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The Rules Of Engagement In The Legume-rhizobial Symbiosis.

G. Oldroyd, J. Murray, P. Poole, J. Downie
Published 2011 · Biology, Medicine

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Rhizobial bacteria enter a symbiotic association with leguminous plants, resulting in differentiated bacteria enclosed in intracellular compartments called symbiosomes within nodules on the root. The nodules and associated symbiosomes are structured for efficient nitrogen fixation. Although the interaction is beneficial to both partners, it comes with rigid rules that are strictly enforced by the plant. Entry into root cells requires appropriate recognition of the rhizobial Nod factor signaling molecule, and this recognition activates a series of events, including polarized root-hair tip growth, invagination associated with bacterial infection, and the promotion of cell division in the cortex leading to the nodule meristem. The plant's command of the infection process has been highlighted by its enforcement of terminal differentiation upon the bacteria within nodules of some legumes, and this can result in a loss of bacterial viability while permitting effective nitrogen fixation. Here, we review the mechanisms by which the plant allows bacterial infection and promotes the formation of the nodule, as well as the details of how this intimate association plays out inside the cells of the nodule where a complex interchange of metabolites and regulatory peptides force the bacteria into a nitrogen-fixing organelle-like state.
This paper references
10.1093/JXB/10.2.250
Some Observations on Root-hair Infection by Nodule Bacteria
P. S. Nutman (1959)
10.1128/AEM.50.3.717-720.1985
Rhizobium sp. Degradation of Legume Root Hair Cell Wall at the Site of Infection Thread Origin.
R. Ridge (1985)
10.1073/PNAS.86.4.1244
Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors.
A. Hirsch (1989)
10.1038/351670A0
Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa
G. Truchet (1991)
10.1126/science.257.5066.70
Induction of Pre-Infection Thread Structures in the Leguminous Host Plant by Mitogenic Lipo-Oligosaccharides of Rhizobium
A. V. van Brussel (1992)
10.1101/GAD.7.8.1485
A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development.
J. Glazebrook (1993)
10.1007/978-94-011-0177-6_16
Effects of Nod Factors on Alfalfa Root Hair Ca ++ and H + Currents and on Cytoskeletal Behavior
N. S. Allen (1994)
10.1105/tpc.6.2.215
Morphogenetic Rescue of Rhizobium meliloti Nodulation Mutants by trans-Zeatin Secretion.
J. Cooper (1994)
10.1016/S0092-8674(00)81234-9
Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals
D. Ehrhardt (1996)
10.1046/j.1365-2958.1996.00078.x
The general l‐amino acid permease of Rhizobium leguminosarum is an ABC uptake system that also influences efflux of solutes
D. Walshaw (1996)
10.1006/DBIO.1996.0060
Tip-localized calcium entry fluctuates during pollen tube growth.
E. Pierson (1996)
10.1007/s004250050219
Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity
T. Bibikova (1997)
10.1126/SCIENCE.275.5299.527
A Legume Ethylene-Insensitive Mutant Hyperinfected by Its Rhizobial Symbiont
R. Penmetsa (1997)
10.1111/J.1574-6976.1997.TB00342.X
Nodulation of groundnut by Bradyrhizobium: a simple infection process by crack entry
F. Boogerd (1997)
10.1073/PNAS.95.16.9687
MsPG3, a Medicago sativa polygalacturonase gene expressed during the alfalfa-Rhizobium meliloti interaction.
J. Muñoz (1998)
10.1104/PP.116.3.871
Rearrangement of actin microfilaments in plant root hairs responding to rhizobium etli nodulation signals
Crdenas (1998)
10.1046/J.1365-313X.1998.00090.X
Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides.
U. Mathesius (1998)
10.1046/J.1365-313X.1999.00415.X
Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana.
T. Bibikova (1999)
10.1038/46058
A plant regulator controlling development of symbiotic root nodules
L. Schauser (1999)
Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements.
A. Timmers (1999)
10.1094/MPMI.1999.12.9.829
Rhizobium Nod Factors Induce an Increase in Sub-apical Fine Bundles of Actin Filaments in Vicia sativa Root Hairs within Minutes
N. Ruijter (1999)
10.1007/s004380000330
Analysis of ENOD40 expression in alb1, a symbiotic mutant of Lotus japonicus that forms empty nodules with incompletely developed nodule vascular bundles
H. Imaizumi-Anraku (2000)
10.1104/PP.010295
Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots.
