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 »
- Authors:
-
- University of Nebraska—Lincoln, Center for Plant Science Innovation, Department of Agronomy and Horticulture, Lincoln, Nebraska, USA
- University of Nebraska—Lincoln, Center for Plant Science Innovation, Department of Biochemistry, Lincoln, Nebraska, USA
- 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}
}
https://doi.org/10.1128/mSystems.00749-20
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
Benzoxazinoids in Root Exudates of Maize Attract Pseudomonas putida to the Rhizosphere
journal, April 2012
- Neal, Andrew L.; Ahmad, Shakoor; Gordon-Weeks, Ruth
- PLoS ONE, Vol. 7, Issue 4
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
Authoritative sources in a hyperlinked environment
journal, September 1999
- Kleinberg, Jon M.
- Journal of the ACM, Vol. 46, Issue 5
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?
journal, January 2018
- Sasse, Joelle; Martinoia, Enrico; Northen, Trent
- Trends in Plant Science, Vol. 23, Issue 1
Exometabolomics and MSI: deconstructing how cells interact to transform their small molecule environment
journal, August 2015
- Silva, Leslie P.; Northen, Trent R.
- Current Opinion in Biotechnology, Vol. 34
Mineralization of the allelochemical sorgoleone in soil
journal, August 2009
- Gimsing, Anne Louise; Bælum, Jacob; Dayan, Franck E.
- Chemosphere, Vol. 76, Issue 8
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
Alkylresorcinol Synthases Expressed in Sorghum bicolor Root Hairs Play an Essential Role in the Biosynthesis of the Allelopathic Benzoquinone Sorgoleone
journal, March 2010
- Cook, Daniel; Rimando, Agnes M.; Clemente, Thomas E.
- The Plant Cell, Vol. 22, Issue 3
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
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018
- Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao
- Nature Microbiology, Vol. 3, Issue 4
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
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
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
Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2
journal, July 2011
- Zhou, Jizhong; Deng, Ye; Luo, Feng
- mBio, Vol. 2, Issue 4
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
Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize
journal, November 2016
- Zhu, Shusheng; Vivanco, Jorge M.; Manter, Daniel K.
- Applied Soil Ecology, Vol. 107
Practical innovations for high-throughput amplicon sequencing
journal, September 2013
- Lundberg, Derek S.; Yourstone, Scott; Mieczkowski, Piotr
- Nature Methods, Vol. 10, Issue 10
A Genomic Resource for the Development, Improvement, and Exploitation of Sorghum for Bioenergy
journal, June 2016
- Brenton, Zachary W.; Cooper, Elizabeth A.; Myers, Mathew T.
- Genetics, Vol. 204, Issue 1
Nitrogen Mineralization, Immobilization, and Nitrification
book, September 2018
- Hart, Stephen C.; Stark, John M.; Davidson, Eric A.
- SSSA Book Series
Inferring Correlation Networks from Genomic Survey Data
journal, September 2012
- Friedman, Jonathan; Alm, Eric J.
- PLoS Computational Biology, Vol. 8, Issue 9
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
Networking in the Plant Microbiome
journal, February 2016
- van der Heijden, Marcel G. A.; Hartmann, Martin
- PLOS Biology, Vol. 14, Issue 2
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
Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition
journal, June 2017
- Coskun, Devrim; Britto, Dev T.; Shi, Weiming
- Nature Plants, Vol. 3, Issue 6
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
How Plant Root Exudates Shape the Nitrogen Cycle
journal, August 2017
- Coskun, Devrim; Britto, Dev T.; Shi, Weiming
- Trends in Plant Science, Vol. 22, Issue 8
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
The Soil-Borne Legacy
journal, March 2018
- Bakker, Peter A. H. M.; Pieterse, Corné M. J.; de Jonge, Ronnie
- Cell, Vol. 172, Issue 6
Role of root exudates in metal acquisition and tolerance
journal, October 2017
- Chen, Yi-Tze; Wang, Ying; Yeh, Kuo-Chen
- Current Opinion in Plant Biology, Vol. 39
Biological nitrification inhibition in sorghum: the role of sorgoleone production
journal, March 2014
- Tesfamariam, Tsehaye; Yoshinaga, H.; Deshpande, S. P.
- Plant and Soil, Vol. 379, Issue 1-2
The nitrogen cycle
journal, February 2016
- Stein, Lisa Y.; Klotz, Martin G.
- Current Biology, Vol. 26, Issue 3
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
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
Metabolomics in the Rhizosphere: Tapping into Belowground Chemical Communication
journal, March 2016
- van Dam, Nicole M.; Bouwmeester, Harro J.
- Trends in Plant Science, Vol. 21, Issue 3
Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
journal, August 2015
- Shi, Shengjing; Nuccio, Erin; Herman, Donald J.
- mBio, Vol. 6, Issue 4
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
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
UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013
- Edgar, Robert C.
