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

Title: Deciphering the microbial and molecular responses of geographically diverse Setaria accessions grown in a nutrient-poor soil

Abstract

The microbial and molecular characterization of the ectorhizosphere is an important step towards developing a more complete understanding of how the cultivation of biofuel crops can be undertaken in nutrient poor environments. The ectorhizosphere of Setaria is of particular interest because the plant component of this plant-microbe system is an important agricultural grain crop and a model for biofuel grasses. Importantly, Setaria lends itself to high throughput molecular studies. As such, we have identified important intra- and interspecific microbial and molecular differences in the ectorhizospheres of three geographically distant Setaria italica accessions and their wild ancestor S . viridis . All were grown in a nutrient-poor soil with and without nutrient addition. To assess the contrasting impact of nutrient deficiency observed for two S . italica accessions, we quantitatively evaluated differences in soil organic matter, microbial community, and metabolite profiles. Together, these measurements suggest that rhizosphere priming differs with Setaria accession, which comes from alterations in microbial community abundances, specifically Actinobacteria and Proteobacteria populations. When globally comparing the metabolomic response of Setaria to nutrient addition, plants produced distinctly different metabolic profiles in the leaves and roots. With nutrient addition, increases of nitrogen containing metabolites were significantly higher in plant leavesmore » and roots along with significant increases in tyrosine derived alkaloids, serotonin, and synephrine. Glycerol was also found to be significantly increased in the leaves as well as the ectorhizosphere. These differences provide insight into how C 4 grasses adapt to changing nutrient availability in soils or with contrasting fertilization schemas. Gained knowledge could then be utilized in plant enhancement and bioengineering efforts to produce plants with superior traits when grown in nutrient poor soils.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo; ORCiD logo;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1834641
Alternate Identifier(s):
OSTI ID: 1839072
Report Number(s):
PNNL-SA-169097
Journal ID: ISSN 1932-6203; 10.1371/journal.pone.0259937
Grant/Contract Number:  
LDRD; AC05-76RL01830
Resource Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Name: PLoS ONE Journal Volume: 16 Journal Issue: 12; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Setaria, Nutrient, Soil Organic Matter, Metabolomics, Rhizosphere, Microbial Community

