Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Metabolomics of sorghum roots during nitrogen stress reveals compromised metabolic capacity for salicylic acid biosynthesis

Abstract

Abstract Sorghum ( Sorghum bicolor [L.] Moench) is the fifth most productive cereal crop worldwide with some hybrids having high biomass yield traits making it promising for sustainable, economical biofuel production. To maximize biofuel feedstock yields, a more complete understanding of metabolic responses to low nitrogen (N) will be useful for incorporation in crop improvement efforts. In this study, 10 diverse sorghum entries (including inbreds and hybrids) were field‐grown under low and full N conditions and roots were sampled at two time points for metabolomics and 16S amplicon sequencing. Roots of plants grown under low N showed altered metabolic profiles at both sampling dates including metabolites important in N storage and synthesis of aromatic amino acids. Complementary investigation of the rhizosphere microbiome revealed dominance by a single operational taxonomic unit ( OTU ) in an early sampling that was taxonomically assigned to the genus Pseudomonas . Abundance of this Pseudomonas OTU was significantly greater under low N in July and was decreased dramatically in September. Correlation of Pseudomonas abundance with root metabolites revealed a strong negative association with the defense hormone salicylic acid ( SA ) under full N but not under low N, suggesting reduced defense response. Roots frommore » plants with N stress also contained reduced phenylalanine, a precursor for SA , providing further evidence for compromised metabolic capacity for defense response under low N conditions. Our findings suggest that interactions between biotic and abiotic stresses may affect metabolic capacity for plant defense and need to be concurrently prioritized as breeding programs become established for biofuels production on marginal soils.« less

Authors:
 [1];  [2];  [3];  [3];  [4];  [4];  [4];  [4];  [2];  [3];  [5];  [6];  [6];  [1]
+ Show Author Affiliations
  1. Department of Horticulture and Landscape Architecture Colorado State University Fort Collins Colorado
  2. Joint Genome Institute Department of Energy Walnut Creek California
  3. Bioinformatics &, Computational Biology Iowa State University Ames Iowa
  4. Donald Danforth Plant Science Center St. Louis Missouri
  5. Plant and Environmental Genetics and Biochemistry Departments Clemson University Clemson South Carolina
  6. Center for Biotechnology University of Nebraska‐Lincoln Lincoln Nebraska
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Biological Systems Science Division (SC-23.2 )
OSTI Identifier:
1499822
Alternate Identifier(s):
OSTI ID: 1503920; OSTI ID: 1508062
Grant/Contract Number:  
DE‐SC0014395; SC0014395; AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Plant Direct
Additional Journal Information:
Journal Name: Plant Direct Journal Volume: 3 Journal Issue: 3; Journal ID: ISSN 2475-4455
Publisher:
Wiley Blackwell (John Wiley & Sons)
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; metabolism; metabolomics; microbiome; nitrogen; rhizosphere; roots; salicylic acid; sorghum; stress

