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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

Journal Article · · BMC Biology

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.

Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE
Contributing Organization:
University of Wisconsin
Grant/Contract Number:
SC0018247; SC0014377
OSTI ID:
1618586
Alternate ID(s):
OSTI ID: 1634771
Journal Information:
BMC Biology, Vol. 17, Issue 1; ISSN 1741-7007
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 84 works
Citation information provided by
Web of Science

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  • Kasel, Mirjam C. K.; Schueller, Michael J.; Ferrieri, Richard A.
  • Journal of Labelled Compounds and Radiopharmaceuticals, Vol. 53, Issue 9 https://doi.org/10.1002/jlcr.1786
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Feeding the world: improving photosynthetic efficiency for sustainable crop production journal February 2019
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Host genotype and age shape the leaf and root microbiomes of a wild perennial plant text January 2016
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Biological nitrogen fixation: An efficient source of nitrogen for sustainable agricultural production? book January 1995
Isolation and Identification of Natural Endophytic Rhizobia from Rice (Oryza sativa L.) Through rDNA PCR-RFLP and Sequence Analysis journal April 2006
Rhizobium meliloti Lipooligosaccharide Nodulation Factors: Different Structural Requirements for Bacterial Entry into Target Root Hair Cells and Induction of Plant Symbiotic Developmental Responses journal October 1994
Ammonium excretion, auxin production and effects of maize inoculation with ethylenediamine-resistant mutants of Pseudomonas sp. dataset January 2018
Biological nitrogen fixation: An efficient source of nitrogen for sustainable agricultural production? journal July 1995
Membrane association of Klebsiella pneumoniae NifL is affected by molecular oxygen and combined nitrogen journal March 2002
The "oxygen paradox" of dinitrogen-fixing bacteria journal March 2000
The diversity of actinorhizal symbiosis journal March 2012
Differential growth responses of Brachypodium distachyon genotypes to inoculation with plant growth promoting rhizobacteria journal February 2016
Contribution of biological nitrogen fixation to Elephant grass (Pennisetum purpureum Schum.) journal September 2011
Evidence from field nitrogen balance and 15N natural abundance data for the contribution of biological N2 fixation to Brazilian sugarcane varieties journal October 2011
Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions journal May 2018
Molecular basis of symbiotic host specificity in rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals journal December 1991
Increased plant uptake of nitrogen from 15N-depleted fertilizer using plant growth-promoting rhizobacteria journal September 2010
Implications of Azospirillum brasilense inoculation and nutrient addition on maize in soils of the Brazilian Cerrado under greenhouse and field conditions journal October 2013
CYCLOPS, A DNA-Binding Transcriptional Activator, Orchestrates Symbiotic Root Nodule Development journal February 2014
Fertiliser availability in a resource-limited world: Production and recycling of nitrogen and phosphorus journal January 2011
Plant growth promotion in cereal and leguminous agricultural important plants: From microorganism capacities to crop production journal May 2014
Living inside plants: bacterial endophytes journal August 2011
Symbiosis and the social network of higher plants journal February 2013
Staying in touch: mechanical signals in plant–microbe interactions journal August 2014
Legume LysM receptors mediate symbiotic and pathogenic signalling journal October 2017
Uptake of bacteria into living plant cells, the unifying and distinct feature of the nitrogen-fixing root nodule symbiosis journal August 2018
How inefficient rhizobia prolong their existence within nodules journal April 2010
Evolution of the plant–microbe symbiotic ‘toolkit’ journal June 2013
How Soil Biota Drive Ecosystem Stability journal December 2018
Metabolic engineering of a diazotrophic bacterium improves ammonium release and biofertilization of plants and microalgae journal March 2017
Evolution of signal transduction in intracellular symbiosis journal November 2002
The "nitrogenase-protective" FeSII protein of Azotobacter vinelandii: overexpression, characterization, and crystallization journal October 1995
A Conformational Switch Triggers Nitrogenase Protection from Oxygen Damage by Shethna Protein II (FeSII) journal December 2015
Transfer of Nitrogen-fixation Genes by Conjugation in Klebsiella pneumoniae journal November 1971
A plant regulator controlling development of symbiotic root nodules journal November 1999
Rhizobium–legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS journal July 2015
Agricultural sustainability and intensive production practices journal August 2002
Quantifying nitrogen-fixation in feather moss carpets of boreal forests journal October 2002
Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases journal October 2003
Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition journal June 2006
Arabidopsis NIN-like transcription factors have a central role in nitrate signalling journal March 2013
How a century of ammonia synthesis changed the world journal September 2008
Rhizobia: from saprophytes to endosymbionts journal January 2018
Arbuscular mycorrhiza: the mother of plant root endosymbioses journal October 2008
Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants journal March 2013
Genetic regulation of biological nitrogen fixation journal August 2004
Erroneous predictions of auxotrophies by CarveMe journal December 2022
Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation journal May 2012
Potential for Nitrogen Fixation in Maize Genotypes in Brazil journal June 1975
Effect of exogenous flavonoids on nodulation of pea (Pisum sativum L.) journal August 2002
Signals and players in the transcriptional regulation of root responses by local and systemic N signaling in Arabidopsis thaliana journal March 2017
Comparative transcriptome analysis of Poncirus trifoliata identifies a core set of genes involved in arbuscular mycorrhizal symbiosis journal July 2018
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
Rhizobia Can Induce Nodules in White Clover by “Hijacking” Mature Cortical Cells Activated During Lateral Root Development journal February 2000
Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems journal July 2013
Characterization of Herbaspirillum seropedicae gen. nov., sp. nov., a Root-Associated Nitrogen-Fixing Bacterium journal January 1986
Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti Involves the Nodulation Factor-Dependent Induction of Root Hairs journal March 2005
A Nitrogen-Fixing Endophyte of Sugarcane Stems (A New Role for the Apoplast) journal August 1994
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
The Azorhizobium caulinodans nitrogen-fixation regulatory gene, nifA, is controlled by the cellular nitrogen and oxygen status journal June 1989
Rhizobium leguminosarum has two glucosamine syntheses, GImS and NodM, required for nodulation and development of nitrogen-fixing nodules journal April 1992
Reconciling the incompatible: N2 fixation And O2 journal December 1992
Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation: Tansley review journal February 2007
Branching out in new directions: the control of root architecture by lateral root formation journal August 2008
Azospirillum , a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects journal October 2000
Predominant nifH transcript phylotypes related to Rhizobium rosettiformans in field-grown sugarcane plants and in Norway spruce : Transcription of journal January 2011
Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules. journal January 1988
The Basis of Ammonium Release in nifLMutants of Azotobacter vinelandii journal December 1999
Clustered Genes Required for the Synthesis of Heterocyst Envelope Polysaccharide in Anabaena sp. Strain PCC 7120 journal February 2005
Transport and Metabolism in Legume-Rhizobia Symbioses journal April 2013
The Environmental Costs and Benefits of Fracking journal October 2014
The Rules of Engagement in the Legume-Rhizobial Symbiosis journal December 2011
Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes journal June 2008
Nitrogenase Structure and Function: A Biochemical-Genetic Perspective journal October 1995
Efficiency of Symbiotic Nitrogen Fixation in Legumes journal June 1980
Research Progress and Perspectives of Nitrogen Fixing Bacterium, Gluconacetobacter diazotrophicus , in Monocot Plants journal January 2014
Azospirillum: benefits that go far beyond biological nitrogen fixation journal May 2018
Exopolysaccharide Biosynthesis Enables Mature Biofilm Formation on Abiotic Surfaces by Herbaspirillum seropedicae journal October 2014
Expression of Active Subunit of Nitrogenase via Integration into Plant Organelle Genome journal August 2016
Streptomyces thermoautotrophicus does not fix nitrogen text January 2016
Tree Species Control Rates of Free-Living Nitrogen Fixation in a Tropical rain Forest journal October 2008
The Green Roof Microbiome: Improving Plant Survival for Ecosystem Service Delivery journal February 2018
Genetic basis of cytokinin and auxin functions during root nodule development journal January 2013
Expression of 16 Nitrogenase Proteins within the Plant Mitochondrial Matrix journal March 2017
The Symbiosome: Legume and Rhizobia Co-evolution toward a Nitrogen-Fixing Organelle? journal January 2018
Impact of Plant Peptides on Symbiotic Nodule Development and Functioning journal July 2018
Hormonal Control of Lateral Root and Nodule Development in Legumes journal August 2015
Chasing unicorns: Nodulation origins and the paradox of novelty journal October 2016
Ammonium excretion, auxin production and effects of maize inoculation with ethylenediamine-resistant mutants of Pseudomonas sp. dataset January 2018

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