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Title: Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops

Abstract

Nitrogen is an essential element of life, and nitrogen availability often limits crop yields. Since the Green Revolution, massive amounts of synthetic nitrogen fertilizers have been produced from atmospheric nitrogen and natural gas, threatening the sustainability of global food production and degrading the environment. There is a need for alternative means of bringing nitrogen to crops, and taking greater advantage of biological nitrogen fixation seems a logical option. Legumes are used in most cropping systems around the world because of the nitrogen-fixing symbiosis with rhizobia. However, the world's three major cereal crops-rice, wheat, and maize-do not associate with rhizobia. In this review, we will survey how genetic approaches in rhizobia and their legume hosts allowed tremendous progress in understanding the molecular mechanisms controlling root nodule symbioses, and how this knowledge paves the way for engineering such associations in non-legume crops. We will also discuss challenges in bringing these systems into the field and how they can be surmounted by interdisciplinary collaborations between synthetic biologists, microbiologists, plant biologists, breeders, agronomists, and policymakers.

Authors:
; ; ; ORCiD logo
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Org.:
University of Wisconsin
OSTI Identifier:
1618586
Alternate Identifier(s):
OSTI ID: 1634771
Grant/Contract Number:  
SC0018247; SC0014377
Resource Type:
Published Article
Journal Name:
BMC Biology
Additional Journal Information:
Journal Name: BMC Biology Journal Volume: 17 Journal Issue: 1; Journal ID: ISSN 1741-7007
Publisher:
BioMed Central
Country of Publication:
United Kingdom
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 09 BIOMASS FUELS; nitrogen fixation; symbiosis; bioenergy crop

Citation Formats

Pankievicz, Vânia C. S., Irving, Thomas B., Maia, Lucas G. S., and Ané, Jean-Michel. Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops. United Kingdom: N. p., 2019. Web. doi:10.1186/s12915-019-0710-0.
Pankievicz, Vânia C. S., Irving, Thomas B., Maia, Lucas G. S., & Ané, Jean-Michel. Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops. United Kingdom. https://doi.org/10.1186/s12915-019-0710-0
Pankievicz, Vânia C. S., Irving, Thomas B., Maia, Lucas G. S., and Ané, Jean-Michel. Tue . "Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops". United Kingdom. https://doi.org/10.1186/s12915-019-0710-0.
@article{osti_1618586,
title = {Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops},
author = {Pankievicz, Vânia C. S. and Irving, Thomas B. and Maia, Lucas G. S. and Ané, Jean-Michel},
abstractNote = {Nitrogen is an essential element of life, and nitrogen availability often limits crop yields. Since the Green Revolution, massive amounts of synthetic nitrogen fertilizers have been produced from atmospheric nitrogen and natural gas, threatening the sustainability of global food production and degrading the environment. There is a need for alternative means of bringing nitrogen to crops, and taking greater advantage of biological nitrogen fixation seems a logical option. Legumes are used in most cropping systems around the world because of the nitrogen-fixing symbiosis with rhizobia. However, the world's three major cereal crops-rice, wheat, and maize-do not associate with rhizobia. In this review, we will survey how genetic approaches in rhizobia and their legume hosts allowed tremendous progress in understanding the molecular mechanisms controlling root nodule symbioses, and how this knowledge paves the way for engineering such associations in non-legume crops. We will also discuss challenges in bringing these systems into the field and how they can be surmounted by interdisciplinary collaborations between synthetic biologists, microbiologists, plant biologists, breeders, agronomists, and policymakers.},
doi = {10.1186/s12915-019-0710-0},
journal = {BMC Biology},
number = 1,
volume = 17,
place = {United Kingdom},
year = {2019},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s12915-019-0710-0

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Cited by: 4 works
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Figures / Tables:

Fig. 1 Fig. 1: Different types of nitrogen-fixing associations with plants. The three challenges of biological nitrogen fixation are solved with different efficiency by these types of interactions—energy source, oxygen protection, and transfer of fixed nitrogen to the plant. The efficiency of each bacterial partner is indicated by + (low), ++ (moderate),more » or +++ (high). The nitrogen fixation rates depend on the efficiency of the interaction. a Root nodule symbiosis, 50–465 kg N ha−1 y−1; b associative nitrogen fixation, 2–170 kg N ha−1 y−1; and c, d free-living nitrogen fixation, 1–80 kg N ha−1 y−1« less

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Works referenced in this record:

Maturation of Nitrogenase: a Biochemical Puzzle
journal, January 2005


Arbuscular mycorrhiza: the mother of plant root endosymbioses
journal, October 2008


Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation
journal, May 2012

  • Ivanov, S.; Fedorova, E. E.; Limpens, E.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 21
  • DOI: 10.1073/pnas.1200407109

Clustered Genes Required for the Synthesis of Heterocyst Envelope Polysaccharide in Anabaena sp. Strain PCC 7120
journal, February 2005


MtNODULE ROOT1 and MtNODULE ROOT2 Are Essential for Indeterminate Nodule Identity
journal, July 2018

  • Magne, Kevin; Couzigou, Jean-Malo; Schiessl, Katharina
  • Plant Physiology, Vol. 178, Issue 1
  • DOI: 10.1104/pp.18.00610

