skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Integrated analysis of zone-specific protein and metabolite profiles within nitrogen-fixing Medicago truncatula-Sinorhizobium medicae nodules

Abstract

Symbiotic nitrogen fixation (SNF) between rhizobia and legumes requires metabolic coordination within specialized root organs called nodules. Nodules formed in the symbiosis between S. medicae and barrel medic (M. truncatula) are indeterminate, cylindrical, and contain spatially distinct developmental zones. Bacteria in the infection zone II (ZII), interzone II-III (IZ), and nitrogen fixation zone III (ZIII) represent different stages in the metabolic progression from free-living bacteria into nitrogen fixing bacteroids. To better understand the coordination of plant and bacterial metabolism within the nodule, we used liquid and gas chromatography coupled to tandem mass spectrometry (MS) to observe protein and metabolite profiles representative of ZII, IZ, ZIII, whole-nodule, and primary root. Our MS-based approach confidently identified 361 S. medicae proteins and 888 M. truncatula proteins, as well as 160 metabolites from each tissue. The data are consistent with several organ- and zone-specific protein and metabolite localization patterns characterized previously. Here, we used our comprehensive dataset to demonstrate how multiple branches of primary metabolism are coordinated between symbionts and zones, including central carbon, fatty acid, and amino acid metabolism. For example, M. truncatula glycolysis enzymes accumulate from zone I to zone III within the nodule, while equivalent S. medicae enzymes decrease in abundance.more » We also show the localization of S. medicae's transition to dicarboxylic acid-dependent carbon metabolism within the IZ. The spatial abundance patterns of S. medicae fatty acid (FA) biosynthesis enzymes indicate an increased demand for FA production in the IZ and ZIII as compared to ZI. Our observations provide a resource for those seeking to understand coordinated physiological changes during the development of SNF.« less

Authors:
ORCiD logo [1];  [2];  [2];  [1];  [1];  [3]
  1. Washington State Univ., Pullman, WA (United States). Molecular Plant Science Program and Inst. of Biological Chemistry
  2. Washington State Univ., Pullman, WA (United States). Inst. of Biological Chemistry
  3. Centre National de la Recherche Scientifique (CNRS), Annecy-le-Vieux (France)
Publication Date:
Research Org.:
Washington State Univ., Pullman, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1372597
Alternate Identifier(s):
OSTI ID: 1392986
Grant/Contract Number:  
FG03-96ER20225
Resource Type:
Journal Article: Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 12; Journal Issue: 7; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Ogden, Aaron J., Gargouri, Mahmoud, Park, JeongJin, Gang, David R., Kahn, Michael L., and Mergaert, Peter. Integrated analysis of zone-specific protein and metabolite profiles within nitrogen-fixing Medicago truncatula-Sinorhizobium medicae nodules. United States: N. p., 2017. Web. doi:10.1371/journal.pone.0180894.
Ogden, Aaron J., Gargouri, Mahmoud, Park, JeongJin, Gang, David R., Kahn, Michael L., & Mergaert, Peter. Integrated analysis of zone-specific protein and metabolite profiles within nitrogen-fixing Medicago truncatula-Sinorhizobium medicae nodules. United States. doi:10.1371/journal.pone.0180894.
Ogden, Aaron J., Gargouri, Mahmoud, Park, JeongJin, Gang, David R., Kahn, Michael L., and Mergaert, Peter. Mon . "Integrated analysis of zone-specific protein and metabolite profiles within nitrogen-fixing Medicago truncatula-Sinorhizobium medicae nodules". United States. doi:10.1371/journal.pone.0180894.
@article{osti_1372597,
title = {Integrated analysis of zone-specific protein and metabolite profiles within nitrogen-fixing Medicago truncatula-Sinorhizobium medicae nodules},
author = {Ogden, Aaron J. and Gargouri, Mahmoud and Park, JeongJin and Gang, David R. and Kahn, Michael L. and Mergaert, Peter},
abstractNote = {Symbiotic nitrogen fixation (SNF) between rhizobia and legumes requires metabolic coordination within specialized root organs called nodules. Nodules formed in the symbiosis between S. medicae and barrel medic (M. truncatula) are indeterminate, cylindrical, and contain spatially distinct developmental zones. Bacteria in the infection zone II (ZII), interzone II-III (IZ), and nitrogen fixation zone III (ZIII) represent different stages in the metabolic progression from free-living bacteria into nitrogen fixing bacteroids. To better understand the coordination of plant and bacterial metabolism within the nodule, we used liquid and gas chromatography coupled to tandem mass spectrometry (MS) to observe protein and metabolite profiles representative of ZII, IZ, ZIII, whole-nodule, and primary root. Our MS-based approach confidently identified 361 S. medicae proteins and 888 M. truncatula proteins, as well as 160 metabolites from each tissue. The data are consistent with several organ- and zone-specific protein and metabolite localization patterns characterized previously. Here, we used our comprehensive dataset to demonstrate how multiple branches of primary metabolism are coordinated between symbionts and zones, including central carbon, fatty acid, and amino acid metabolism. For example, M. truncatula glycolysis enzymes accumulate from zone I to zone III within the nodule, while equivalent S. medicae enzymes decrease in abundance. We also show the localization of S. medicae's transition to dicarboxylic acid-dependent carbon metabolism within the IZ. The spatial abundance patterns of S. medicae fatty acid (FA) biosynthesis enzymes indicate an increased demand for FA production in the IZ and ZIII as compared to ZI. Our observations provide a resource for those seeking to understand coordinated physiological changes during the development of SNF.},
doi = {10.1371/journal.pone.0180894},
journal = {PLoS ONE},
number = 7,
volume = 12,
place = {United States},
year = {Mon Jul 10 00:00:00 EDT 2017},
month = {Mon Jul 10 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1371/journal.pone.0180894

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

The Molecular-Genetics of Nitrogen Assimilation Into Amino Acids In Higher Plants
journal, June 1996

  • Lam, H.-M.; Coschigano, K. T.; Oliveira, I. C.
  • Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1, p. 569-593
  • DOI: 10.1146/annurev.arplant.47.1.569

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27