Plant hormonal regulation of nitrogen-fixing nodule organogenesis

Legumes have evolved symbiotic interactions with rhizobial bacteria to efficiently utilize nitrogen. Recent progress in symbiosis has revealed several key components of host plants required for nitrogen-fixing nodule organogenesis, in which complicated metabolic and signaling pathways in the host plant are reprogrammed to generate nodules in the cortex upon perception of the rhizobial Nod factor. Following the recognition of Nod factors, plant hormones are likely to be essential throughout nodule organogenesis for integration of developmental and environmental signaling cues into nodule development. Here, we review the molecular events involved in plant hormonal regulation and signaling cross-talk for nitrogen-fixing nodule development, and discuss how these signaling networks are integrated into Nod factor-mediated signaling during plantmicrobe interactions.

• Publication year

  2012

• Venue

  Molecules and Cells

• Publication date

  2012-07-20

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1007/s10059-012-0131-1PMID 22820920PMCID PMC3887813
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• A MAP Kinase Kinase Interacts with SymRK and Regulates Nodule Organogenesis in Lotus japonicus[C][W]

  2012cited by this paper
• MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula.

  2011influential reference
• Strigolactones promote nodulation in pea

  2011cited by this paper
• Interplay of flg22-induced defence responses and nodulation in Lotus japonicus

  2011cited by this paper
• Mitogen-activated protein kinase signaling in plants under abiotic stress

  2011cited by this paper
• Plant primary meristems: shared functions and regulatory mechanisms.

  2010cited by this paper
• Plant-microbe communications for symbiosis.

  2010cited by this paper
• First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa)

  2010cited by this paper
• Plant and Animal Sensors of Conserved Microbial Signatures

  2010cited by this paper
• CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically1[C][W][OA]

  2010influential reference
• How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground

  2010cited by this paper
• The strigolactone story.

  2010cited by this paper
• Molecular analysis of legume nodule development and autoregulation.

  2010cited by this paper
• The unbearable naivety of legumes in symbiosis.

  2009cited by this paper
• Evolution of root endosymbiosis with bacteria: How novel are nodules?

  2009cited by this paper
• A novel ABA insensitive mutant of Lotus japonicus with a wilty phenotype displays unaltered nodulation regulation.

  2009cited by this paper
• Roles for Auxin, Cytokinin, and Strigolactone in Regulating Shoot Branching1[C][W][OA]

  2009cited by this paper
• Gibberellin controls the nodulation signaling pathway in Lotus japonicus.

  2009cited by this paper
• GRAS Proteins Form a DNA Binding Complex to Induce Gene Expression during Nodulation Signaling in Medicago truncatula[W]

  2009cited by this paper
• Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation.

  2009cited by this paper
• Too much love, a root regulator associated with the long-distance control of nodulation in Lotus japonicus.

  2009cited by this paper
• CYCLOPS, a mediator of symbiotic intracellular accommodation

  2008influential reference
• Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants.

  2008cited by this paper
• The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations.

  2008cited by this paper
• EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation in Medicago truncatula[W]

  2008influential reference
• Strigolactone inhibition of shoot branching

  2008cited by this paper
• Inhibition of shoot branching by new terpenoid plant hormones

  2008cited by this paper
• Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling

  2008cited by this paper
• Arbuscular mycorrhiza: the mother of plant root endosymbioses

  2008cited by this paper
• Coordinating nodule morphogenesis with rhizobial infection in legumes.

  2008cited by this paper
• Abscisic Acid Coordinates Nod Factor and Cytokinin Signaling during the Regulation of Nodulation in Medicago truncatula

  2008cited by this paper
• Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK.

  2008cited by this paper
• LysM domains mediate lipochitin–oligosaccharide recognition and Nfr genes extend the symbiotic host range

  2007cited by this paper
• Overlap of Proteome Changes in Medicago truncatula in Response to Auxin and Sinorhizobium meliloti1[W][OA]

  2007cited by this paper
• Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants.