- Nature Methods, Vol. 10, Issue 10
Maize synthesized benzoxazinoids affect the host associated microbiome
journal, April 2019
- Kudjordjie, Enoch Narh; Sapkota, Rumakanta; Steffensen, Stine K.
- Microbiome, Vol. 7, Issue 1
Soil bacterial networks are less stable under drought than fungal networks
journal, August 2018
- de Vries, Franciska T.; Griffiths, Rob I.; Bailey, Mark
- Nature Communications, Vol. 9, Issue 1
Suppression of soil nitrification by plants
journal, April 2015
- Subbarao, Guntur Venkata; Yoshihashi, Tadashi; Worthington, Margaret
- Plant Science, Vol. 233
Sorgoleone
journal, July 2010
- Dayan, Franck E.; Rimando, Agnes M.; Pan, Zhiqiang
- Phytochemistry, Vol. 71, Issue 10
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
Biological nitrification inhibition (BNI) activity in sorghum and its characterization
journal, August 2012
- Subbarao, G. V.; Nakahara, K.; Ishikawa, T.
- Plant and Soil, Vol. 366, Issue 1-2
Mode of Action, Localization of Production, Chemical Nature, and Activity of Sorgoleone: A Potent PSII Inhibitor in Sorghum spp. Root Exudates 1
journal, October 2001
- Czarnota, Mark A.; Paul, Rex N.; Dayan, Franck E.
- Weed Technology, Vol. 15, Issue 4
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
Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa
journal, July 2015
- Lebeis, S. L.; Paredes, S. H.; Lundberg, D. S.
- Science, Vol. 349, Issue 6250
F UNCTION AND M ECHANISM OF O RGANIC A NION E XUDATION FROM P LANT R OOTS
journal, June 2001
- Ryan, Pr; Delhaize, E.; Jones, Dl
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 52, Issue 1
A specialized metabolic network selectively modulates Arabidopsis root microbiota
journal, May 2019
- Huang, Ancheng C.; Jiang, Ting; Liu, Yong-Xin
- Science, Vol. 364, Issue 6440
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
Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots
journal, March 2019
- Banerjee, Samiran; Walder, Florian; Büchi, Lucie
- The ISME Journal, Vol. 13, Issue 7
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
Deciphering microbial interactions and detecting keystone species with co-occurrence networks
journal, May 2014
- Berry, David; Widder, Stefanie
- Frontiers in Microbiology, Vol. 5
A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes
journal, August 1986
- Peters, N.; Frost, J.; Long, S.
- Science, Vol. 233, Issue 4767
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
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
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
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
A cytochrome P450 CYP71 enzyme expressed in Sorghum bicolor root hair cells participates in the biosynthesis of the benzoquinone allelochemical sorgoleone
journal, February 2018
- Pan, Zhiqiang; Baerson, Scott R.; Wang, Mei
- New Phytologist, Vol. 218, Issue 2
Variation in Sodium Exclusion and Salt Tolerance in Triticum tauschii
journal, July 1991
- Schachtman, D. P.; Munns, Ranna; Whitecross, M. I.
- Crop Science, Vol. 31, Issue 4
Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities?: Root exudates and rhizosphere bacteria
journal, March 2010
- Dennis, Paul G.; Miller, Anthony J.; Hirsch, Penny R.
- FEMS Microbiology Ecology, Vol. 72, Issue 3
Interplay among NH 4 + uptake, rhizosphere pH and plasma membrane H+-ATPase determine the release of BNIs in sorghum roots – possible mechanisms and underlying hypothesis
journal, February 2012
- Zhu, Yiyong; Zeng, Houqing; Shen, Qirong
- Plant and Soil, Vol. 358, Issue 1-2
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
Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation
journal, November 2012
- Prosser, James I.; Nicol, Graeme W.
- Trends in Microbiology, Vol. 20, Issue 11
A Bioluminescence Assay Using Nitrosomonas europaeafor Rapid and Sensitive Detection of Nitrification Inhibitors
journal, October 1998
- Iizumi, Taro; Mizumoto, Masahiro; Nakamura, Kanji
- Applied and Environmental Microbiology, Vol. 64, Issue 10
Chemical Signaling Between Plants and Plant-Pathogenic Bacteria
journal, August 2013
- Venturi, Vittorio; Fuqua, Clay
- Annual Review of Phytopathology, Vol. 51, Issue 1
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
Functional diversity of Nocardia in metabolism: Metabolism of Nocardia
journal, August 2013
- Luo, Quan; Hiessl, Sebastian; Steinbüchel, Alexander
- Environmental Microbiology, Vol. 16, Issue 1
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
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola
journal, August 2006
- Subbarao, G. V.; Ishikawa, T.; Ito, O.
- Plant and Soil, Vol. 288, Issue 1-2
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota
journal, July 2018
- Hu, Lingfei; Robert, Christelle A. M.; Cadot, Selma
- Nature Communications, Vol. 9, Issue 1