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

Title: The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation

Abstract

Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities. Studies with model plants have begun to reveal the complex interactions between root exudates and soil microbes, but little is known about the influence of specialized exudates from crop plants. The aims of this work were to understand whether sorgoleone, a unique lipophilic secondary benzoquinone exuded only from the root hairs of sorghum, influences belowground microbial community structure in the field, to assess the effect of purified sorgoleone on the cultured bacteria from field soils, and to determine whether sorgoleone inhibits nitrification under field conditions. Studies were conducted comparing wild-type sorghum and lines with genetically reduced sorgoleone exudation. In the soil near roots and rhizosphere, sorgoleone influenced microbial community structure as measured by β-diversity and network analysis. Under greenhouse conditions, the soil nitrogen content was an important factor in determining the impacts of sorgoleone. Sorgoleone delayed the formation of the bacterial and archaeal networks early in plant development and only inhibited nitrification at specific sampling times under field conditions. Sorgoleone was also shown to both inhibit and promote cultured bacterial isolate growth in laboratory tests. Thesemore » findings provide new insights into the role of secondary metabolites in shaping the composition and function of the sorghum root-associated bacterial microbiomes. Understanding how root exudates modify soil microbiomes may potentially unlock an important tool for enhancing crop sustainability and yield in our changing environment.« less

Authors:
 [1];  [1];  [2];  [3]; ORCiD logo [1];
  1. University of Nebraska—Lincoln, Center for Plant Science Innovation, Department of Agronomy and Horticulture, Lincoln, Nebraska, USA
  2. University of Nebraska—Lincoln, Center for Plant Science Innovation, Department of Biochemistry, Lincoln, Nebraska, USA
  3. Colorado State University, Department of Agricultural Biology, Fort Collins, Colorado, USA
Publication Date:
Research Org.:
Univ. of Nebraska, Lincoln, NE (United States)
Sponsoring Org.:
USDOE Office of Science (SC); US Dept. of Agriculture (USDA)
OSTI Identifier:
1772168
Alternate Identifier(s):
OSTI ID: 1851911
Grant/Contract Number:  
SC0014395; 2020-67019-31796
Resource Type:
Published Article
Journal Name:
mSystems
Additional Journal Information:
Journal Name: mSystems Journal Volume: 6 Journal Issue: 2; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; root exudates; nitrification; microbiome; sorghum; sorgoleone; nitrogen; soil property

Citation Formats

Wang, Peng, Chai, Yen Ning, Roston, Rebecca, Dayan, Franck E., Schachtman, Daniel P., and Bulgarelli, ed., Davide. The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation. United States: N. p., 2021. Web. doi:10.1128/mSystems.00749-20.
Wang, Peng, Chai, Yen Ning, Roston, Rebecca, Dayan, Franck E., Schachtman, Daniel P., & Bulgarelli, ed., Davide. The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation. United States. https://doi.org/10.1128/mSystems.00749-20
Wang, Peng, Chai, Yen Ning, Roston, Rebecca, Dayan, Franck E., Schachtman, Daniel P., and Bulgarelli, ed., Davide. Tue . "The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation". United States. https://doi.org/10.1128/mSystems.00749-20.
@article{osti_1772168,
title = {The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation},
author = {Wang, Peng and Chai, Yen Ning and Roston, Rebecca and Dayan, Franck E. and Schachtman, Daniel P. and Bulgarelli, ed., Davide},
abstractNote = {Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities. Studies with model plants have begun to reveal the complex interactions between root exudates and soil microbes, but little is known about the influence of specialized exudates from crop plants. The aims of this work were to understand whether sorgoleone, a unique lipophilic secondary benzoquinone exuded only from the root hairs of sorghum, influences belowground microbial community structure in the field, to assess the effect of purified sorgoleone on the cultured bacteria from field soils, and to determine whether sorgoleone inhibits nitrification under field conditions. Studies were conducted comparing wild-type sorghum and lines with genetically reduced sorgoleone exudation. In the soil near roots and rhizosphere, sorgoleone influenced microbial community structure as measured by β-diversity and network analysis. Under greenhouse conditions, the soil nitrogen content was an important factor in determining the impacts of sorgoleone. Sorgoleone delayed the formation of the bacterial and archaeal networks early in plant development and only inhibited nitrification at specific sampling times under field conditions. Sorgoleone was also shown to both inhibit and promote cultured bacterial isolate growth in laboratory tests. These findings provide new insights into the role of secondary metabolites in shaping the composition and function of the sorghum root-associated bacterial microbiomes. Understanding how root exudates modify soil microbiomes may potentially unlock an important tool for enhancing crop sustainability and yield in our changing environment.},
doi = {10.1128/mSystems.00749-20},
journal = {mSystems},
number = 2,
volume = 6,
place = {United States},
year = {Tue Apr 27 00:00:00 EDT 2021},
month = {Tue Apr 27 00:00:00 EDT 2021}
}