  2007cited by this paper
• 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase1 Interacts with NORK and Is Crucial for Nodulation in Medicago truncatula

  2007cited by this paper
• A Cytokinin Perception Mutant Colonized by Rhizobium in the Absence of Nodule Organogenesis

  2007cited by this paper
• Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase1

  2007cited by this paper
• A Gain-of-Function Mutation in a Cytokinin Receptor Triggers Spontaneous Root Nodule Organogenesis

  2007cited by this paper
• AP2-ERF Transcription Factors Mediate Nod Factor–Dependent Mt ENOD11 Activation in Root Hairs via a Novel cis-Regulatory Motif[W]

  2007cited by this paper
• Auxin and nitric oxide control indeterminate nodule formation

  2007cited by this paper
• An ERF Transcription Factor in Medicago truncatula That Is Essential for Nod Factor Signal Transduction[W]

  2007influential reference
• Silencing the Flavonoid Pathway in Medicago truncatula Inhibits Root Nodule Formation and Prevents Auxin Transport Regulation by Rhizobia[W]

  2006cited by this paper
• Shoot-applied polyamines suppress nodule formation in soybean (Glycine max).

  2006cited by this paper
• Defective Long-Distance Auxin Transport Regulation in the Medicago truncatula super numeric nodules Mutant1[W]

  2006cited by this paper
• Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition

  2006cited by this paper
• Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development

  2006cited by this paper
• Shoot-applied MeJA suppresses root nodulation in Lotus japonicus.

  2006cited by this paper
• Lotus japonicus Nodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume1[C][W]

  2006influential reference
• The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti[W]

  2006cited by this paper
• Effects of Endogenous Salicylic Acid on Nodulation in the Model Legumes Lotus japonicus and Medicago truncatula1[W]

  2006influential reference
• Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 gene expression in nodule initiation.

  2006influential reference
• The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes.

  2006cited by this paper
• Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum.

  2006cited by this paper
• Long-distance signaling to control root nodule number.

  2006cited by this paper
• Integrative plant biology: role of phloem long-distance macromolecular trafficking.

  2006cited by this paper
• Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation.

  2006cited by this paper
• The Medicago truncatula Lysine Motif-Receptor-Like Kinase Gene Family Includes NFP and New Nodule-Expressed Genes1[W]

  2006cited by this paper
• Global gene expression in the rhizobial-legume symbiosis.

  2006cited by this paper
• Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators

  2005influential reference
• klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction.

  2005cited by this paper
• NSP1 of the GRAS Protein Family Is Essential for Rhizobial Nod Factor-Induced Transcription

  2005cited by this paper
• Gibberellins Are Involved in Nodulation of Sesbania rostrata1

  2005cited by this paper
• Transcript Analysis of Early Nodulation Events in Medicago truncatula12[W]

  2005cited by this paper
• Flavonoids as developmental regulators.

  2005influential reference
• Nodulation Phenotypes of Gibberellin and Brassinosteroid Mutants of Pea1

  2005cited by this paper
• Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses.

  2004cited by this paper
• Phosphorylation of 1-Aminocyclopropane-1-Carboxylic Acid Synthase by MPK6, a Stress-Responsive Mitogen-Activated Protein Kinase, Induces Ethylene Biosynthesis in Arabidopsisw⃞

  2004cited by this paper
• Medicago truncatula DMI1 Required for Bacterial and Fungal Symbioses in Legumes

  2004cited by this paper
• Brassinosteroids Interact with Auxin to Promote Lateral Root Development in Arabidopsis1

  2004cited by this paper
• Perception of Bradyrhizobium japonicum Nod factor by soybean [Glycine max (L.) Merr.] root hairs under abiotic stress conditions.

  2004cited by this paper
• Control of nodule number by the phytohormone abscisic Acid in the roots of two leguminous species.

  2004cited by this paper
• A Putative Ca2+ and Calmodulin-Dependent Protein Kinase Required for Bacterial and Fungal Symbioses

  2004cited by this paper
• Variation in Expression and Protein Localization of the PIN Family of Auxin Efflux Facilitator Proteins in Flavonoid Mutants with Altered Auxin Transport in Arabidopsis thaliana

  2004influential reference
• Brassinosteroids Do Not Undergo Long-Distance Transport in Pea. Implications for the Regulation of Endogenous Brassinosteroid Levels1

  2004cited by this paper
• Brassinosteroid Selectively Regulates PIN Gene Expression in Arabidopsis

  2004influential reference
• A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning.