The "nitrogenase-protective" FeSII protein of Azotobacter vinelandii: overexpression, characterization, and crystallization
journal, October 1995

  • Moshiri, Farhad; Crouse, Brian R.; Johnson, Michael K.
  • Biochemistry, Vol. 34, Issue 40
  • DOI: 10.1021/bi00040a007

Expression of a functional oxygen-labile nitrogenase component in the mitochondrial matrix of aerobically grown yeast
journal, April 2016

  • López-Torrejón, Gema; Jiménez-Vicente, Emilio; Buesa, José María
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11426

Living inside plants: bacterial endophytes
journal, August 2011


Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca
journal, April 2012

  • Temme, K.; Zhao, D.; Voigt, C. A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 18
  • DOI: 10.1073/pnas.1120788109

A plant regulator controlling development of symbiotic root nodules
journal, November 1999

  • Schauser, Leif; Roussis, Andreas; Stiller, Jiri
  • Nature, Vol. 402, Issue 6758
  • DOI: 10.1038/46058

The ammonium excreting Azospirillum brasilense strain HM053: a new alternative inoculant for maize
journal, June 2019


What Does It Take to Evolve A Nitrogen-Fixing Endosymbiosis?
journal, March 2016


Robust biological nitrogen fixation in a model grass-bacterial association
journal, March 2015

  • Pankievicz, Vânia C. S.; do Amaral, Fernanda P.; Santos, Karina F. D. N.
  • The Plant Journal, Vol. 81, Issue 6
  • DOI: 10.1111/tpj.12777

The Green Roof Microbiome: Improving Plant Survival for Ecosystem Service Delivery
journal, February 2018

  • Fulthorpe, Roberta; MacIvor, J. Scott; Jia, Pu
  • Frontiers in Ecology and Evolution, Vol. 6
  • DOI: 10.3389/fevo.2018.00005

TOO MUCH LOVE, a Novel Kelch Repeat-Containing F-box Protein, Functions in the Long-Distance Regulation of the Legume–Rhizobium Symbiosis
journal, March 2013

  • Takahara, Masahiro; Magori, Shimpei; Soyano, Takashi
  • Plant and Cell Physiology, Vol. 54, Issue 4
  • DOI: 10.1093/pcp/pct022

State of the art in eukaryotic nitrogenase engineering
journal, December 2017


To Fix or Not To Fix: Controls on Free-Living Nitrogen Fixation in the Rhizosphere
journal, January 2019

  • Smercina, Darian N.; Evans, Sarah E.; Friesen, Maren L.
  • Applied and Environmental Microbiology, Vol. 85, Issue 6
  • DOI: 10.1128/AEM.02546-18

Isolation and Identification of Natural Endophytic Rhizobia from Rice (Oryza sativa L.) Through rDNA PCR-RFLP and Sequence Analysis
journal, January 2006

  • Singh, Ramesh K.; Mishra, Ravi P. N.; Jaiswal, Hemant K.
  • Current Microbiology, Vol. 52, Issue 2
  • DOI: 10.1007/s00284-005-0136-5

Evolution of root endosymbiosis with bacteria: how novel are nodules?
journal, February 2009


Isotopic analysis of cyanobacterial nitrogen fixation associated with subarctic lichen and bryophyte species
journal, April 2010

  • Gavazov, Konstantin S.; Soudzilovskaia, Nadejda A.; van Logtestijn, Richard S. P.
  • Plant and Soil, Vol. 333, Issue 1-2
  • DOI: 10.1007/s11104-010-0374-6

Optimizing [13N]N2 radiochemistry for nitrogen-fixation in root nodules of legumes
journal, June 2010

  • Kasel, Mirjam C. K.; Schueller, Michael J.; Ferrieri, Richard A.
  • Journal of Labelled Compounds and Radiopharmaceuticals, Vol. 53, Issue 9
  • DOI: 10.1002/jlcr.1786

Characterization of Herbaspirillum seropedicae gen. nov., sp. nov., a Root-Associated Nitrogen-Fixing Bacterium
journal, January 1986

  • Baldani, J. I.; Baldani, V. L. D.; Seldin, L.
  • International Journal of Systematic Bacteriology, Vol. 36, Issue 1
  • DOI: 10.1099/00207713-36-1-86

Biological nitrogen fixation in non-legume plants
journal, March 2013

  • Santi, Carole; Bogusz, Didier; Franche, Claudine
  • Annals of Botany, Vol. 111, Issue 5
  • DOI: 10.1093/aob/mct048

The Sym35 Gene Required for Root Nodule Development in Pea Is an Ortholog of Nin from Lotus japonicus
journal, February 2003

  • Borisov, Alexey Y.; Madsen, Lene H.; Tsyganov, Viktor E.
  • Plant Physiology, Vol. 131, Issue 3
  • DOI: 10.1104/pp.102.016071

Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont
journal, March 2018

  • Warshan, Denis; Liaimer, Anton; Pederson, Eric
  • Molecular Biology and Evolution, Vol. 35, Issue 5
  • DOI: 10.1093/molbev/msy029

Global inputs of biological nitrogen fixation in agricultural systems
journal, July 2008