Citation Formats

Peterson, Matthew J., Handakumbura, Pubudu P., Thompson, Allison M., Russell, Zachary R., Kim, Young-Mo, Fansler, Sarah J., Smith, Montana L., Toyoda, Jason G., Chu, Rosey K., Stanfill, Bryan A., Fransen, Steven C., Bailey, Vanessa L., Jansson, Christer, Hixson, Kim K., Callister, Stephen J., and Mehanathan, ed., Muthamilarasan. Deciphering the microbial and molecular responses of geographically diverse Setaria accessions grown in a nutrient-poor soil. United States: N. p., 2021. Web. doi:10.1371/journal.pone.0259937.
Peterson, Matthew J., Handakumbura, Pubudu P., Thompson, Allison M., Russell, Zachary R., Kim, Young-Mo, Fansler, Sarah J., Smith, Montana L., Toyoda, Jason G., Chu, Rosey K., Stanfill, Bryan A., Fransen, Steven C., Bailey, Vanessa L., Jansson, Christer, Hixson, Kim K., Callister, Stephen J., & Mehanathan, ed., Muthamilarasan. Deciphering the microbial and molecular responses of geographically diverse Setaria accessions grown in a nutrient-poor soil. United States. https://doi.org/10.1371/journal.pone.0259937
Peterson, Matthew J., Handakumbura, Pubudu P., Thompson, Allison M., Russell, Zachary R., Kim, Young-Mo, Fansler, Sarah J., Smith, Montana L., Toyoda, Jason G., Chu, Rosey K., Stanfill, Bryan A., Fransen, Steven C., Bailey, Vanessa L., Jansson, Christer, Hixson, Kim K., Callister, Stephen J., and Mehanathan, ed., Muthamilarasan. Wed . "Deciphering the microbial and molecular responses of geographically diverse Setaria accessions grown in a nutrient-poor soil". United States. https://doi.org/10.1371/journal.pone.0259937.
@article{osti_1834641,
title = {Deciphering the microbial and molecular responses of geographically diverse Setaria accessions grown in a nutrient-poor soil},
author = {Peterson, Matthew J. and Handakumbura, Pubudu P. and Thompson, Allison M. and Russell, Zachary R. and Kim, Young-Mo and Fansler, Sarah J. and Smith, Montana L. and Toyoda, Jason G. and Chu, Rosey K. and Stanfill, Bryan A. and Fransen, Steven C. and Bailey, Vanessa L. and Jansson, Christer and Hixson, Kim K. and Callister, Stephen J. and Mehanathan, ed., Muthamilarasan},
abstractNote = {The microbial and molecular characterization of the ectorhizosphere is an important step towards developing a more complete understanding of how the cultivation of biofuel crops can be undertaken in nutrient poor environments. The ectorhizosphere of Setaria is of particular interest because the plant component of this plant-microbe system is an important agricultural grain crop and a model for biofuel grasses. Importantly, Setaria lends itself to high throughput molecular studies. As such, we have identified important intra- and interspecific microbial and molecular differences in the ectorhizospheres of three geographically distant Setaria italica accessions and their wild ancestor S . viridis . All were grown in a nutrient-poor soil with and without nutrient addition. To assess the contrasting impact of nutrient deficiency observed for two S . italica accessions, we quantitatively evaluated differences in soil organic matter, microbial community, and metabolite profiles. Together, these measurements suggest that rhizosphere priming differs with Setaria accession, which comes from alterations in microbial community abundances, specifically Actinobacteria and Proteobacteria populations. When globally comparing the metabolomic response of Setaria to nutrient addition, plants produced distinctly different metabolic profiles in the leaves and roots. With nutrient addition, increases of nitrogen containing metabolites were significantly higher in plant leaves and roots along with significant increases in tyrosine derived alkaloids, serotonin, and synephrine. Glycerol was also found to be significantly increased in the leaves as well as the ectorhizosphere. These differences provide insight into how C 4 grasses adapt to changing nutrient availability in soils or with contrasting fertilization schemas. Gained knowledge could then be utilized in plant enhancement and bioengineering efforts to produce plants with superior traits when grown in nutrient poor soils.},
doi = {10.1371/journal.pone.0259937},
journal = {PLoS ONE},
number = 12,
volume = 16,
place = {United States},
year = {Wed Dec 08 00:00:00 EST 2021},
month = {Wed Dec 08 00:00:00 EST 2021}
}

Works referenced in this record:

Association of an SNP in a novel DREB2-like gene SiDREB2 with stress tolerance in foxtail millet [Setaria italica (L.)]
journal, March 2011

  • Lata, Charu; Bhutty, Sarita; Bahadur, Ranjit Prasad
  • Journal of Experimental Botany, Vol. 62, Issue 10
  • DOI: 10.1093/jxb/err016

Phytoserotonin: A review
journal, June 2011

  • Akula, Ramakrishna; Giridhar, P.; Ravishankar, G. A.
  • Plant Signaling & Behavior, Vol. 6, Issue 6
  • DOI: 10.4161/psb.6.6.15242

Glutamate in plants: metabolism, regulation, and signalling
journal, March 2007

  • Forde, B. G.; Lea, P. J.
  • Journal of Experimental Botany, Vol. 58, Issue 9
  • DOI: 10.1093/jxb/erm121

Microbial metabolism of phenolic amines: degradation of dl-synephrine by an unidentified arthrobacter
journal, June 1975


DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008


A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica)
journal, June 2013

  • Jia, Guanqing; Huang, Xuehui; Zhi, Hui
  • Nature Genetics, Vol. 45, Issue 8
  • DOI: 10.1038/ng.2673

Effects of abiotic stress on physiological plasticity and water use of Setaria viridis (L.)
journal, October 2016