Works referenced in this record:

Sorgoleone release from sorghum roots shapes the composition of nitrifying populations, total bacteria, and archaea and determines the level of nitrification
journal, October 2019

  • Sarr, Papa Saliou; Ando, Yasuo; Nakamura, Satoshi
  • Biology and Fertility of Soils, Vol. 56, Issue 2
  • DOI: 10.1007/s00374-019-01405-3

Benzoxazinoids in Root Exudates of Maize Attract Pseudomonas putida to the Rhizosphere
journal, April 2012


Decomposition of 14C-labelled lignin and phenols by a Nocardia sp.
journal, January 1977

  • Trojanowski, J.; Haider, K.; Sundman, V.
  • Archives of Microbiology, Vol. 114, Issue 2
  • DOI: 10.1007/BF00410776

Authoritative sources in a hyperlinked environment
journal, September 1999


Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?
journal, January 2018


Exometabolomics and MSI: deconstructing how cells interact to transform their small molecule environment
journal, August 2015


Mineralization of the allelochemical sorgoleone in soil
journal, August 2009


ggplot2
book, January 2009


Exometabolomic Profiling of Bacterial Strains as Cultivated Using Arabidopsis Root Extract as the Sole Carbon Source
journal, August 2018

  • Jacoby, Richard P.; Martyn, Anna; Kopriva, Stanislav
  • Molecular Plant-Microbe Interactions®, Vol. 31, Issue 8
  • DOI: 10.1094/MPMI-10-17-0253-R

Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies
journal, July 2016

  • Gohl, Daryl M.; Vangay, Pajau; Garbe, John
  • Nature Biotechnology, Vol. 34, Issue 9
  • DOI: 10.1038/nbt.3601

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


Small molecules below-ground: the role of specialized metabolites in the rhizosphere
journal, April 2017

  • Massalha, Hassan; Korenblum, Elisa; Tholl, Dorothea
  • The Plant Journal, Vol. 90, Issue 4
  • DOI: 10.1111/tpj.13543

Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses
journal, December 2019

  • Varoquaux, Nelle; Cole, Benjamin; Gao, Cheng
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 52
  • DOI: 10.1073/pnas.1907500116

The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization
journal, December 2017

  • McCormick, Ryan F.; Truong, Sandra K.; Sreedasyam, Avinash
  • The Plant Journal, Vol. 93, Issue 2
  • DOI: 10.1111/tpj.13781

Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2
journal, July 2011


Keystone taxa as drivers of microbiome structure and functioning
journal, May 2018

  • Banerjee, Samiran; Schlaeppi, Klaus; van der Heijden, Marcel G. A.
  • Nature Reviews Microbiology, Vol. 16, Issue 9
  • DOI: 10.1038/s41579-018-0024-1

Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize
journal, November 2016


Practical innovations for high-throughput amplicon sequencing
journal, September 2013

  • Lundberg, Derek S.; Yourstone, Scott; Mieczkowski, Piotr
  • Nature Methods, Vol. 10, Issue 10
  • DOI: 10.1038/nmeth.2634

A Genomic Resource for the Development, Improvement, and Exploitation of Sorghum for Bioenergy
journal, June 2016


Nitrogen Mineralization, Immobilization, and Nitrification
book, September 2018


Inferring Correlation Networks from Genomic Survey Data
journal, September 2012


NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes
journal, July 2006

  • DeSantis, T. Z.; Hugenholtz, P.; Keller, K.
  • Nucleic Acids Research, Vol. 34, Issue Web Server
  • DOI: 10.1093/nar/gkl244

Networking in the Plant Microbiome
journal, February 2016


Root Exudates Regulate Soil Fungal Community Composition and Diversity
journal, December 2007

  • Broeckling, C. D.; Broz, A. K.; Bergelson, J.
  • Applied and Environmental Microbiology, Vol. 74, Issue 3
  • DOI: 10.1128/AEM.02188-07

Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition
journal, June 2017


Anatomy of Sorgoleone‐Secreting Root Hairs of Sorghum Species
journal, November 2003

  • Czarnota, Mark A.; Paul, Rex N.; Weston, Leslie A.
  • International Journal of Plant Sciences, Vol. 164, Issue 6
  • DOI: 10.1086/378661

How Plant Root Exudates Shape the Nitrogen Cycle
journal, August 2017


MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health
journal, April 2018

  • Stringlis, Ioannis A.; Yu, Ke; Feussner, Kirstin
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 22
  • DOI: 10.1073/pnas.1722335115

The Soil-Borne Legacy
journal, March 2018


Role of root exudates in metal acquisition and tolerance
journal, October 2017


Biological nitrification inhibition in sorghum: the role of sorgoleone production
journal, March 2014


The nitrogen cycle
journal, February 2016


Plant Antimicrobial Agents and Their Effects on Plant and Human Pathogens
journal, July 2009

  • González-Lamothe, Rocío; Mitchell, Gabriel; Gattuso, Mariza
  • International Journal of Molecular Sciences, Vol. 10, Issue 8
  • DOI: 10.3390/ijms10083400

Metabolic regulation of the maize rhizobiome by benzoxazinoids
journal, February 2019

  • Cotton, T. E. Anne; Pétriacq, Pierre; Cameron, Duncan D.
  • The ISME Journal, Vol. 13, Issue 7
  • DOI: 10.1038/s41396-019-0375-2

Metabolomics in the Rhizosphere: Tapping into Belowground Chemical Communication
journal, March 2016


Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
journal, August 2015


Belowground microbial communities respond to water deficit and are shaped by decades of maize hybrid breeding
journal, June 2019

  • Wang, Peng; Marsh, Ellen L.; Kruger, Greg
  • Environmental Microbiology, Vol. 22, Issue 3
  • DOI: 10.1111/1462-2920.14701

Isolation and Analysis of Microbial Communities in Soil, Rhizosphere, and Roots in Perennial Grass Experiments
journal, January 2018

  • McPherson, Morgan R.; Wang, Peng; Marsh, Ellen L.
  • Journal of Visualized Experiments, Issue 137
  • DOI: 10.3791/57932

UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013


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

Soil bacterial networks are less stable under drought than fungal networks
journal, August 2018


Suppression of soil nitrification by plants
journal, April 2015


Sorgoleone
journal, July 2010


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

Biological nitrification inhibition (BNI) activity in sorghum and its characterization
journal, August 2012


Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria
journal, April 2018

  • Xu, Ling; Naylor, Dan; Dong, Zhaobin
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 18
  • DOI: 10.1073/pnas.1717308115

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


F UNCTION AND M ECHANISM OF O RGANIC A NION E XUDATION FROM P LANT R OOTS
journal, June 2001


A specialized metabolic network selectively modulates Arabidopsis root microbiota
journal, May 2019


Using network analysis to explore co-occurrence patterns in soil microbial communities
journal, September 2011

  • Barberán, Albert; Bates, Scott T.; Casamayor, Emilio O.
  • The ISME Journal, Vol. 6, Issue 2
  • DOI: 10.1038/ismej.2011.119

Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots
journal, March 2019


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

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


A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes
journal, August 1986


The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis
journal, December 2004

  • Cole, J. R.
  • Nucleic Acids Research, Vol. 33, Issue Database issue
  • DOI: 10.1093/nar/gki038

Plant host habitat and root exudates shape soil bacterial community structure
journal, August 2008

  • Haichar, Feth el Zahar; Marol, Christine; Berge, Odile
  • The ISME Journal, Vol. 2, Issue 12
  • DOI: 10.1038/ismej.2008.80

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

Metabolic niches in the rhizosphere microbiome: new tools and approaches to analyse metabolic mechanisms of plant–microbe nutrient exchange
journal, December 2018

  • Jacoby, Richard P.; Kopriva, Stanislav
  • Journal of Experimental Botany, Vol. 70, Issue 4
  • DOI: 10.1093/jxb/ery438

Variation in Sodium Exclusion and Salt Tolerance in Triticum tauschii
journal, July 1991


Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities?: Root exudates and rhizosphere bacteria
journal, March 2010


A global atlas of the dominant bacteria found in soil
journal, January 2018

  • Delgado-Baquerizo, Manuel; Oliverio, Angela M.; Brewer, Tess E.
  • Science, Vol. 359, Issue 6373
  • DOI: 10.1126/science.aap9516

Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation
journal, November 2012


A Bioluminescence Assay Using Nitrosomonas europaeafor Rapid and Sensitive Detection of Nitrification Inhibitors
journal, October 1998


Chemical Signaling Between Plants and Plant-Pathogenic Bacteria
journal, August 2013


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

Functional diversity of Nocardia in metabolism: Metabolism of Nocardia
journal, August 2013

  • Luo, Quan; Hiessl, Sebastian; Steinbüchel, Alexander
  • Environmental Microbiology, Vol. 16, Issue 1
  • DOI: 10.1111/1462-2920.12221

Enhancement of Plant-Microbe Interactions Using a Rhizosphere Metabolomics-Driven Approach and Its Application in the Removal of Polychlorinated Biphenyls
journal, May 2003

  • Narasimhan, Kothandaraman; Basheer, Chanbasha; Bajic, Vladimir B.
  • Plant Physiology, Vol. 132, Issue 1
  • DOI: 10.1104/pp.102.016295

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


A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola
journal, August 2006


Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota
journal, July 2018