  2004influential reference
• A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals

  2003cited by this paper
• The Sym35 Gene Required for Root Nodule Development in Pea Is an Ortholog of Nin from Lotus japonicus 1

  2003cited by this paper
• ETHYLENE RESPONSE FACTOR1 Integrates Signals from Ethylene and Jasmonate Pathways in Plant Defense Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007468.

  2003cited by this paper
• Activation of a Stress-Responsive Mitogen-Activated Protein Kinase Cascade Induces the Biosynthesis of Ethylene in Plants Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011411.

  2003cited by this paper
• The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation.

  2003cited by this paper
• Auxin distribution in Lotus japonicus during root nodule development

  2003cited by this paper
• Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases

  2003cited by this paper
• LysM Domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection

  2003cited by this paper
• Local, efflux-dependent auxin gradients as a common module for plant organ formation.

  2003cited by this paper
• HAR1 mediates systemic regulation of symbiotic organ development

  2002cited by this paper
• A genetic linkage map of the model legume Lotus japonicus and strategies for fast mapping of new loci.

  2002cited by this paper
• Shoot control of root development and nodulation is mediated by a receptor-like kinase

  2002cited by this paper
• Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases.

  2002cited by this paper
• A receptor kinase gene regulating symbiotic nodule development

  2002cited by this paper
• MAP kinase signalling cascade in Arabidopsis innate immunity

  2002cited by this paper
• Long-Distance Signaling in Nodulation Directed by a CLAVATA1-Like Receptor Kinase

  2002cited by this paper
• A plant receptor-like kinase required for both bacterial and fungal symbiosis

  2002cited by this paper
• Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction.

  2001cited by this paper
• Ethylene Inhibits the Nod Factor Signal Transduction Pathway of Medicago truncatula

  2001influential reference
• The phloem as a conduit for inter-organ communication.

  2001cited by this paper
• MAPK cascades in plant defense signaling.

  2001cited by this paper
• SIMKK, a Mitogen-Activated Protein Kinase (MAPK) Kinase, Is a Specific Activator of the Salt Stress–Induced MAPK, SIMK

  2000cited by this paper
• Four Genes of Medicago truncatula Controlling Components of a Nod Factor Transduction Pathway

  2000cited by this paper

• Boosting crop resilience to waterlogging through hormone-regulated root traits

  2026cites this paper
• Arbuscular mycorrhiza symbiosis—from molecular dialogues to biotechnological applications

  2025cites this paper
• Molecular dialogue in legume-rhizobium symbiosis: signaling mechanisms and genetic insights

  2025cites this paper
• Phenylpropanoids metabolism: recent insight into stress tolerance and plant development cues

  2025cites this paper
• Effect of Ascochyta rabiei on symbiotic efficiency and productivity of Cicer arietinum

  2025cites this paper
• Boosting Rhizobium-legume symbiosis: The role of nodule non-rhizobial bacteria in hormonal and nutritional regulation under stress.

  2025cites this paper
• Exogenous Application of ENOD40 and CEP1 Peptides Boosts Symbiotic Signaling Gene Expression and Productivity in Common Bean

  2025influential citation
• Differential symbiotic compatibilities between rhizobium strains and cultivated and wild soybeans revealed by anatomical and transcriptome analyses

  2024cites this paper
• Genomic Insights and Plant Growth-Promoting Potential of Rhizobial Strains from Agave americana

  2024cites this paper
• Bacterial Endophytes from Legumes Native to Arid Environments Are Promising Tools to Improve Mesorhizobium–Chickpea Symbiosis under Salinity

  2024cites this paper
• Interactions between Entomopathogenic Fungi and Insects and Prospects with Glycans

  2023cites this paper
• Enhancing Rhizobium–Legume Symbiosis and Reducing Nitrogen Fertilizer Use Are Potential Options for Mitigating Climate Change

  2023cites this paper
• MicroRNA 4407 modulates nodulation in soybean by repressing a root-specific ISOPENTENYLTRANSFERASE (GmIPT3).

