Structure, variation, and assembly of the root-associated microbiomes of rice

Joseph Edwards, Cameron Johnson, Christian Santos-Medellín, Eugene Lurie, Natraj Kumar Podishetty, Srijak Bhatnagar, Jonathan A Eisen, Venkatesan Sundaresan, L. Dangl Jeffery

Research output: Contribution to journalArticle

404 Citations (Scopus)

Abstract

Plants depend upon beneficial interactions between roots and microbes for nutrient availability, growth promotion, and disease suppression. High-throughput sequencing approaches have provided recent insights into root microbiomes, but our current understanding is still limited relative to animal microbiomes. Here we present a detailed characterization of the root-associated microbiomes of the crop plant rice by deep sequencing, using plants grown under controlled conditions as well as field cultivation at multiple sites. The spatial resolution of the study distinguished three root-associated compartments, the endosphere (root interior), rhizoplane (root surface), and rhizosphere (soil close to the root surface), each of which was found to harbor a distinct microbiome. Under controlled greenhouse conditions, microbiome composition varied with soil source and genotype. In field conditions, geographical location and cultivation practice, namely organic vs. conventional, were factors contributing to microbiome variation. Rice cultivation is a major source of global methane emissions, and methanogenic archaea could be detected in all spatial compartments of field-grown rice. The depth and scale of this study were used to build coabundance networks that revealed potential microbial consortia, some of which were involved in methane cycling. Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role. Similarities in the distribution of phyla in the root microbiomes of rice and other plants suggest that conclusions derived from this study might be generally applicable to land plants.

Original languageEnglish (US)
Pages (from-to)E911-E920
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number8
DOIs
StatePublished - Feb 24 2015

Fingerprint

Microbiota
Soil
Methane
Microbial Consortia
Embryophyta
Oryza
High-Throughput Nucleotide Sequencing
Rhizosphere
Archaea
Genotype
Food
Growth

Keywords

  • Methane cycling
  • Microbiome assembly
  • Microbiomes
  • Rice
  • Soil microbial communities

ASJC Scopus subject areas

  • General

Cite this

Edwards, J., Johnson, C., Santos-Medellín, C., Lurie, E., Podishetty, N. K., Bhatnagar, S., ... Jeffery, L. D. (2015). Structure, variation, and assembly of the root-associated microbiomes of rice. Proceedings of the National Academy of Sciences of the United States of America, 112(8), E911-E920. https://doi.org/10.1073/pnas.1414592112

Structure, variation, and assembly of the root-associated microbiomes of rice. / Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian; Lurie, Eugene; Podishetty, Natraj Kumar; Bhatnagar, Srijak; Eisen, Jonathan A; Sundaresan, Venkatesan; Jeffery, L. Dangl.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 8, 24.02.2015, p. E911-E920.

Research output: Contribution to journalArticle

Edwards, J, Johnson, C, Santos-Medellín, C, Lurie, E, Podishetty, NK, Bhatnagar, S, Eisen, JA, Sundaresan, V & Jeffery, LD 2015, 'Structure, variation, and assembly of the root-associated microbiomes of rice', Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 8, pp. E911-E920. https://doi.org/10.1073/pnas.1414592112
Edwards, Joseph ; Johnson, Cameron ; Santos-Medellín, Christian ; Lurie, Eugene ; Podishetty, Natraj Kumar ; Bhatnagar, Srijak ; Eisen, Jonathan A ; Sundaresan, Venkatesan ; Jeffery, L. Dangl. / Structure, variation, and assembly of the root-associated microbiomes of rice. In: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; Vol. 112, No. 8. pp. E911-E920.
@article{057a00afa49e4081903fe8c4b9e2f667,
title = "Structure, variation, and assembly of the root-associated microbiomes of rice",
abstract = "Plants depend upon beneficial interactions between roots and microbes for nutrient availability, growth promotion, and disease suppression. High-throughput sequencing approaches have provided recent insights into root microbiomes, but our current understanding is still limited relative to animal microbiomes. Here we present a detailed characterization of the root-associated microbiomes of the crop plant rice by deep sequencing, using plants grown under controlled conditions as well as field cultivation at multiple sites. The spatial resolution of the study distinguished three root-associated compartments, the endosphere (root interior), rhizoplane (root surface), and rhizosphere (soil close to the root surface), each of which was found to harbor a distinct microbiome. Under controlled greenhouse conditions, microbiome composition varied with soil source and genotype. In field conditions, geographical location and cultivation practice, namely organic vs. conventional, were factors contributing to microbiome variation. Rice cultivation is a major source of global methane emissions, and methanogenic archaea could be detected in all spatial compartments of field-grown rice. The depth and scale of this study were used to build coabundance networks that revealed potential microbial consortia, some of which were involved in methane cycling. Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role. Similarities in the distribution of phyla in the root microbiomes of rice and other plants suggest that conclusions derived from this study might be generally applicable to land plants.",
keywords = "Methane cycling, Microbiome assembly, Microbiomes, Rice, Soil microbial communities",
author = "Joseph Edwards and Cameron Johnson and Christian Santos-Medell{\'i}n and Eugene Lurie and Podishetty, {Natraj Kumar} and Srijak Bhatnagar and Eisen, {Jonathan A} and Venkatesan Sundaresan and Jeffery, {L. Dangl}",
year = "2015",
month = "2",
day = "24",
doi = "10.1073/pnas.1414592112",
language = "English (US)",
volume = "112",
pages = "E911--E920",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "8",