Automated Analysis of Electrospray Ionization Fourier Transform Ion Cyclotron Resonance Mass Spectra of Natural Organic Matter
journal, July 2006

  • Kujawinski, Elizabeth B.; Behn, Mark D.
  • Analytical Chemistry, Vol. 78, Issue 13
  • DOI: 10.1021/ac0600306

Formularity: Software for Automated Formula Assignment of Natural and Other Organic Matter from Ultrahigh-Resolution Mass Spectra
journal, November 2017


Using ESI FT-ICR MS to Characterize Dissolved Organic Matter in Salt Lakes with Different Salinity
journal, October 2020


The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications
journal, October 2018

  • Nilsson, Rolf Henrik; Larsson, Karl-Henrik; Taylor, Andy F. S.
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1022

Characterization of dissolved organic matter in Lake Superior and its watershed using ultrahigh resolution mass spectrometry
journal, February 2012


The Safety of Citrus aurantium (Bitter Orange) and its Primary Protoalkaloid p -Synephrine: SAFETY OF CITRUS AURANTIUM (BITTER ORANGE) AND P -SYNEPHRINE
journal, April 2011

  • Stohs, Sidney J.; Preuss, Harry G.; Shara, Mohd
  • Phytotherapy Research, Vol. 25, Issue 10
  • DOI: 10.1002/ptr.3490

Setaria viridis : A Model for C 4 Photosynthesis
journal, August 2010

  • Brutnell, Thomas P.; Wang, Lin; Swartwood, Kerry
  • The Plant Cell, Vol. 22, Issue 8
  • DOI: 10.1105/tpc.110.075309

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


MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses
journal, May 2016


Cyanide action in plants — from toxic to regulatory
journal, October 2006

  • Siegień, Irena; Bogatek, Renata
  • Acta Physiologiae Plantarum, Vol. 28, Issue 5
  • DOI: 10.1007/BF02706632

Palmitic acid mediated change of rhizosphere and alleviation of Fusarium wilt disease in watermelon
journal, June 2021

  • Ma, Kexin; Kou, Jinming; Khashi U. Rahman, Muhammad
  • Saudi Journal of Biological Sciences, Vol. 28, Issue 6
  • DOI: 10.1016/j.sjbs.2021.03.040

p-Synephrine suppresses lipopolysaccharide-induced acute lung injury by inhibition of the NF-κB signaling pathway
journal, February 2014


3-Hydroxyisobutyrate Dehydrogenase Is Involved in Both, Valine and Isoleucine Degradation in Arabidopsis thaliana
journal, July 2017

  • Schertl, Peter; Danne, Lennart; Braun, Hans-Peter
  • Plant Physiology, Vol. 175, Issue 1
  • DOI: 10.1104/pp.17.00649

Root Exudation of Phytochemicals in Arabidopsis Follows Specific Patterns That Are Developmentally Programmed and Correlate with Soil Microbial Functions
journal, February 2013


Microbiome and Exudates of the Root and Rhizosphere of Brachypodium distachyon, a Model for Wheat
journal, October 2016


The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks
journal, November 2013

  • Yilmaz, Pelin; Parfrey, Laura Wegener; Yarza, Pablo
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1209

The Glycerol-Dependent Metabolic Persistence of Pseudomonas putida KT2440 Reflects the Regulatory Logic of the GlpR Repressor
journal, March 2015

  • Nikel, Pablo I.; Romero-Campero, Francisco J.; Zeidman, Joshua A.
  • mBio, Vol. 6, Issue 2
  • DOI: 10.1128/mBio.00340-15

Amino Acid Catabolism in Plants
journal, November 2015

  • Hildebrandt, Tatjana M.; Nunes Nesi, Adriano; Araújo, Wagner L.
  • Molecular Plant, Vol. 8, Issue 11
  • DOI: 10.1016/j.molp.2015.09.005

Assessment of active bacteria metabolizing phenolic acids in the peanut (Arachis hypogaea L.) rhizosphere
journal, December 2017


Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition
journal, May 2011


Preparation of Lipide Extracts from Brain Tissue
journal, August 1951


Foxtail millet: a model crop for genetic and genomic studies in bioenergy grasses
journal, June 2012


Proteomic analysis of salt stress responses in foxtail millet (Setaria italica L. cv. Prasad) seedlings
journal, November 2008


Cyanide metabolism in higher plants
journal, September 1972

  • Castric, Peter A.; Farnden, Kevin J. F.; Conn, Eric E.
  • Archives of Biochemistry and Biophysics, Vol. 152, Issue 1
  • DOI: 10.1016/0003-9861(72)90193-2

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

pmartR : Quality Control and Statistics for Mass Spectrometry-Based Biological Data
journal, January 2019

  • Stratton, Kelly G.; Webb-Robertson, Bobbie-Jo M.; McCue, Lee Ann
  • Journal of Proteome Research, Vol. 18, Issue 3
  • DOI: 10.1021/acs.jproteome.8b00760

Effect of benzoic acid on soil microbial communities associated with soilborne peanut diseases
journal, February 2017


Investigating organic matter properties affecting the binding behavior of heavy metals in the rhizosphere of wetlands
journal, October 2018


Effects of temperature, soil substrate, and microbial community on carbon mineralization across three climatically contrasting forest sites
journal, December 2017

  • Tang, Zuoxin; Sun, Xiaolu; Luo, Zhongkui
  • Ecology and Evolution, Vol. 8, Issue 2
  • DOI: 10.1002/ece3.3708

Graphical Method for Analysis of Ultrahigh-Resolution Broadband Mass Spectra of Natural Organic Matter, the Van Krevelen Diagram
journal, October 2003

  • Kim, Sunghwan; Kramer, Robert W.; Hatcher, Patrick G.
  • Analytical Chemistry, Vol. 75, Issue 20
  • DOI: 10.1021/ac034415p

The Taxon Hypothesis Paradigm—On the Unambiguous Detection and Communication of Taxa
journal, November 2020


Sequential extraction protocol for organic matter from soils and sediments using high resolution mass spectrometry
journal, June 2017


Non-Targeted Metabolomics Reveals Sorghum Rhizosphere-Associated Exudates are Influenced by the Belowground Interaction of Substrate and Sorghum Genotype
journal, January 2019

  • Miller, Sarah B.; Heuberger, Adam L.; Broeckling, Corey D.
  • International Journal of Molecular Sciences, Vol. 20, Issue 2
  • DOI: 10.3390/ijms20020431

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater: SPE-DOM from seawater
journal, June 2008

  • Dittmar, Thorsten; Koch, Boris; Hertkorn, Norbert
  • Limnology and Oceanography: Methods, Vol. 6, Issue 6
  • DOI: 10.4319/lom.2008.6.230

Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential
journal, May 2012

  • Zhang, Gengyun; Liu, Xin; Quan, Zhiwu
  • Nature Biotechnology, Vol. 30, Issue 6
  • DOI: 10.1038/nbt.2195

cDNA-AFLP Analysis Reveals Differential Gene Expression in Response to Salt Stress in Foxtail Millet (Setaria italica L.)
journal, July 2008

  • Jayaraman, Ananthi; Puranik, Swati; Rai, Neeraj Kumar
  • Molecular Biotechnology, Vol. 40, Issue 3
  • DOI: 10.1007/s12033-008-9081-4

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency?
journal, October 2014


MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis
journal, May 2009

  • Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian
  • Analytical Chemistry, Vol. 81, Issue 9
  • DOI: 10.1021/ac802689c

Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses
journal, March 2011

  • Li, P.; Brutnell, T. P.
  • Journal of Experimental Botany, Vol. 62, Issue 9
  • DOI: 10.1093/jxb/err096

N 2 Fixation by Azospirillum brasilense and Its Incorporation into Host Setaria italica
journal, September 1983


Nitrogen use efficiency. 2. Amino acid metabolism
journal, December 2007