Citation Formats

Sheflin, Amy M., Chiniquy, Dawn, Yuan, Chaohui, Goren, Emily, Kumar, Indrajit, Braud, Max, Brutnell, Thomas, Eveland, Andrea L., Tringe, Susannah, Liu, Peng, Kresovich, Stephen, Marsh, Ellen L., Schachtman, Daniel P., and Prenni, Jessica E. Metabolomics of sorghum roots during nitrogen stress reveals compromised metabolic capacity for salicylic acid biosynthesis. United Kingdom: N. p., 2019. Web. doi:10.1002/pld3.122.
Copy to clipboard
Sheflin, Amy M., Chiniquy, Dawn, Yuan, Chaohui, Goren, Emily, Kumar, Indrajit, Braud, Max, Brutnell, Thomas, Eveland, Andrea L., Tringe, Susannah, Liu, Peng, Kresovich, Stephen, Marsh, Ellen L., Schachtman, Daniel P., & Prenni, Jessica E. Metabolomics of sorghum roots during nitrogen stress reveals compromised metabolic capacity for salicylic acid biosynthesis. United Kingdom. https://doi.org/10.1002/pld3.122
Copy to clipboard
Sheflin, Amy M., Chiniquy, Dawn, Yuan, Chaohui, Goren, Emily, Kumar, Indrajit, Braud, Max, Brutnell, Thomas, Eveland, Andrea L., Tringe, Susannah, Liu, Peng, Kresovich, Stephen, Marsh, Ellen L., Schachtman, Daniel P., and Prenni, Jessica E. Thu . "Metabolomics of sorghum roots during nitrogen stress reveals compromised metabolic capacity for salicylic acid biosynthesis". United Kingdom. https://doi.org/10.1002/pld3.122.
Copy to clipboard
@article{osti_1499822,
title = {Metabolomics of sorghum roots during nitrogen stress reveals compromised metabolic capacity for salicylic acid biosynthesis},
author = {Sheflin, Amy M. and Chiniquy, Dawn and Yuan, Chaohui and Goren, Emily and Kumar, Indrajit and Braud, Max and Brutnell, Thomas and Eveland, Andrea L. and Tringe, Susannah and Liu, Peng and Kresovich, Stephen and Marsh, Ellen L. and Schachtman, Daniel P. and Prenni, Jessica E.},
abstractNote = {Abstract Sorghum ( Sorghum bicolor [L.] Moench) is the fifth most productive cereal crop worldwide with some hybrids having high biomass yield traits making it promising for sustainable, economical biofuel production. To maximize biofuel feedstock yields, a more complete understanding of metabolic responses to low nitrogen (N) will be useful for incorporation in crop improvement efforts. In this study, 10 diverse sorghum entries (including inbreds and hybrids) were field‐grown under low and full N conditions and roots were sampled at two time points for metabolomics and 16S amplicon sequencing. Roots of plants grown under low N showed altered metabolic profiles at both sampling dates including metabolites important in N storage and synthesis of aromatic amino acids. Complementary investigation of the rhizosphere microbiome revealed dominance by a single operational taxonomic unit ( OTU ) in an early sampling that was taxonomically assigned to the genus Pseudomonas . Abundance of this Pseudomonas OTU was significantly greater under low N in July and was decreased dramatically in September. Correlation of Pseudomonas abundance with root metabolites revealed a strong negative association with the defense hormone salicylic acid ( SA ) under full N but not under low N, suggesting reduced defense response. Roots from plants with N stress also contained reduced phenylalanine, a precursor for SA , providing further evidence for compromised metabolic capacity for defense response under low N conditions. Our findings suggest that interactions between biotic and abiotic stresses may affect metabolic capacity for plant defense and need to be concurrently prioritized as breeding programs become established for biofuels production on marginal soils.},
doi = {10.1002/pld3.122},
journal = {Plant Direct},
number = 3,
volume = 3,
place = {United Kingdom},
year = {Thu Mar 14 00:00:00 EDT 2019},
month = {Thu Mar 14 00:00:00 EDT 2019}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1002/pld3.122
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 21 works
Citation information provided by
Web of Science
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Understanding and engineering beneficial plant-microbe interactions: plant growth promotion in energy crops
journal, November 2014

  • Farrar, Kerrie; Bryant, David; Cope-Selby, Naomi
  • Plant Biotechnology Journal, Vol. 12, Issue 9
  • DOI: 10.1111/pbi.12279

The Sorghum bicolor genome and the diversification of grasses
journal, January 2009

  • Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy
  • Nature, Vol. 457, Issue 7229
  • DOI: 10.1038/nature07723

MetaboAnalyst 3.0—making metabolomics more meaningful
journal, April 2015

  • Xia, Jianguo; Sinelnikov, Igor V.; Han, Beomsoo
  • Nucleic Acids Research, Vol. 43, Issue W1
  • DOI: 10.1093/nar/gkv380

Alterations in Leaf Carbohydrate Metabolism in Response to Nitrogen Stress
journal, November 1988

  • Rufty, Thomas W.; Huber, Steven C.; Volk, Richard J.
  • Plant Physiology, Vol. 88, Issue 3
  • DOI: 10.1104/pp.88.3.725

Diversity of nifH gene pools in the rhizosphere of two cultivars of sorghum ( Sorghum bicolor ) treated with contrasting levels of nitrogen fertilizer
journal, February 2008

Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance
journal, June 2014

Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys
journal, December 2015

XCMS:  Processing Mass Spectrometry Data for Metabolite Profiling Using Nonlinear Peak Alignment, Matching, and Identification
journal, February 2006

  • Smith, Colin A.; Want, Elizabeth J.; O'Maille, Grace
  • Analytical Chemistry, Vol. 78, Issue 3
  • DOI: 10.1021/ac051437y

Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency
journal, December 2010

  • Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri
  • Journal of Plant Nutrition and Soil Science, Vol. 174, Issue 1
  • DOI: 10.1002/jpln.201000085

Skyline: an open source document editor for creating and analyzing targeted proteomics experiments
journal, February 2010

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

Metabolite fingerprinting of pennycress ( Thlaspi arvense L.) embryos to assess active pathways during oil synthesis
journal, February 2015

  • Tsogtbaatar, Enkhtuul; Cocuron, Jean-Christophe; Sonera, Marcos Corchado
  • Journal of Experimental Botany, Vol. 66, Issue 14
  • DOI: 10.1093/jxb/erv020

Manifestations of Hybrid Vigor in Sorghum1
journal, January 1963

Metabolomics in plant environmental physiology
journal, August 2013

  • Brunetti, Cecilia; George, Rachel M.; Tattini, Massimiliano
  • Journal of Experimental Botany, Vol. 64, Issue 13
  • DOI: 10.1093/jxb/ert244

Biosynthesis of salicylic acid in plants
journal, June 2009

  • Chen, Zhixiang; Zheng, Zuyu; Huang, Junli
  • Plant Signaling & Behavior, Vol. 4, Issue 6
  • DOI: 10.4161/psb.4.6.8392

Metabolite Profiling of Low-P Tolerant and Low-P Sensitive Maize Genotypes under Phosphorus Starvation and Restoration Conditions
journal, June 2015

2016 Billion-Ton Report: Advancing Domestic Resources for a Thriving Bioeconomy
report, July 2016

  • Langholtz, M. H.; Stokes, B. J.; Eaton, L. M.
  • DOE/EE-1440
  • DOI: 10.2172/1271651

Primer and platform effects on 16S rRNA tag sequencing
journal, August 2015

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

RAMClust: A Novel Feature Clustering Method Enables Spectral-Matching-Based Annotation for Metabolomics Data
journal, June 2014

  • Broeckling, C. D.; Afsar, F. A.; Neumann, S.
  • Analytical Chemistry, Vol. 86, Issue 14
  • DOI: 10.1021/ac501530d

Search and clustering orders of magnitude faster than BLAST
journal, August 2010

Up-Regulation and Localization of Asparagine Synthetase in Tomato Leaves Infected by the Bacterial Pathogen Pseudomonas syringae
journal, June 2004

  • Olea, Francisco; Pérez-García, Alejandro; Cantón, Francisco R.
  • Plant and Cell Physiology, Vol. 45, Issue 6
  • DOI: 10.1093/pcp/pch092

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

High-parent heterosis for biomass yield in photoperiod-sensitive sorghum hybrids
journal, October 2014

The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity
journal, September 2007

  • Tavernier, Virginie; Cadiou, Sandrine; Pageau, Karine
  • Journal of Experimental Botany, Vol. 58, Issue 12
  • DOI: 10.1093/jxb/erm182

On a Test of Whether one of Two Random Variables is Stochastically Larger than the Other
journal, March 1947

PERANAN RIZOBAKTERI DAN FUNGI MIKORIZA ARBUSKULAR DALAM MENINGKATKAN EFISIENSI PENYERAPAN HARA SORGUM MANIS (Sorghum bicolor L. Moench)
journal, October 2014

  • Rupaedah, Bedah; Anas, Iswandi; Santosa, Dwi Andreas
  • Jurnal Ilmu Tanah dan Lingkungan, Vol. 16, Issue 2
  • DOI: 10.29244/jitl.16.2.45-52

Mapping QTLs and association of differentially expressed gene transcripts for multiple agronomic traits under different nitrogen levels in sorghum
journal, January 2016

Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture
journal, March 2010

  • Masclaux-Daubresse, Céline; Daniel-Vedele, Françoise; Dechorgnat, Julie
  • Annals of Botany, Vol. 105, Issue 7
  • DOI: 10.1093/aob/mcq028

Population genomic and genome-wide association studies of agroclimatic traits in sorghum
journal, December 2012

  • Morris, G. P.; Ramu, P.; Deshpande, S. P.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 2
  • DOI: 10.1073/pnas.1215985110

Metabolomics – the link between genotypes and phenotypes
journal, January 2002

Trehalose and plant stress responses: friend or foe?
journal, July 2010

Asparagine Metabolic Pathways in Arabidopsis
journal, December 2015

  • Gaufichon, Laure; Rothstein, Steven J.; Suzuki, Akira
  • Plant and Cell Physiology, Vol. 57, Issue 4
  • DOI: 10.1093/pcp/pcv184