Characterization of an oxygen-stable nitrogenase complex isolated from Azotobacter chroococcum
journal, September 1979


Molecular adaptations of H erbaspirillum seropedicae during colonization of the maize rhizosphere: H. seropedicae transcript profiles in maize rhizosphere
journal, June 2015

  • Balsanelli, Eduardo; Tadra-Sfeir, Michelle Z.; Faoro, Helisson
  • Environmental Microbiology, Vol. 18, Issue 8
  • DOI: 10.1111/1462-2920.12887

Transport and Metabolism in Legume-Rhizobia Symbioses
journal, April 2013


Medicago truncatula IPD3 Is a Member of the Common Symbiotic Signaling Pathway Required for Rhizobial and Mycorrhizal Symbioses
journal, November 2011

  • Horváth, Beatrix; Yeun, Li Huey; Domonkos, Ágota
  • Molecular Plant-Microbe Interactions, Vol. 24, Issue 11
  • DOI: 10.1094/MPMI-01-11-0015

Human health effects of a changing global nitrogen cycle
journal, June 2003


Potential precision of the δ15N natural abundance method in field estimates of nitrogen fixation by crop and pasture legumes in south-west Australia
journal, January 1994

  • Unkovich, Mj; Pate, Js; Sanford, P.
  • Australian Journal of Agricultural Research, Vol. 45, Issue 1
  • DOI: 10.1071/AR9940119

Signals and players in the transcriptional regulation of root responses by local and systemic N signaling in Arabidopsis thaliana
journal, March 2017

  • Bellegarde, Fanny; Gojon, Alain; Martin, Antoine
  • Journal of Experimental Botany, Vol. 68, Issue 10
  • DOI: 10.1093/jxb/erx062

Symbiotic Leghemoglobins Are Crucial for Nitrogen Fixation in Legume Root Nodules but Not for General Plant Growth and Development
journal, March 2005


Involvement of the ammonium transporter AmtB in nitrogenase regulation and ammonium excretion in Pseudomonas stutzeri A1501
journal, June 2012


Chemolithoautotrophic assimilation of dinitrogen by Streptomyces thermoautotrophicus UBT1: identification of an unusual N2-fixing system.
journal, January 1992


Ammonia?An Early Stable Product of Nitrogen Fixation by Soybean Root Nodules F. J. Bergersen
journal, January 1965

  • Bergersen, Fj
  • Australian Journal of Biological Sciences, Vol. 18, Issue 1
  • DOI: 10.1071/BI9650001

Genetic regulation of biological nitrogen fixation
journal, August 2004

  • Dixon, Ray; Kahn, Daniel
  • Nature Reviews Microbiology, Vol. 2, Issue 8
  • DOI: 10.1038/nrmicro954

Metabolic Integration of Bacterial Endosymbionts through Antimicrobial Peptides
journal, September 2017

  • Mergaert, Peter; Kikuchi, Yoshitomo; Shigenobu, Shuji
  • Trends in Microbiology, Vol. 25, Issue 9
  • DOI: 10.1016/j.tim.2017.04.007

Purification and In Vitro Activity of Mitochondria Targeted Nitrogenase Cofactor Maturase NifB
journal, September 2017

  • Burén, Stefan; Jiang, Xi; López-Torrejón, Gema
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01567

Current Usage of Symbiosis and Associated Terminology
journal, November 2012

  • Martin, Bradford D.; Schwab, Ernest
  • International Journal of Biology, Vol. 5, Issue 1
  • DOI: 10.5539/ijb.v5n1p32

Arabidopsis lateral root development: an emerging story
journal, July 2009


A Nitrogen-Fixing Endophyte of Sugarcane Stems (A New Role for the Apoplast)
journal, August 1994


Transfer of Nitrogen-fixation Genes by Conjugation in Klebsiella pneumoniae
journal, November 1971

  • Dixon, R. A.; Postgate, J. R.
  • Nature, Vol. 234, Issue 5323
  • DOI: 10.1038/234047a0

Diazotroph Community Characterization via a High-Throughput nifH Amplicon Sequencing and Analysis Pipeline
journal, November 2017

  • Gaby, John Christian; Rishishwar, Lavanya; Valderrama-Aguirre, Lina C.
  • Applied and Environmental Microbiology, Vol. 84, Issue 4
  • DOI: 10.1128/AEM.01512-17

Excretion of ammonium by Azospirillum brasilense mutants resistant to ethylenediamine
journal, July 1991

  • Machado, H. B.; Funayama, S.; Rigo, L. U.
  • Canadian Journal of Microbiology, Vol. 37, Issue 7
  • DOI: 10.1139/m91-092

Symbiosis and the social network of higher plants
journal, February 2013

  • Venkateshwaran, Muthusubramanian; Volkening, Jeremy D.; Sussman, Michael R.
  • Current Opinion in Plant Biology, Vol. 16, Issue 1
  • DOI: 10.1016/j.pbi.2012.11.007

Polyprotein strategy for stoichiometric assembly of nitrogen fixation components for synthetic biology
journal, July 2018

  • Yang, Jianguo; Xie, Xiaqing; Xiang, Nan
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 36
  • DOI: 10.1073/pnas.1804992115

Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013


Comparative transcriptome analysis of Poncirus trifoliata identifies a core set of genes involved in arbuscular mycorrhizal symbiosis
journal, July 2018

  • An, Jianyong; Sun, Mengqian; van Velzen, Robin
  • Journal of Experimental Botany, Vol. 69, Issue 21
  • DOI: 10.1093/jxb/ery283

Nitrogen-fixing bacteria of the genusBeijerinckia Derx in the rhizosphere of sugar cane
journal, November 1961


Staying in touch: mechanical signals in plant–microbe interactions
journal, August 2014

  • Jayaraman, Dhileepkumar; Gilroy, Simon; Ané, Jean-Michel
  • Current Opinion in Plant Biology, Vol. 20
  • DOI: 10.1016/j.pbi.2014.05.003

Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition
journal, June 2006

  • Gleason, Cynthia; Chaudhuri, Shubho; Yang, Tianbao
  • Nature, Vol. 441, Issue 7097
  • DOI: 10.1038/nature04812

Rhizobia Can Induce Nodules in White Clover by “Hijacking” Mature Cortical Cells Activated During Lateral Root Development
journal, February 2000

  • Mathesius, Ulrike; Weinman, Jeremy J.; Rolfe, Barry G.
  • Molecular Plant-Microbe Interactions, Vol. 13, Issue 2
  • DOI: 10.1094/MPMI.2000.13.2.170

Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants
journal, March 2013


Receptor-mediated exopolysaccharide perception controls bacterial infection
journal, July 2015

  • Kawaharada, Y.; Kelly, S.; Nielsen, M. Wibroe
  • Nature, Vol. 523, Issue 7560
  • DOI: 10.1038/nature14611

Endophytic nitrogen fixation in sugarcane: present knowledge and future applications
journal, May 2003

  • Boddey, Robert M.; Urquiaga, Segundo; Alves, Bruno J. R.
  • Plant and Soil, Vol. 252, Issue 1
  • DOI: 10.1023/A:1024152126541

Multiple benefits of legumes for agriculture sustainability: an overview
journal, February 2017

  • Stagnari, Fabio; Maggio, Albino; Galieni, Angelica
  • Chemical and Biological Technologies in Agriculture, Vol. 4, Issue 1
  • DOI: 10.1186/s40538-016-0085-1

Earth Microbiome Project and Global Systems Biology
journal, April 2018


Excretion of ammonium by a nifL mutant of Azotobacter vinelandii fixing nitrogen.
journal, January 1992


Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti Involves the Nodulation Factor-Dependent Induction of Root Hairs
journal, March 2005

  • Karas, Bogumil; Murray, Jeremy; Gorzelak, Monika
  • Plant Physiology, Vol. 137, Issue 4
  • DOI: 10.1104/pp.104.057513

Exopolysaccharide Biosynthesis Enables Mature Biofilm Formation on Abiotic Surfaces by Herbaspirillum seropedicae
journal, October 2014


The Role of Nitrogen Fixation in Crop Production
journal, November 1998


The art of isolating nitrogen-fixing bacteria from non-leguminous plants using N-free semi-solid media: a practical guide for microbiologists
journal, July 2014

  • Baldani, José Ivo; Reis, Veronica Massena; Videira, Sandy Sampaio
  • Plant and Soil, Vol. 384, Issue 1-2
  • DOI: 10.1007/s11104-014-2186-6

Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions
journal, May 2018


Potential for Nitrogen Fixation in Maize Genotypes in Brazil
journal, June 1975

  • Von Bulow, J. F. W.; Dobereiner, J.
  • Proceedings of the National Academy of Sciences, Vol. 72, Issue 6
  • DOI: 10.1073/pnas.72.6.2389

Medicago LYK3, an Entry Receptor in Rhizobial Nodulation Factor Signaling
journal, June 2007

  • Smit, Patrick; Limpens, Erik; Geurts, Rene
  • Plant Physiology, Vol. 145, Issue 1
  • DOI: 10.1104/pp.107.100495

Hormonal Control of Lateral Root and Nodule Development in Legumes
journal, August 2015


Ammonium excretion, auxin production and effects of maize inoculation with ethylenediamine-resistant mutants of Pseudomonas sp.
journal, August 2018

  • Ramos, Luan da Luz; Rodrigues, Elisete Pains; Silva, Mayara Barbosa
  • Bragantia, Vol. 77, Issue 3
  • DOI: 10.1590/1678-4499.2017190

Improving photosynthesis and crop productivity by accelerating recovery from photoprotection
journal, November 2016

  • Kromdijk, Johannes; Głowacka, Katarzyna; Leonelli, Lauriebeth
  • Science, Vol. 354, Issue 6314
  • DOI: 10.1126/science.aai8878

Competition between rhizobia under different environmental conditions affects the nodulation of a legume
journal, March 2017


Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes
journal, April 2016

  • Mus, Florence; Crook, Matthew B.; Garcia, Kevin
  • Applied and Environmental Microbiology, Vol. 82, Issue 13
  • DOI: 10.1128/AEM.01055-16

Nitrogen fixation in eukaryotes – New models for symbiosis
journal, January 2007

  • Kneip, Christoph; Lockhart, Peter; Voß, Christine
  • BMC Evolutionary Biology, Vol. 7, Issue 1
  • DOI: 10.1186/1471-2148-7-55