K. Vissenberg (2001)
10.1094/MPMI.2002.15.2.164
Patterns of pectin methylesterase transcripts in developing stem nodules of Sesbania rostrata.
S. Lievens (2002)
10.1038/nature00842
A receptor kinase gene regulating symbiotic nodule development
G. Endré (2002)
10.1128/MMBR.66.2.203-222.2002
Key Role of Bacterial NH4+ Metabolism in Rhizobium-Plant Symbiosis
E. Patriarca (2002)
10.1038/nature00841
A plant receptor-like kinase required for both bacterial and fungal symbiosis
S. Stracke (2002)
10.1074/jbc.M106754200
GmZIP1 Encodes a Symbiosis-specific Zinc Transporter in Soybean*
S. Moreau (2002)
10.1128/JB.184.15.4071-4080.2002
Rhizobium leguminosarum Has a Second General Amino Acid Permease with Unusually Broad Substrate Specificity and High Similarity to Branched-Chain Amino Acid Transporters (Bra/LIV) of the ABC Family
A. Hosie (2002)
10.1104/pp.005777
ACTIN2 Is Essential for Bulge Site Selection and Tip Growth during Root Hair Development of Arabidopsis1
C. Ringli (2002)
10.1094/MPMI.2002.15.6.522
Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula.
S. Ramu (2002)
10.1046/j.1365-2958.2002.02826.x
The Sinorhizobium meliloti stringent response affects multiple aspects of symbiosis
D. Wells (2002)
10.1247/CSF.27.1
Vinexin, CAP/ponsin, ArgBP2: a novel adaptor protein family regulating cytoskeletal organization and signal transduction.
N. Kioka (2002)
10.1105/TPC.005892
Positioning of Nuclei in Arabidopsis Root Hairs
T. Ketelaar (2002)
10.1104/pp.102.010710
Identification and Characterization of Nodulation-Signaling Pathway 2, a Gene of Medicago truncatula Involved in Nod Factor Signaling1
G. Oldroyd (2003)
10.1104/pp.102.017020
crinkle, a Novel Symbiotic Mutant That Affects the Infection Thread Growth and Alters the Root Hair, Trichome, and Seed Development in Lotus japonicus 1
M. Tansengco (2003)
10.1007/s00425-003-1097-1
The distributional changes and role of microtubules in Nod factor-challenged Medicago sativa root hairs
Ravisha R Weerasinghe (2003)
10.1105/tpc.014373
Endoreduplication Mediated by the Anaphase-Promoting Complex Activator CCS52A Is Required for Symbiotic Cell Differentiation in Medicago truncatula Nodules Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014373.
J. Vinardell (2003)
10.1094/MPMI.2003.16.3.217
Expression of the bacterial catalase genes during Sinorhizobium meliloti-Medicago sativa symbiosis and their crucial role during the infection process.
A. Jamet (2003)
10.1046/J.1365-313X.2003.01802.X
The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport.
B. Kaiser (2003)
10.1073/pnas.1333899100
Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume
W. D'Haeze (2003)
10.1038/nature01527
Amino-acid cycling drives nitrogen fixation in the legume–Rhizobium symbiosis
E. Lodwig (2003)
10.1104/pp.103.021634
Nod Factor-Induced Root Hair Curling: Continuous Polar Growth towards the Point of Nod Factor Application1
J. Esseling (2003)
10.1038/nature02045
A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals
E. Madsen (2003)
10.1104/pp.102.018192
A Novel Family in Medicago truncatula Consisting of More Than 300 Nodule-Specific Genes Coding for Small, Secreted Polypeptides with Conserved Cysteine Motifs1,212
P. Mergaert (2003)
10.1038/nature02039
Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases
S. Radutoiu (2003)
10.1093/JXB/ERG004
Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes.
T. Holdaway-Clarke (2003)
10.1126/SCIENCE.1090074
LysM Domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection
E. Limpens (2003)
10.1128/JB.185.18.5602-5610.2003
Mutations in rpoBC Suppress the Defects of a Sinorhizobium meliloti relA Mutant
D. Wells (2003)
10.1111/J.1469-8137.2004.01121.X
An unusual infection mechanism and nodule morphogenesis in white lupin (Lupinus albus).
Alfonso González-Sama (2004)
10.1126/SCIENCE.1093038
A Putative Ca2+ and Calmodulin-Dependent Protein Kinase Required for Bacterial and Fungal Symbioses
J. Levy (2004)
10.1093/PCP/PCH076
Pollen development and tube growth are affected in the symbiotic mutant of Lotus japonicus, crinkle.
M. Tansengco (2004)
10.1038/nrm1424
Calcium, kinases and nodulation signalling in legumes
G. Oldroyd (2004)
10.1128/MMBR.68.2.280-300.2004
Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes
D. Gage (2004)
10.1111/J.1365-313X.2004.02038.X
Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses.
D. Lohar (2004)
10.1104/pp.104.049064
nip, a Symbiotic Medicago truncatula Mutant That Forms Root Nodules with Aberrant Infection Threads and Plant Defense-Like Response1
Harita Veereshlingam (2004)
10.1007/BF00395142
Ultrastructure of infection-thread development during the infection of soybean by Rhizobium japonicum
B. Turgeon (2004)
10.1094/MPMI.2004.17.3.292
Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions.
A. Becker (2004)
10.1073/PNAS.0400595101
A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning.
R. Mitra (2004)
10.1073/PNAS.0407269101
A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote-host interaction.
M. Barnett (2004)
10.1126/SCIENCE.1092986
Medicago truncatula DMI1 Required for Bacterial and Fungal Symbioses in Legumes
J. Ané (2004)
10.1016/J.TPLANTS.2004.09.005
Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes.
S. Goormachtig (2004)
10.1073/PNAS.0307137101
Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids.
G. Ferguson (2004)
10.1111/J.1365-313X.2004.02155.X
From pollen tubes to infection threads: recruitment of Medicago floral pectic genes for symbiosis.
I. Rodríguez-Llorente (2004)
10.1080/07352680490480734
Plant Cell Wall Remodelling in the Rhizobium–Legume Symbiosis
N. Brewin (2004)
10.1104/pp.104.056630
Characterization of the Lotus japonicus Symbiotic Mutant lot1 That Shows a Reduced Nodule Number and Distorted Trichomes1
Y. Ooki (2005)
10.1038/nature03237
Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots
H. Imaizumi-Anraku (2005)
10.1111/J.1365-313X.2005.02522.X
Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway.
B. Oláh (2005)
10.1094/MPMI-18-1195
Nod factors alter the microtubule cytoskeleton in Medicago truncatula root hairs to allow root hair reorientation.
B. Sieberer (2005)
10.1016/J.PBI.2005.05.013
Nod factor signaling genes and their function in the early stages of Rhizobium infection.
R. Geurts (2005)
10.1073/PNAS.0407926102
Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus.
Ravisha R Weerasinghe (2005)
10.1105/tpc.105.031641
Microtubule Dynamics in Living Root Hairs: Transient Slowing by Lipochitin Oligosaccharide Nodulation Signalsw⃞
Valya N Vassileva (2005)
10.1126/SCIENCE.1111025
NSP1 of the GRAS Protein Family Is Essential for Rhizobial Nod Factor-Induced Transcription
P. Smit (2005)
10.1146/ANNUREV.CELLBIO.21.122303.114901
Spatial control of cell expansion by the plant cytoskeleton.
Laurie G Smith (2005)
10.1105/tpc.104.030106
The Sulfate Transporter SST1 Is Crucial for Symbiotic Nitrogen Fixation in Lotus japonicus Root Nodules
Lene Krusell (2005)
10.1094/MPMI-18-0533
Role of cellulose fibrils and exopolysaccharides of Rhizobium leguminosarum in attachment to and infection of Vicia sativa root hairs.
M. Laus (2005)
10.1104/pp.105.070326
Transcript Analysis of Early Nodulation Events in Medicago truncatula12[W]
D. Lohar (2005)
10.1094/MPMI-18-0067
Role of polyhydroxybutyrate and glycogen as carbon storage compounds in pea and bean bacteroids.
E. Lodwig (2005)
10.1104/pp.104.057513
Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti Involves the Nodulation Factor-Dependent Induction of Root Hairs1[w]
Bogumil Karas (2005)
10.1126/SCIENCE.1110951
Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators
P. Kaló (2005)
10.1128/JB.187.15.5460-5469.2005
Effective Symbiosis between Rhizobium etli and Phaseolus vulgaris Requires the Alarmone ppGpp
M. Moris (2005)
10.1016/j.conb.2005.05.006
Presynaptic calcium and control of vesicle fusion
R. Schneggenburger (2005)
10.1104/pp.106.089508
Lotus japonicus Nodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume1[C][W]
A. Heckmann (2006)
10.1073/PNAS.0600912103
Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis.