  2023cites this paper
• Aspartic Acid-Based Nano-Copper Induces Resilience in Zea mays to Applied Lead Stress Via Conserving Photosynthetic Pigments and Triggering the Antioxidant Biosystem

  2023cites this paper
• Medicago truncatula-Sinorhizobium meliloti-Fusarium oxysporum Tripartite Interaction Alters Nodulation and Nitrogen Fixation

  2023cites this paper
• Common gene expression patterns are observed in rice roots during associations with plant growth-promoting bacteria, Herbaspirillum seropedicae and Azospirillum brasilense

  2022cites this paper
• Overexpression of Terpenoid Biosynthesis Genes Modifies Root Growth and Nodulation in Soybean (Glycine max)

  2022cites this paper
• Multiple Facets of Nitrogen: From Atmospheric Gas to Indispensable Agricultural Input

  2022cites this paper
• The plant growth-promoting bacteria, Azospirillum brasilense, induce a diverse array of genes in rice shoots and promote their growth

  2022cites this paper
• Phenylalanine Ammonia-Lyase Enzyme Activity in the Symbiotic System Glycine max – Bradyrhizobium japonicum by Seed Inoculation Different in Activity and Virulation Strain and Treatment with Fungicides

  2021cites this paper
• Overexpression of Terpenoid Biosynthesis Genes From Garden Sage (Salvia officinalis) Modulates Rhizobia Interaction and Nodulation in Soybean

  2021cites this paper
• Maternal effects on seedling development in Phaseolus vulgaris L.: the role of nitrogen management

  2021influential citation
• GmbZIP1 negatively regulates ABA-induced inhibition of nodulation by targeting GmENOD40–1 in soybean

  2021cites this paper
• Overexpression of alfalfa SIMK promotes root hair growth, nodule clustering and shoot biomass production

  2020cites this paper
• Role of fixing nitrogen in common bean growth under water deficit conditions

  2020cites this paper
• Hormone‐induced nodule‐like structures in land plants: an update

  2020cites this paper
• Optimizing Rhizobium-legume symbioses by simultaneous measurement of rhizobial competitiveness and N2 fixation in nodules

  2020cites this paper
• Multilegume biofertilizer: a dream

  2020cites this paper
• The invisible life inside plants: Deciphering the riddles of endophytic bacterial diversity.

  2020cites this paper
• MicroRNAs as Fine-Tuners of Gene Regulation in Plant–Microbe Interactions

  2020cites this paper
• NEGATIVE HORMONAL REGULATION OF SYMBIOTIC NODULE DEVELOPMENT.

  2020cites this paper
• Microbial Diversity in Soil: Biological Tools for Abiotic Stress Management in Plants

  2019cites this paper
• RNA-seq reveals differentially expressed genes in rice (Oryza sativa) roots during interactions with plant-growth promoting bacteria, Azospirillum brasilense

  2019cites this paper
• Computational mapping of the differentially expressed gene-lncRNA pairs present at the root nodule developmental stages of Arachis hypogaea

  2019cites this paper
• Mediterranean Native Leguminous Plants: A Reservoir of Endophytic Bacteria with Potential to Enhance Chickpea Growth under Stress Conditions

  2019cites this paper
• A Roadmap toward Engineered Nitrogen-Fixing Nodule Symbiosis

  2019cites this paper
• NEGATIVE HORMONAL REGULATION OF SYMBIOTIC NODULE DEVELOPMENT. II. SALICILIC, JASMONIC AND ABSCISIC ACIDS (review)

  2018cites this paper
• Jasmonic acid regulation of the anti‐herbivory mechanism conferred by fungal endophytes in grasses

  2018cites this paper
• The plant hormone salicylic acid interacts with the mechanism of anti-herbivory conferred by fungal endophytes in grasses.

  2018influential citation
• Seed and Foliar Application of Amino Acids Improve Variables of Nitrogen Metabolism and Productivity in Soybean Crop

  2018cites this paper
• A convenient, soil-free method for the production of root nodules in soybean to study the effects of exogenous additives Author Names: Swarup

  2018cites this paper
• Down-regulation of PvTRX1h increases nodule number and affects auxin, starch, and metabolic fingerprints in the common bean (Phaseolus vulgaris L.).