The Symbiosome: Legume and Rhizobia Co-evolution toward a Nitrogen-Fixing Organelle?
journal, January 2018

  • Coba de la Peña, Teodoro; Fedorova, Elena; Pueyo, José J.
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.02229

Azospirillum: benefits that go far beyond biological nitrogen fixation
journal, May 2018


Activation of Symbiosis Signaling by Arbuscular Mycorrhizal Fungi in Legumes and Rice
journal, February 2015

  • Sun, Jongho; Miller, J. Benjamin; Granqvist, Emma
  • The Plant Cell, Vol. 27, Issue 3
  • DOI: 10.1105/tpc.114.131326

Expression of 16 Nitrogenase Proteins within the Plant Mitochondrial Matrix
journal, March 2017

  • Allen, Robert S.; Tilbrook, Kimberley; Warden, Andrew C.
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.00287

Chasing unicorns: Nodulation origins and the paradox of novelty
journal, October 2016


The Rules of Engagement in the Legume-Rhizobial Symbiosis
journal, December 2011


Increased plant uptake of nitrogen from 15N-depleted fertilizer using plant growth-promoting rhizobacteria
journal, September 2010


Succinate Transport Is Not Essential for Symbiotic Nitrogen Fixation by Sinorhizobium meliloti or Rhizobium leguminosarum
journal, September 2017

  • Mitsch, Michael J.; diCenzo, George C.; Cowie, Alison
  • Applied and Environmental Microbiology, Vol. 84, Issue 1
  • DOI: 10.1128/AEM.01561-17

How a century of ammonia synthesis changed the world
journal, September 2008

  • Erisman, Jan Willem; Sutton, Mark A.; Galloway, James
  • Nature Geoscience, Vol. 1, Issue 10
  • DOI: 10.1038/ngeo325

The Basis of Ammonium Release in nifLMutants of Azotobacter vinelandii
journal, December 1999


Effect of exogenous flavonoids on nodulation of pea (Pisum sativum L.)
journal, August 2002


Quantitative Imaging of Nitrogen Fixation by Individual Bacteria Within Animal Cells
journal, September 2007


Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems
journal, January 1999


Commonalities and Differences in Controlling Multipartite Intracellular Infections of Legume Roots by Symbiotic Microbes
journal, February 2018

  • Lace, Beatrice; Ott, Thomas
  • Plant and Cell Physiology, Vol. 59, Issue 4
  • DOI: 10.1093/pcp/pcy043

Expression of Active Subunit of Nitrogenase via Integration into Plant Organelle Genome
journal, August 2016


Diazotrophic Growth Allows Azotobacter vinelandii To Overcome the Deleterious Effects of a glnE Deletion
journal, April 2017

  • Mus, Florence; Tseng, Alex; Dixon, Ray
  • Applied and Environmental Microbiology, Vol. 83, Issue 13
  • DOI: 10.1128/AEM.00808-17

Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes
journal, June 2008


Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase
journal, March 2007

  • Marsh, John F.; Rakocevic, Alexandra; Mitra, Raka M.
  • Plant Physiology, Vol. 144, Issue 1
  • DOI: 10.1104/pp.106.093021

Streptomyces thermoautotrophicus does not fix nitrogen
journal, February 2016

  • MacKellar, Drew; Lieber, Lucas; Norman, Jeffrey S.
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep20086

Metabolism of Rhizobium Bacteroids
journal, January 2003

  • Lodwig, Emma; Poole, Philip
  • Critical Reviews in Plant Sciences, Vol. 22, Issue 1
  • DOI: 10.1080/713610850

Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases
journal, October 2003

  • Radutoiu, Simona; Madsen, Lene Heegaard; Madsen, Esben Bjørn
  • Nature, Vol. 425, Issue 6958
  • DOI: 10.1038/nature02039

A mass spectrometry method for measuring 15N incorporation into pheophytin
journal, August 2002


Diazotrophic endophytes: progress and prospects for nitrogen fixation in monocots
journal, September 1996


Quantitative Proteomic Analysis of the Interaction Between the Endophytic Plant-Growth-Promoting Bacterium Gluconacetobacter diazotrophicus and Sugarcane
journal, May 2011

  • Lery, Letícia M. S.; Hemerly, Adriana S.; Nogueira, Eduardo M.
  • Molecular Plant-Microbe Interactions, Vol. 24, Issue 5
  • DOI: 10.1094/MPMI-08-10-0178

Closing yield gaps through nutrient and water management
journal, August 2012

  • Mueller, Nathaniel D.; Gerber, James S.; Johnston, Matt
  • Nature, Vol. 490, Issue 7419
  • DOI: 10.1038/nature11420

Plant growth promotion in cereal and leguminous agricultural important plants: From microorganism capacities to crop production
journal, May 2014

  • Pérez-Montaño, F.; Alías-Villegas, C.; Bellogín, R. A.
  • Microbiological Research, Vol. 169, Issue 5-6
  • DOI: 10.1016/j.micres.2013.09.011

Legume LysM receptors mediate symbiotic and pathogenic signalling
journal, October 2017