P. Mergaert (2006)
10.1094/MPMI-19-1444
Identification of symbiotically defective mutants of Lotus japonicus affected in infection thread growth.
Fabien Lombardo (2006)
10.1093/PCP/PCL022
LjnsRING, a novel RING finger protein, is required for symbiotic interactions between Mesorhizobium loti and Lotus japonicus.
K. Shimomura (2006)
10.1105/tpc.106.043778
The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti[W]
S. Gonzalez-Rizzo (2006)
10.1038/nature04862
Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development
L. Tirichine (2006)
10.1128/JB.188.8.3143-3148.2006
BacA-Mediated Bleomycin Sensitivity in Sinorhizobium meliloti Is Independent of the Unusual Lipid A Modification
G. Ferguson (2006)
10.1016/S0074-7696(06)52004-2
Organization and function of the actin cytoskeleton in developing root cells.
E. Blancaflor (2006)
10.1104/pp.105.075879
Defective Long-Distance Auxin Transport Regulation in the Medicago truncatula super numeric nodules Mutant1[W]
Giel E. van Noorden (2006)
10.1073/PNAS.0508883103
A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis.
N. Kanamori (2006)
10.1094/MPMI-19-0363
Sinorhizobium meliloti differentiation during symbiosis with alfalfa: a transcriptomic dissection.
D. Capela (2006)
10.1016/J.TPLANTS.2006.10.002
Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes.
Jozef Šamaj (2006)
10.1104/pp.106.080168
Imaging of Dynamic Secretory Vesicles in Living Pollen Tubes of Picea meyeri Using Evanescent Wave Microscopy1[W]
X. Wang (2006)
10.1101/GAD.402806
MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula.
J. Combier (2006)
10.1094/MPMI-19-0801
New nodulation mutants responsible for infection thread development in Lotus japonicus.
K. Yano (2006)
10.1094/MPMI-19-0914
Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus.
H. Miwa (2006)
10.1038/nature04812
Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition
C. Gleason (2006)
10.1104/pp.107.098764
A Symbiotic Plant Peroxidase Involved in Bacterial Invasion of the Tropical Legume Sesbania rostrata1[C][W][OA]
Jeroen Den Herder (2007)
10.1105/tpc.107.055863
Cytokinins Act Directly on Lateral Root Founder Cells to Inhibit Root Initiation[W]
L. Laplaze (2007)
10.1038/ncb1657
Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts
N. Balasubramanian (2007)
10.1111/J.1469-8137.2007.02042.X
Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth.
Martin Potocký (2007)
10.1126/SCIENCE.1132514
A Cytokinin Perception Mutant Colonized by Rhizobium in the Absence of Nodule Organogenesis
J. Murray (2007)
10.1104/pp.106.093021
Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase1
J. F. Marsh (2007)
10.1105/tpc.106.048264
An ERF Transcription Factor in Medicago truncatula That Is Essential for Nod Factor Signal Transduction[W]
P. H. Middleton (2007)
10.1094/MPMI-20-9-1138
Genomic organization and evolutionary insights on GRP and NCR genes, two large nodule-specific gene families in Medicago truncatula.
Benoit Alunni (2007)
10.1094/MPMI-20-10-1298
An oligonucleotide microarray resource for transcriptional profiling of Bradyrhizobium japonicum.
W. Chang (2007)
10.1104/pp.107.100495
Medicago LYK3, an Entry Receptor in Rhizobial Nodulation Factor Signaling1[W]
P. Smit (2007)
10.1105/tpc.107.052944
AP2-ERF Transcription Factors Mediate Nod Factor–Dependent Mt ENOD11 Activation in Root Hairs via a Novel cis-Regulatory Motif[W]
Andry Andriankaja (2007)
10.1105/tpc.106.046938
NUCLEOPORIN85 Is Required for Calcium Spiking, Fungal and Bacterial Symbioses, and Seed Production in Lotus japonicus
Katsuharu Saito (2007)
10.1104/pp.106.092585
The MtMMPL1 Early Nodulin Is a Novel Member of the Matrix Metalloendoproteinase Family with a Role in Medicago truncatula Infection by Sinorhizobium meliloti1[W][OA]
J. Combier (2007)
10.1094/MPMI-20-8-0912
A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula.