}

TY - JOUR

T1 - Structure, variation, and assembly of the root-associated microbiomes of rice

AU - Edwards, Joseph

AU - Johnson, Cameron

AU - Santos-Medellín, Christian

AU - Lurie, Eugene

AU - Podishetty, Natraj Kumar

AU - Bhatnagar, Srijak

AU - Eisen, Jonathan A

AU - Sundaresan, Venkatesan

AU - Jeffery, L. Dangl

PY - 2015/2/24

Y1 - 2015/2/24

N2 - Plants depend upon beneficial interactions between roots and microbes for nutrient availability, growth promotion, and disease suppression. High-throughput sequencing approaches have provided recent insights into root microbiomes, but our current understanding is still limited relative to animal microbiomes. Here we present a detailed characterization of the root-associated microbiomes of the crop plant rice by deep sequencing, using plants grown under controlled conditions as well as field cultivation at multiple sites. The spatial resolution of the study distinguished three root-associated compartments, the endosphere (root interior), rhizoplane (root surface), and rhizosphere (soil close to the root surface), each of which was found to harbor a distinct microbiome. Under controlled greenhouse conditions, microbiome composition varied with soil source and genotype. In field conditions, geographical location and cultivation practice, namely organic vs. conventional, were factors contributing to microbiome variation. Rice cultivation is a major source of global methane emissions, and methanogenic archaea could be detected in all spatial compartments of field-grown rice. The depth and scale of this study were used to build coabundance networks that revealed potential microbial consortia, some of which were involved in methane cycling. Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role. Similarities in the distribution of phyla in the root microbiomes of rice and other plants suggest that conclusions derived from this study might be generally applicable to land plants.

AB - Plants depend upon beneficial interactions between roots and microbes for nutrient availability, growth promotion, and disease suppression. High-throughput sequencing approaches have provided recent insights into root microbiomes, but our current understanding is still limited relative to animal microbiomes. Here we present a detailed characterization of the root-associated microbiomes of the crop plant rice by deep sequencing, using plants grown under controlled conditions as well as field cultivation at multiple sites. The spatial resolution of the study distinguished three root-associated compartments, the endosphere (root interior), rhizoplane (root surface), and rhizosphere (soil close to the root surface), each of which was found to harbor a distinct microbiome. Under controlled greenhouse conditions, microbiome composition varied with soil source and genotype. In field conditions, geographical location and cultivation practice, namely organic vs. conventional, were factors contributing to microbiome variation. Rice cultivation is a major source of global methane emissions, and methanogenic archaea could be detected in all spatial compartments of field-grown rice. The depth and scale of this study were used to build coabundance networks that revealed potential microbial consortia, some of which were involved in methane cycling. Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role. Similarities in the distribution of phyla in the root microbiomes of rice and other plants suggest that conclusions derived from this study might be generally applicable to land plants.

KW - Methane cycling

KW - Microbiome assembly

KW - Microbiomes

KW - Rice

KW - Soil microbial communities

UR - http://www.scopus.com/inward/record.url?scp=84923647491&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84923647491&partnerID=8YFLogxK

U2 - 10.1073/pnas.1414592112

DO - 10.1073/pnas.1414592112

M3 - Article

VL - 112

SP - E911-E920

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 8

ER -