Endophytic colonization of plant roots by nitrogen-fixing bacteria
journal, May 2003


Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria
journal, December 1998


Reconstruction and minimal gene requirements for the alternative iron-only nitrogenase in Escherichia coli
journal, August 2014

  • Yang, J.; Xie, X.; Wang, X.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 35
  • DOI: 10.1073/pnas.1411185111

N2 Fixation by non-heterocystous cyanobacteria
journal, February 1997


Challenges to develop nitrogen-fixing cereals by direct nif-gene transfer
journal, August 2014


Quantifying nitrogen-fixation in feather moss carpets of boreal forests
journal, October 2002

  • DeLuca, Thomas H.; Zackrisson, Olle; Nilsson, Marie-Charlotte
  • Nature, Vol. 419, Issue 6910
  • DOI: 10.1038/nature01051

Reconciling the incompatible: N2 fixation And O2
journal, December 1992


How Soil Biota Drive Ecosystem Stability
journal, December 2018


Rhizobium Lipo-Chitooligosaccharide Nodulation Factors: Signaling Molecules Mediating Recognition and Morphogenesis
journal, June 1996


Lipochitooligosaccharide recognition: an ancient story
journal, June 2014

  • Liang, Yan; Tóth, Katalin; Cao, Yangrong
  • New Phytologist, Vol. 204, Issue 2
  • DOI: 10.1111/nph.12898

Relationships for estimating N 2 fixation in legumes: incidence for N balance of legume-based cropping systems in Europe
journal, March 2015

  • Anglade, Juliette; Billen, Gilles; Garnier, Josette
  • Ecosphere, Vol. 6, Issue 3
  • DOI: 10.1890/ES14-00353.1

A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane
journal, May 1988

  • Cavalcante, Vladimir A.; Dobereiner, J.
  • Plant and Soil, Vol. 108, Issue 1
  • DOI: 10.1007/BF02370096

Rhizobium–legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS
journal, July 2015

  • Okazaki, Shin; Tittabutr, Panlada; Teulet, Albin
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.103

Yield of sugarcane varieties and their sugar quality grown in different soil types and inoculated with a diazotrophic bacteria consortium
journal, July 2017


Agricultural management of grain legumes: has it led to an increase in nitrogen fixation?
journal, March 2000


Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula
journal, June 2017

  • Wang, Qi; Yang, Shengming; Liu, Jinge
  • Proceedings of the National Academy of Sciences
  • DOI: 10.1073/pnas.1700715114

Biological nitrogen fixation: An efficient source of nitrogen for sustainable agricultural production?
journal, July 1995

  • Peoples, M. B.; Herridge, D. F.; Ladha, J. K.
  • Plant and Soil, Vol. 174, Issue 1-2
  • DOI: 10.1007/BF00032239

Impact of Plant Peptides on Symbiotic Nodule Development and Functioning
journal, July 2018

  • Kereszt, Attila; Mergaert, Peter; Montiel, Jesús
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.01026

Detection of nifH Sequences in Sugarcane ( Saccharum officinarum L.) and Pineapple ( Ananas comosus [L.] Merr.)
journal, April 2005


Tree Species Control Rates of Free-Living Nitrogen Fixation in a Tropical rain Forest
journal, October 2008

  • Reed, Sasha C.; Cleveland, Cory C.; Townsend, Alan R.
  • Ecology, Vol. 89, Issue 10
  • DOI: 10.1890/07-1430.1

Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes
journal, December 2003


Differential growth responses of Brachypodium distachyon genotypes to inoculation with plant growth promoting rhizobacteria
journal, February 2016

  • do Amaral, Fernanda P.; Pankievicz, Vânia C. S.; Arisi, Ana Carolina M.
  • Plant Molecular Biology, Vol. 90, Issue 6
  • DOI: 10.1007/s11103-016-0449-8

The oil-contaminated soil diazotroph Azoarcus olearius DQS-4 T is genetically and phenotypically similar to the model grass endophyte Azoarcus sp. BH72 : Genomic analysis of
journal, January 2017

  • Faoro, Helisson; Rene Menegazzo, Rodrigo; Battistoni, Federico
  • Environmental Microbiology Reports, Vol. 9, Issue 3
  • DOI: 10.1111/1758-2229.12502

Global patterns of terrestrial biological nitrogen (N 2 ) fixation in natural ecosystems
journal, June 1999

  • Cleveland, Cory C.; Townsend, Alan R.; Schimel, David S.
  • Global Biogeochemical Cycles, Vol. 13, Issue 2
  • DOI: 10.1029/1999GB900014

Evaluation of Primers Targeting the Diazotroph Functional Gene and Development of NifMAP – A Bioinformatics Pipeline for Analyzing nifH Amplicon Data
journal, April 2018

  • Angel, Roey; Nepel, Maximilian; Panhölzl, Christopher
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.00703

Inferring the Evolutionary History of Mo-Dependent Nitrogen Fixation from Phylogenetic Studies of nifK and nifDK
journal, July 2010


Nitrate leaching losses from soybeans (Glycine max L. Merr.)
journal, June 1990


Evolution of signal transduction in intracellular symbiosis
journal, November 2002


Genetic basis of cytokinin and auxin functions during root nodule development
journal, January 2013

  • Suzaki, Takuya; Ito, Momoyo; Kawaguchi, Masayoshi
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00042

Evidence from field nitrogen balance and 15N natural abundance data for the contribution of biological N2 fixation to Brazilian sugarcane varieties
journal, October 2011

  • Urquiaga, Segundo; Xavier, Rogério P.; de Morais, Rafael F.
  • Plant and Soil, Vol. 356, Issue 1-2
  • DOI: 10.1007/s11104-011-1016-3

Synergistic effects of plant-growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeonpea (Cajanus cajan)
journal, February 2006


Characterization of an oxygen-stable nitrogenase complex isolated from Azotobacter chroococcum
journal, September 1979


Feeding the world: improving photosynthetic efficiency for sustainable crop production
journal, February 2019

  • Simkin, Andrew J.; López-Calcagno, Patricia E.; Raines, Christine A.
  • Journal of Experimental Botany, Vol. 70, Issue 4
  • DOI: 10.1093/jxb/ery445

A Minimal Nitrogen Fixation Gene Cluster from Paenibacillus sp. WLY78 Enables Expression of Active Nitrogenase in Escherichia coli
journal, October 2013


Tough love: accommodating intracellular bacteria through directed secretion of antimicrobial peptides during the nitrogen-fixing symbiosis
journal, August 2018


Emerging Functions of Nodulin-Like Proteins in Non-Nodulating Plant Species
journal, January 2014

  • Denancé, Nicolas; Szurek, Boris; Noël, Laurent D.
  • Plant and Cell Physiology, Vol. 55, Issue 3
  • DOI: 10.1093/pcp/pct198

Global nitrogen budgets in cereals: A 50-year assessment for maize, rice and wheat production systems
journal, January 2016

  • Ladha, J. K.; Tirol-Padre, A.; Reddy, C. K.
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep19355

Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume-Rhizobium Interactions
journal, March 2018


Efficiency of Symbiotic Nitrogen Fixation in Legumes
journal, June 1980


Membrane association of Klebsiella pneumoniae NifL is affected by molecular oxygen and combined nitrogen
journal, March 2002

  • Klopprogge, Kai; Grabbe, Roman; Hoppert, Michael
  • Archives of Microbiology, Vol. 177, Issue 3
  • DOI: 10.1007/s00203-001-0379-x

Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms.
journal, March 1995

  • Soltis, D. E.; Soltis, P. S.; Morgan, D. R.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 7
  • DOI: 10.1073/pnas.92.7.2647

Host genotype and age shape the leaf and root microbiomes of a wild perennial plant
journal, July 2016

  • Wagner, Maggie R.; Lundberg, Derek S.; del Rio, Tijana G.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12151

Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota
journal, August 2018


Arabidopsis NIN-like transcription factors have a central role in nitrate signalling
journal, March 2013

  • Konishi, Mineko; Yanagisawa, Shuichi
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms2621

The Environmental Costs and Benefits of Fracking
journal, October 2014


Does a Common Pathway Transduce Symbiotic Signals in Plant–Microbe Interactions?
journal, February 2016


Positioning the nodule, the hormone dictum
journal, February 2009

  • Ding, Yiliang; Oldroyd, Giles E. D.
  • Plant Signaling & Behavior, Vol. 4, Issue 2
  • DOI: 10.4161/psb.4.2.7693

Agricultural sustainability and intensive production practices
journal, August 2002

  • Tilman, David; Cassman, Kenneth G.; Matson, Pamela A.
  • Nature, Vol. 418, Issue 6898
  • DOI: 10.1038/nature01014

Metabolic engineering of a diazotrophic bacterium improves ammonium release and biofertilization of plants and microalgae
journal, March 2017

  • Ambrosio, Rafael; Ortiz-Marquez, Juan Cesar Federico; Curatti, Leonardo
  • Metabolic Engineering, Vol. 40
  • DOI: 10.1016/j.ymben.2017.01.002

Contribution of biological nitrogen fixation to Elephant grass (Pennisetum purpureum Schum.)
journal, September 2011

  • de Morais, Rafael F.; Quesada, Diego M.; Reis, Veronica M.
  • Plant and Soil, Vol. 356, Issue 1-2
  • DOI: 10.1007/s11104-011-0944-2

The diversity of actinorhizal symbiosis
journal, March 2012


The Critical E 4 State of Nitrogenase Catalysis
journal, July 2018


CYCLOPS, A DNA-Binding Transcriptional Activator, Orchestrates Symbiotic Root Nodule Development
journal, February 2014


Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules.
journal, January 1988


Biological nitrogen fixation associated with sugar cane and rice: Contributions and prospects for improvement
journal, July 1995

  • Boddey, R. M.; de Oliveira, O. C.; Urquiaga, S.
  • Plant and Soil, Vol. 174, Issue 1-2
  • DOI: 10.1007/BF00032247

Nitrogenase Structure and Function: A Biochemical-Genetic Perspective
journal, October 1995


How inefficient rhizobia prolong their existence within nodules
journal, April 2010


Methods for quantification of nitrogen fixation associated with gramineae
journal, January 1987


Primary transcripts of microRNAs encode regulatory peptides
journal, March 2015

  • Lauressergues, Dominique; Couzigou, Jean-Malo; Clemente, Hélène San
  • Nature, Vol. 520, Issue 7545
  • DOI: 10.1038/nature14346

Genomic features of bacterial adaptation to plants
journal, December 2017

  • Levy, Asaf; Salas Gonzalez, Isai; Mittelviefhaus, Maximilian
  • Nature Genetics, Vol. 50, Issue 1
  • DOI: 10.1038/s41588-017-0012-9

Nitrogen Fixation in Wheat Provided by Klebsiella pneumoniae 342
journal, October 2004

  • Iniguez, A. Leonardo; Dong, Yuemei; Triplett, Eric W.
  • Molecular Plant-Microbe Interactions, Vol. 17, Issue 10
  • DOI: 10.1094/MPMI.2004.17.10.1078

Effect of inoculation ofAzospirillum spp. on nitrogen accumulation by field-grown wheat
journal, February 1986

  • Boddey, Robert M.; Baldani, Vera L. D.; Baldani, Jose I.
  • Plant and Soil, Vol. 95, Issue 1
  • DOI: 10.1007/BF02378857

New insights into Nod factor biosynthesis: Analyses of chitooligomers and lipo-chitooligomers of Rhizobium sp. IRBG74 mutants
journal, November 2016


Predominant nifH transcript phylotypes related to Rhizobium rosettiformans in field-grown sugarcane plants and in Norway spruce : Transcription of
journal, January 2011


Branching out in new directions: the control of root architecture by lateral root formation
journal, August 2008


Products of Biological Nitrogen Fixation in Higher Plants: Synthesis, Transport, and Metabolism
journal, June 1986


Nitrogen Fixation in Cereals
journal, August 2018

  • Rosenblueth, Mónica; Ormeño-Orrillo, Ernesto; López-López, Aline
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.01794

Azorhizobium caulinodans PIIand GlnK Proteins Control Nitrogen Fixation and Ammonia Assimilation
journal, April 1999


Medicago Plants Control Nodulation by Regulating Proteolysis of the Receptor-Like Kinase DMI2
journal, May 2018

  • Pan, Huairong; Stonoha-Arther, Christina; Wang, Dong
  • Plant Physiology, Vol. 177, Issue 2
  • DOI: 10.1104/pp.17.01542

Rhizobia: from saprophytes to endosymbionts
journal, January 2018

  • Poole, Philip; Ramachandran, Vinoy; Terpolilli, Jason
  • Nature Reviews Microbiology, Vol. 16, Issue 5
  • DOI: 10.1038/nrmicro.2017.171

Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes
journal, January 2012


The "oxygen paradox" of dinitrogen-fixing bacteria
journal, March 2000

  • Marchal, K.; Vanderleyden, J.
  • Biology and Fertility of Soils, Vol. 30, Issue 5-6
  • DOI: 10.1007/s003740050017

Research Progress and Perspectives of Nitrogen Fixing Bacterium, Gluconacetobacter diazotrophicus , in Monocot Plants
journal, January 2014

  • Eskin, N.; Vessey, K.; Tian, L.
  • International Journal of Agronomy, Vol. 2014
  • DOI: 10.1155/2014/208383

Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72
journal, October 2006

  • Krause, Andrea; Ramakumar, Adarsh; Bartels, Daniela
  • Nature Biotechnology, Vol. 24, Issue 11
  • DOI: 10.1038/nbt1243

A Conformational Switch Triggers Nitrogenase Protection from Oxygen Damage by Shethna Protein II (FeSII)
journal, December 2015

  • Schlesier, Julia; Rohde, Michael; Gerhardt, Stefan
  • Journal of the American Chemical Society, Vol. 138, Issue 1
  • DOI: 10.1021/jacs.5b10341

Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems
journal, July 2013

  • Vitousek, Peter M.; Menge, Duncan N. L.; Reed, Sasha C.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621
  • DOI: 10.1098/rstb.2013.0119

Agronomic applications of azospirillum: An evaluation of 20 years worldwide field inoculation
journal, December 1994


Importance of Poly-3-Hydroxybutyrate Metabolism to the Ability of Herbaspirillum seropedicae To Promote Plant Growth
journal, January 2019

  • Silveira Alves, Luis Paulo; Plucani do Amaral, Fernanda; Kim, Daewon
  • Applied and Environmental Microbiology, Vol. 85, Issue 6
  • DOI: 10.1128/AEM.02586-18

Nitrogen Fixation by Gunnera–Nostoc Symbiosis
journal, December 1969


Effects of inoculation with plant growth-promoting rhizobacteria on resident rhizosphere microorganisms
journal, November 2007


Evolution of the plant–microbe symbiotic ‘toolkit’
journal, June 2013

  • Delaux, Pierre-Marc; Séjalon-Delmas, Nathalie; Bécard, Guillaume
  • Trends in Plant Science, Vol. 18, Issue 6
  • DOI: 10.1016/j.tplants.2013.01.008

Symbiotic Nitrogen Fixation
journal, July 1995

  • Mylona, Panagiota; Pawlowski, Katharina; Bisseling, Ton
  • The Plant Cell, Vol. 7, Issue 7
  • DOI: 10.2307/3870043

Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.