  2018cites this paper
• A convenient, soil‐free method for the production of root nodules in soybean to study the effects of exogenous additives

  2018cites this paper
• Comparative transcriptome analysis provides key insights into gene expression pattern during the formation of nodule-like structures in Brachypodium

  2018cites this paper
• Use of CRISPR/Cas9 for Symbiotic Nitrogen Fixation Research in Legumes.

  2017cites this paper
• Transcriptional analysis of genes involved in competitive nodulation in Bradyrhizobium diazoefficiens at the presence of soybean root exudates

  2017cites this paper
• Role of Plant Hormones and Small Signalling Molecules in Nodulation Under P Stress

  2017cites this paper
• MAP Kinase-Mediated Negative Regulation of Symbiotic Nodule Formation in Medicago truncatula

  2017cites this paper
• Comparative transcriptome analysis of nodules of two Mesorhizobium–chickpea associations with differential symbiotic efficiency under phosphate deficiency

  2017cites this paper
• Interplay of Pathogen-Induced Defense Responses and Symbiotic Establishment in Medicago truncatula

  2017cites this paper
• Dissecting hormonal pathways in nitrogen-fixing rhizobium symbioses

  2017cites this paper
• Plant Flavonoids: Key Players in Signaling, Establishment, and Regulation of Rhizobial and Mycorrhizal Endosymbioses

  2017cites this paper
• N-fixation in legumes--An assessment of the potential threat posed by ozone pollution.

  2016cites this paper
• Rhizobial gibberellin negatively regulates host nodule number

  2016cites this paper
• Effector-Triggered Immunity Determines Host Genotype-Specific Incompatibility in Legume-Rhizobium Symbiosis.

  2016cites this paper
• A Developmental and Molecular View of Formation of Auxin-Induced Nodule-Like Structures in Land Plants

  2016influential citation
• LSK1, μια SHAGGY-like kinase με ρόλο στη φυματιογένεση του φυτού Lotus japonicus

  2016influential citation
• Nodulation gene networks in legumes

  2015cites this paper
• Transcriptomic Characterization of Soybean Roots in Response to Bradyrhizobium Infection by RNA Sequencing

  2015cites this paper
• Rapid Identification of Nodule Bacteria with MALDI‐TOF Mass Spectrometry

  2015cites this paper
• Legume-rhizobia signal exchange: promiscuity and environmental effects

  2015cites this paper
• From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula.

  2015cites this paper
• From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula.

  2015cites this paper
• Molecular and cell symbiotic mechanisms

  2015cites this paper
• The potential roles of strigolactones and brassinosteroids in the autoregulation of nodulation pathway.

  2014cites this paper
• The soybean (Glycine max) nodulation-suppressive CLE peptide, GmRIC1, functions interspecifically in common white bean (Phaseolus vulgaris), but not in a supernodulating line mutated in the receptor PvNARK.

  2014cites this paper
• Common and divergent roles of plant hormones in nodulation and arbuscular mycorrhizal symbioses

  2014cites this paper
• Regulatory control of the symbiotic enhanced soybean bHLH transcription factor, GmSAT1.

  2014cites this paper
• Comparative genomics of Bradyrhizobium japonicum CPAC 15 and Bradyrhizobium diazoefficiens CPAC 7: elite model strains for understanding symbiotic performance with soybean

  2014cites this paper
• Mechanistic action of gibberellins in legume nodulation.

  2014cites this paper
• Nod factor perception protein carries weight in biotic interactions.

  2013cites this paper
• Establishing a Symbiotic Relationship Between Legume Plants and Rhizobial Bacteria

  2013cites this paper
• Two-way plant mediated interactions between root-associated microbes and insects: from ecology to mechanisms

  2013cites this paper
• Different interaction among Glomus and Rhizobium species on Phaseolus vulgaris and Zea mays plant growth, physiology and symbiotic development under moderate drought stress conditions

  2013cites this paper
• Two-way plant mediated interactions between root-associated microbes and insects: from ecology to mechanisms

  2013cites this paper
• Biosystems Diversity

  year unknowncites this paper
• Regulatory Mechanisms in Biosystems

  year unknowncites this paper