of Sciences, Vol. 1312, Issue 1
  • DOI: 10.1111/nyas.12396

Deciphering microbial interactions and detecting keystone species with co-occurrence networks
journal, May 2014


Below-ground connections underlying above-ground food production: a framework for optimising ecological connections in the rhizosphere
journal, June 2017

  • de Vries, Franciska T.; Wallenstein, Matthew D.
  • Journal of Ecology, Vol. 105, Issue 4
  • DOI: 10.1111/1365-2745.12783

Complete Genome Sequence of the Metabolically Versatile Plant Growth-Promoting Endophyte Variovorax paradoxus S110
journal, December 2010

  • Han, J. -I.; Choi, H. -K.; Lee, S. -W.
  • Journal of Bacteriology, Vol. 193, Issue 5
  • DOI: 10.1128/JB.00925-10

The rhizosphere bacterium Variovorax paradoxus 5C-2 containing ACC deaminase does not increase systemic ABA signaling in maize ( Zea mays L.)
journal, June 2009

  • Dodd, Ian C.; Jiang, Fan; Teijeiro, Rosalia Garcia
  • Plant Signaling & Behavior, Vol. 4, Issue 6
  • DOI: 10.4161/psb.4.6.8574

Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species
journal, October 2015

  • Coleman-Derr, Devin; Desgarennes, Damaris; Fonseca-Garcia, Citlali
  • New Phytologist, Vol. 209, Issue 2
  • DOI: 10.1111/nph.13697

Diversity and heritability of the maize rhizosphere microbiome under field conditions
journal, April 2013

  • Peiffer, J. A.; Spor, A.; Koren, O.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
  • DOI: 10.1073/pnas.1302837110

The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
journal, June 2016

  • Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.
  • Ecology Letters, Vol. 19, Issue 8
  • DOI: 10.1111/ele.12630

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Drought and host selection influence bacterial community dynamics in the grass root microbiome
journal, July 2017

  • Naylor, Dan; DeGraaf, Stephanie; Purdom, Elizabeth
  • The ISME Journal, Vol. 11, Issue 12
  • DOI: 10.1038/ismej.2017.118