The untranslated leader sequence of the barley lipoxygenase 1 ( Lox1 ) gene confers embryo‐specific expression
journal, August 1998

Analysis of plant microbe interactions in the era of next generation sequencing technologies
journal, May 2014

Designing sorghum as a dedicated bioenergy feedstock
journal, October 2007

  • Rooney, William L.; Blumenthal, Jürg; Bean, Brent
  • Biofuels, Bioproducts and Biorefining, Vol. 1, Issue 2
  • DOI: 10.1002/bbb.15

The aligned rank transform for nonparametric factorial analyses using only anova procedures
conference, January 2011

  • Wobbrock, Jacob O.; Findlater, Leah; Gergle, Darren
  • Proceedings of the 2011 annual conference on Human factors in computing systems - CHI '11
  • DOI: 10.1145/1978942.1978963

Analysis of composition of microbiomes: a novel method for studying microbial composition
journal, May 2015

  • Mandal, Siddhartha; Van Treuren, Will; White, Richard A.
  • Microbial Ecology in Health & Disease, Vol. 26, Issue 0
  • DOI: 10.3402/mehd.v26.27663

Fitting Multivariate Models to Community Data: a Comment on Distance-Based Redundancy Analysis
journal, January 2001

Manipulating the soil microbiome to increase soil health and plant fertility
journal, May 2012

  • Chaparro, Jacqueline M.; Sheflin, Amy M.; Manter, Daniel K.
  • Biology and Fertility of Soils, Vol. 48, Issue 5
  • DOI: 10.1007/s00374-012-0691-4

MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data
journal, April 2017

  • Dhariwal, Achal; Chong, Jasmine; Habib, Salam
  • Nucleic Acids Research, Vol. 45, Issue W1
  • DOI: 10.1093/nar/gkx295

Induction of Trehalase in Arabidopsis Plants Infected With the Trehalose-Producing Pathogen Plasmodiophora brassicae
journal, July 2002

  • Brodmann, David; Schuller, Astrid; Ludwig-Müller, Jutta
  • Molecular Plant-Microbe Interactions, Vol. 15, Issue 7
  • DOI: 10.1094/MPMI.2002.15.7.693

Metabolic profiles of soybean roots during early stages of Fusarium tucumaniae infection
journal, October 2014

  • Scandiani, María M.; Luque, Alicia G.; Razori, María V.
  • Journal of Experimental Botany, Vol. 66, Issue 1
  • DOI: 10.1093/jxb/eru432

Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens
journal, December 1998

  • Thomma, B. P. H. J.; Eggermont, K.; Penninckx, I. A. M. A.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 25
  • DOI: 10.1073/pnas.95.25.15107

Nitrogen signalling in plant interactions with associative and endophytic diazotrophic bacteria
journal, August 2014

  • Carvalho, T. L. G.; Balsemao-Pires, E.; Saraiva, R. M.
  • Journal of Experimental Botany, Vol. 65, Issue 19
  • DOI: 10.1093/jxb/eru319

Enabling Efficient and Confident Annotation of LC−MS Metabolomics Data through MS1 Spectrum and Time Prediction
journal, September 2016

‘Omics’ analyses of regulatory networks in plant abiotic stress responses
journal, April 2010

  • Urano, Kaoru; Kurihara, Yukio; Seki, Motoaki
  • Current Opinion in Plant Biology, Vol. 13, Issue 2
  • DOI: 10.1016/j.pbi.2009.12.006

Data Processing for GC-MS- and LC-MS-Based Untargeted Metabolomics
book, January 2019

Life cycle assessment of different bioenergy production systems including perennial and annual crops
journal, December 2011

Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum
journal, August 2013

  • Mace, Emma S.; Tai, Shuaishuai; Gilding, Edward K.
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3320

Prephenate aminotransferase directs plant phenylalanine biosynthesis via arogenate
journal, November 2010

  • Maeda, Hiroshi; Yoo, Heejin; Dudareva, Natalia
  • Nature Chemical Biology, Vol. 7, Issue 1
  • DOI: 10.1038/nchembio.485

The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems
journal, March 2008

Significance of Inducible Defense-related Proteins in Infected Plants
journal, September 2006

    Sort by:
    [ × clear filter / sort ]

    Similar Records in DOE PAGES and OSTI.GOV collections: