DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Large-scale replicated field study of maize rhizosphere identifies heritable microbes

Abstract

Up until now, soil microbes that colonize plant roots and are responsive to differences in plant genotype remain to be ascertained for agronomically important crops. From a very large-scale longitudinal field study of 27 maize inbred lines planted in three fields, with partial replication 5 y later, we identify root-associated microbiota exhibiting reproducible associations with plant genotype. Analysis of 4,866 samples identified 143 operational taxonomic units (OTUs) whose variation in relative abundances across the samples was significantly regulated by plant genotype, and included five of seven core OTUs present in all samples. Plant genetic effects were significant amid the large effects of plant age on the rhizosphere microbiome, regardless of the specific community of each field, and despite microbiome responses to climate events. Seasonal patterns showed that the plant root microbiome is locally seeded, changes with plant growth, and responds to weather events. However, against this background of variation, specific taxa responded to differences in host genotype. If shown to have beneficial functions, microbes may be considered candidate traits for selective breeding.

Authors:
 [1];  [2];  [1];  [3];  [1];  [2];  [4];  [2]; ORCiD logo [5];  [2];  [6];  [7]; ORCiD logo [7]; ORCiD logo [8];  [9];  [10]
  1. Max Planck Institute for Developmental Biology, Tubingen (Germany)
  2. Cornell Univ., Ithaca, NY (United States)
  3. Univ. of Georgia, Athens, GA (United States)
  4. Univ. of California, San Diego, La Jolla, CA (United States)
  5. Cornell Univ., Ithaca, NY (United States); Bar Ilan Univ., Safed (Israel)
  6. Univ. of Georgia, Athens, GA (United States); Univ. of California, San Diego, La Jolla, CA (United States)
  7. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  8. United States Dept. of Agriculture - Agricultural Research Service, Ithaca, NY (United States); Cornell Univ., Ithaca, NY (United States)
  9. Univ. of North Carolina, Chapel Hill, NC (United States)
  10. Max Planck Institute for Developmental Biology, Tubingen (Germany); Cornell Univ., Ithaca, NY (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE; National Science Foundation (NSF); USDA Agricultural Research Service
OSTI Identifier:
1482534
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 28; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; maize; rhizosphere; soil microbiome; heritability; field study

Citation Formats

Walters, William A., Jin, Zhao, Youngblut, Nicholas, Wallace, Jason G., Sutter, Jessica, Zhang, Wei, González-Peña, Antonio, Peiffer, Jason, Koren, Omry, Shi, Qiaojuan, Knight, Rob, Glavina del Rio, Tijana, Tringe, Susannah G., Buckler, Edward S., Dangl, Jeffery L., and Ley, Ruth E. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. United States: N. p., 2018. Web. doi:10.1073/pnas.1800918115.
Walters, William A., Jin, Zhao, Youngblut, Nicholas, Wallace, Jason G., Sutter, Jessica, Zhang, Wei, González-Peña, Antonio, Peiffer, Jason, Koren, Omry, Shi, Qiaojuan, Knight, Rob, Glavina del Rio, Tijana, Tringe, Susannah G., Buckler, Edward S., Dangl, Jeffery L., & Ley, Ruth E. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. United States. https://doi.org/10.1073/pnas.1800918115
Walters, William A., Jin, Zhao, Youngblut, Nicholas, Wallace, Jason G., Sutter, Jessica, Zhang, Wei, González-Peña, Antonio, Peiffer, Jason, Koren, Omry, Shi, Qiaojuan, Knight, Rob, Glavina del Rio, Tijana, Tringe, Susannah G., Buckler, Edward S., Dangl, Jeffery L., and Ley, Ruth E. Mon . "Large-scale replicated field study of maize rhizosphere identifies heritable microbes". United States. https://doi.org/10.1073/pnas.1800918115. https://www.osti.gov/servlets/purl/1482534.
@article{osti_1482534,
title = {Large-scale replicated field study of maize rhizosphere identifies heritable microbes},
author = {Walters, William A. and Jin, Zhao and Youngblut, Nicholas and Wallace, Jason G. and Sutter, Jessica and Zhang, Wei and González-Peña, Antonio and Peiffer, Jason and Koren, Omry and Shi, Qiaojuan and Knight, Rob and Glavina del Rio, Tijana and Tringe, Susannah G. and Buckler, Edward S. and Dangl, Jeffery L. and Ley, Ruth E.},
abstractNote = {Up until now, soil microbes that colonize plant roots and are responsive to differences in plant genotype remain to be ascertained for agronomically important crops. From a very large-scale longitudinal field study of 27 maize inbred lines planted in three fields, with partial replication 5 y later, we identify root-associated microbiota exhibiting reproducible associations with plant genotype. Analysis of 4,866 samples identified 143 operational taxonomic units (OTUs) whose variation in relative abundances across the samples was significantly regulated by plant genotype, and included five of seven core OTUs present in all samples. Plant genetic effects were significant amid the large effects of plant age on the rhizosphere microbiome, regardless of the specific community of each field, and despite microbiome responses to climate events. Seasonal patterns showed that the plant root microbiome is locally seeded, changes with plant growth, and responds to weather events. However, against this background of variation, specific taxa responded to differences in host genotype. If shown to have beneficial functions, microbes may be considered candidate traits for selective breeding.},
doi = {10.1073/pnas.1800918115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 28,
volume = 115,
place = {United States},
year = {Mon Jun 25 00:00:00 EDT 2018},
month = {Mon Jun 25 00:00:00 EDT 2018}
}

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

Citation Metrics:
Cited by: 263 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

A Genome-Wide Association Study of the Maize Hypersensitive Defense Response Identifies Genes That Cluster in Related Pathways
journal, August 2014


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


Rhizosphere microbiomes of potato cultivated in the High Andes show stable and dynamic core microbiomes with different responses to plant development
journal, December 2016

  • Pfeiffer, Stefan; Mitter, Birgit; Oswald, Andreas
  • FEMS Microbiology Ecology, Vol. 93, Issue 2
  • DOI: 10.1093/femsec/fiw242

Going back to the roots: the microbial ecology of the rhizosphere
journal, September 2013

  • Philippot, Laurent; Raaijmakers, Jos M.; Lemanceau, Philippe
  • Nature Reviews Microbiology, Vol. 11, Issue 11
  • DOI: 10.1038/nrmicro3109

Rice root-associated bacteria: insights into community structures across 10 cultivars: Insights into the bacterial community structure of rice cultivars
journal, April 2011


The evolution of quantitative traits in complex environments
journal, April 2013

  • Anderson, J. T.; Wagner, M. R.; Rushworth, C. A.
  • Heredity, Vol. 112, Issue 1
  • DOI: 10.1038/hdy.2013.33

Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils
journal, July 2017

  • Schlemper, Thiago R.; Leite, Márcio F. A.; Lucheta, Adriano R.
  • FEMS Microbiology Ecology, Vol. 93, Issue 8
  • DOI: 10.1093/femsec/fix096

Characterization of the maize gene sugary1, a determinant of starch composition in kernels.
journal, April 1995

  • James, M. G.; Robertson, D. S.; Myers, A. M.
  • The Plant Cell, Vol. 7, Issue 4
  • DOI: 10.1105/tpc.7.4.417

Host genotype and age shape the leaf and root microbiomes of a wild perennial plant
journal, July 2016

  • Wagner, Maggie R.; Lundberg, Derek S.; del Rio, Tijana G.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12151

Maize HapMap2 identifies extant variation from a genome in flux
journal, June 2012

  • Chia, Jer-Ming; Song, Chi; Bradbury, Peter J.
  • Nature Genetics, Vol. 44, Issue 7
  • DOI: 10.1038/ng.2313

Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa
journal, July 2015


Bacterial diversity in the rhizosphere of maize and the surrounding carbonate-rich bulk soil: Biodiversity in adjacent niches
journal, August 2012


Heritability in the genomics era — concepts and misconceptions
journal, March 2008

  • Visscher, Peter M.; Hill, William G.; Wray, Naomi R.
  • Nature Reviews Genetics, Vol. 9, Issue 4
  • DOI: 10.1038/nrg2322

Beyond the Venn diagram: the hunt for a core microbiome: The hunt for a core microbiome
journal, October 2011


Genetic Properties of the Maize Nested Association Mapping Population
journal, August 2009


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

A new view of the tree of life
journal, April 2016


Maize association population: a high-resolution platform for quantitative trait locus dissection
journal, November 2005


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

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

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


Genome-wide Association Studies in Maize: Praise and Stargaze
journal, March 2017


Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota
journal, August 2012

  • Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11336

Can a diazotrophic endophyte originally isolated from lodgepole pine colonize an agricultural crop (corn) and promote its growth?
journal, October 2015


Organ-Specific Invertase Deficiency in the Primary Root of an Inbred Maize Line
journal, October 1991

  • Duke, Edwin R.; McCarty, Donald R.; Koch, Karen E.
  • Plant Physiology, Vol. 97, Issue 2
  • DOI: 10.1104/pp.97.2.523

Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce
journal, April 2014


The Diversity of Archaea and Bacteria in Association with the Roots of Zea mays L.
journal, February 2001


Fitting Linear Mixed-Effects Models Using lme4
journal, January 2015

  • Bates, Douglas; Mächler, Martin; Bolker, Ben
  • Journal of Statistical Software, Vol. 67, Issue 1
  • DOI: 10.18637/jss.v067.i01

Edaphic properties override the influence of crops on the composition of the soil bacterial community in a semiarid agroecosystem
journal, September 2016


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

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

Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits
journal, June 2017

  • Pérez-Jaramillo, Juan E.; Carrión, Víctor J.; Bosse, Mirte
  • The ISME Journal, Vol. 11, Issue 10
  • DOI: 10.1038/ismej.2017.85

Host genotype and age shape the leaf and root microbiomes of a wild perennial plant
text, January 2016

  • S., Lundberg, Derek; L., Dangl, Jeffery; G., Del Rio, Tijana
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/18y1-ek17

Characterization of the Maize Gene sugary1, a Determinant of Starch Composition in Kernels
journal, April 1995

  • James, Martha G.; Robertson, Donald S.; Myers, Alan M.
  • The Plant Cell, Vol. 7, Issue 4
  • DOI: 10.2307/3870080

Diversity and heritability of the maize rhizosphere microbiome under field conditions
text, January 2013

  • Z., Jin,; S., Buckler, E.; O., Koren,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/rzga-0c56

The Diversity of Archaea and Bacteria in Association with the Roots of Zea mays L.
journal, February 2001


Edaphic properties override the influence of crops on the composition of the soil bacterial community in a semiarid agroecosystem
journal, September 2016


Genome-wide Association Studies in Maize: Praise and Stargaze
journal, March 2017


Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits
journal, June 2017

  • Pérez-Jaramillo, Juan E.; Carrión, Víctor J.; Bosse, Mirte
  • The ISME Journal, Vol. 11, Issue 10
  • DOI: 10.1038/ismej.2017.85

Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota
journal, August 2012

  • Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11336

Heritability in the genomics era — concepts and misconceptions
journal, March 2008

  • Visscher, Peter M.; Hill, William G.; Wray, Naomi R.
  • Nature Reviews Genetics, Vol. 9, Issue 4
  • DOI: 10.1038/nrg2322

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

Rhizosphere microbiomes of potato cultivated in the High Andes show stable and dynamic core microbiomes with different responses to plant development
journal, December 2016

  • Pfeiffer, Stefan; Mitter, Birgit; Oswald, Andreas
  • FEMS Microbiology Ecology, Vol. 93, Issue 2
  • DOI: 10.1093/femsec/fiw242

Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils
journal, July 2017

  • Schlemper, Thiago R.; Leite, Márcio F. A.; Lucheta, Adriano R.
  • FEMS Microbiology Ecology, Vol. 93, Issue 8
  • DOI: 10.1093/femsec/fix096

Organ-Specific Invertase Deficiency in the Primary Root of an Inbred Maize Line
journal, October 1991

  • Duke, Edwin R.; McCarty, Donald R.; Koch, Karen E.
  • Plant Physiology, Vol. 97, Issue 2
  • DOI: 10.1104/pp.97.2.523

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

A Genome-Wide Association Study of the Maize Hypersensitive Defense Response Identifies Genes That Cluster in Related Pathways
journal, August 2014


Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce
journal, April 2014


Works referencing / citing this record:

Prokaryotic taxa play keystone roles in the soil microbiome associated with woody perennial plants in the genus Buxus
journal, August 2019

  • LeBlanc, Nicholas; Crouch, Jo Anne
  • Ecology and Evolution, Vol. 9, Issue 19
  • DOI: 10.1002/ece3.5614

Assembly of root-associated microbial community of typical rice cultivars in different soil types
journal, December 2019


Rhizosphere microbiome structure alters to enable wilt resistance in tomato
journal, October 2018

  • Kwak, Min-Jung; Kong, Hyun Gi; Choi, Kihyuck
  • Nature Biotechnology, Vol. 36, Issue 11
  • DOI: 10.1038/nbt.4232

Local biotic interactions drive species-specific divergence in soil bacterial communities
journal, July 2019


The structure and function of the global citrus rhizosphere microbiome
journal, November 2018


NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice
journal, April 2019


Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil
journal, October 2019

  • Brisson, Vanessa L.; Schmidt, Jennifer E.; Northen, Trent R.
  • Scientific Reports, Vol. 9, Issue 1
  • DOI: 10.1038/s41598-019-52148-y

Evidence of within-species specialization by soil microbes and the implications for plant community diversity
journal, March 2019

  • Eck, Jenalle L.; Stump, Simon M.; Delavaux, Camille S.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 15
  • DOI: 10.1073/pnas.1810767116

Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome
journal, May 2019

  • Voges, Mathias J. E. E. E.; Bai, Yang; Schulze-Lefert, Paul
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 25
  • DOI: 10.1073/pnas.1820691116

Maternal microbes complicate coexistence for tropical trees
journal, April 2019

  • Rogers, Haldre S.; Fricke, Evan C.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 15
  • DOI: 10.1073/pnas.1902736116

Plants exhibit significant effects on the rhizospheric microbiome across contrasting soils in tropical and subtropical China
journal, July 2019

  • Xu, Shangqi; Tian, Lei; Chang, Chunling
  • FEMS Microbiology Ecology, Vol. 95, Issue 8
  • DOI: 10.1093/femsec/fiz100

Eco‐holobiont: A new concept to identify drivers of host‐associated microorganisms
journal, December 2019

  • Singh, Brajesh K.; Liu, Hongwei; Trivedi, Pankaj
  • Environmental Microbiology, Vol. 22, Issue 2
  • DOI: 10.1111/1462-2920.14900

Plant adaptation and speciation studied by population genomic approaches
journal, November 2018

  • Bamba, Masaru; Kawaguchi, Yawako W.; Tsuchimatsu, Takashi
  • Development, Growth & Differentiation, Vol. 61, Issue 1
  • DOI: 10.1111/dgd.12578

Plant growth rate and nitrogen uptake shape rhizosphere bacterial community composition and activity in an agricultural field
journal, October 2019

  • Emmett, Bryan D.; Buckley, Daniel H.; Drinkwater, Laurie E.
  • New Phytologist, Vol. 225, Issue 2
  • DOI: 10.1111/nph.16171

Core Microbiota in Agricultural Soils and Their Potential Associations with Nutrient Cycling
journal, March 2019


Maize synthesized benzoxazinoids affect the host associated microbiome
journal, April 2019

  • Kudjordjie, Enoch Narh; Sapkota, Rumakanta; Steffensen, Stine K.
  • Microbiome, Vol. 7, Issue 1
  • DOI: 10.1186/s40168-019-0677-7

The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts
journal, May 2020


The influence of host genetics on the microbiome
journal, January 2020


The home field advantage of modern plant breeding
journal, December 2019


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


Exploration of Plant-Microbe Interactions for Sustainable Agriculture in CRISPR Era
journal, August 2019


Lablab Purpureus Influences Soil Fertility and Microbial Diversity in a Tropical Maize-Based No-Tillage System
journal, August 2019


Heterosis of leaf and rhizosphere microbiomes in field‐grown maize
journal, July 2020

  • Wagner, Maggie R.; Roberts, Joseph H.; Balint‐Kurti, Peter
  • New Phytologist, Vol. 228, Issue 3
  • DOI: 10.1111/nph.16730

Nitrogen Fertilizers Shape the Composition and Predicted Functions of the Microbiota of Field-Grown Tomato Plants
journal, January 2019


Influence of plant genotype and soil on the wheat rhizosphere microbiome: evidences for a core microbiome across eight African and European soils
journal, April 2020

  • Simonin, Marie; Dasilva, Cindy; Terzi, Valeria
  • FEMS Microbiology Ecology, Vol. 96, Issue 6
  • DOI: 10.1093/femsec/fiaa067

The influence of host genetics on the microbiome
text, January 2020


Prokaryotic taxa play keystone roles in the soil microbiome associated with woody perennial plants in the genus Buxus
journal, August 2019

  • LeBlanc, Nicholas; Crouch, Jo Anne
  • Ecology and Evolution, Vol. 9, Issue 19
  • DOI: 10.1002/ece3.5614

The structure and function of the global citrus rhizosphere microbiome
journal, November 2018


Impacts of Maize Domestication and Breeding on Rhizosphere Microbial Community Recruitment from a Nutrient Depleted Agricultural Soil
journal, October 2019

  • Brisson, Vanessa L.; Schmidt, Jennifer E.; Northen, Trent R.
  • Scientific Reports, Vol. 9, Issue 1
  • DOI: 10.1038/s41598-019-52148-y

Nitrogen Fertilizers Shape the Composition and Predicted Functions of the Microbiota of Field-Grown Tomato Plants
journal, January 2019


Soil microbiota influences clubroot disease by modulating Plasmodiophora brassicae and Brassica napus transcriptomes
journal, July 2020

  • Daval, Stéphanie; Gazengel, Kévin; Belcour, Arnaud
  • Microbial Biotechnology, Vol. 13, Issue 5
  • DOI: 10.1111/1751-7915.13634

Core Microbiota in Agricultural Soils and Their Potential Associations with Nutrient Cycling
journal, March 2019


Maize synthesized benzoxazinoids affect the host associated microbiome
journal, April 2019

  • Kudjordjie, Enoch Narh; Sapkota, Rumakanta; Steffensen, Stine K.
  • Microbiome, Vol. 7, Issue 1
  • DOI: 10.1186/s40168-019-0677-7

Spatiotemporal Dynamics of Maize (Zea mays L.) Root Growth and Its Potential Consequences for the Assembly of the Rhizosphere Microbiota
journal, March 2021


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