E. Messinese (2007)
10.1126/SCIENCE.1132397
A Gain-of-Function Mutation in a Cytokinin Receptor Triggers Spontaneous Root Nodule Organogenesis
Leïla Tirichine (2007)
10.1126/science.1139548
Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia
E. Giraud (2007)
10.1104/pp.108.125674
Mechanism of Infection Thread Elongation in Root Hairs of Medicago truncatula and Dynamic Interplay with Associated Rhizobial Colonization1[W][OA]
J. Fournier (2008)
10.1371/journal.pbio.0060307
Root System Architecture from Coupling Cell Shape to Auxin Transport
M. Laskowski (2008)
10.1105/tpc.108.061739
Abscisic Acid Coordinates Nod Factor and Cytokinin Signaling during the Regulation of Nodulation in Medicago truncatula
Yiliang Ding (2008)
10.1126/science.1164147
A Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem
R. D. Ioio (2008)
10.1073/pnas.0806858105
CYCLOPS, a mediator of symbiotic intracellular accommodation
K. Yano (2008)
10.1016/j.cub.2008.10.063
Plant Pattern-Recognition Receptor FLS2 Is Directed for Degradation by the Bacterial Ubiquitin Ligase AvrPtoB
Vera Göhre (2008)
10.1105/tpc.108.063255
Lotus japonicus CASTOR and POLLUX Are Ion Channels Essential for Perinuclear Calcium Spiking in Legume Root Endosymbiosis[W]
M. Charpentier (2008)
10.1105/tpc.108.059857
EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation in Medicago truncatula[W]
T. Vernié (2008)
10.1094/MPMI-21-5-0535
api, A novel Medicago truncatula symbiotic mutant impaired in nodule primordium invasion.
Alice Teillet (2008)
10.1111/j.1365-2818.2008.02040.x
The role of the plant cytoskeleton in the interaction between legumes and rhizobia
A. Timmers (2008)
10.1146/annurev.genet.42.110807.091427
Molecular determinants of a symbiotic chronic infection.
K. E. Gibson (2008)
10.1073/pnas.0710273105
The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection
J. Arrighi (2008)
10.1111/j.1365-313X.2008.03448.x
MicroRNA166 controls root and nodule development in Medicago truncatula.
A. Boualem (2008)
10.1016/j.ejcb.2008.07.001
Reggies/flotillins regulate cytoskeletal remodeling during neuronal differentiation via CAP/ponsin and Rho GTPases.
M. Langhorst (2008)
10.1073/pnas.0808048105
A mutant GlnD nitrogen sensor protein leads to a nitrogen-fixing but ineffective Sinorhizobium meliloti symbiosis with alfalfa
S. Yurgel (2008)
10.1016/j.tplants.2008.01.003
Cytokinin: secret agent of symbiosis.
F. Frugier (2008)
10.1038/nature06943
Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis
B. Müller (2008)
10.1111/j.1365-313X.2008.03531.x
The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations.
R. Penmetsa (2008)
10.1104/pp.108.118141
A Positive Regulatory Role for LjERF1 in the Nodulation Process Is Revealed by Systematic Analysis of Nodule-Associated Transcription Factors of Lotus japonicus1[W]
E. Asamizu (2008)
10.1038/nrmicro1987
Arbuscular mycorrhiza: the mother of plant root endosymbioses
M. Parniske (2008)
10.1186/1471-2164-9-271
The genome of the versatile nitrogen fixer Azorhizobium caulinodans ORS571
Kyung-Bum Lee (2008)
10.1073/pnas.0802547105
Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots
M. Robledo (2008)
10.1126/scisignal.149re11
De Novo Organ Formation from Differentiated Cells: Root Nodule Organogenesis
M. Crespi (2008)
10.1146/annurev.arplant.59.032607.092839
Coordinating nodule morphogenesis with rhizobial infection in legumes.
G. E. Oldroyd (2008)
10.1016/j.tplants.2009.06.010
Cytokinin-auxin crosstalk.
Laila Moubayidin (2009)
10.1104/pp.109.143024
Knockdown of CELL DIVISION CYCLE16 Reveals an Inverse Relationship between Lateral Root and Nodule Numbers and a Link to Auxin in Medicago truncatula1[W][OA]
Kavitha T. Kuppusamy (2009)
10.1104/pp.109.143933
LIN, a Novel Type of U-Box/WD40 Protein, Controls Early Infection by Rhizobia in Legumes1[C][W][OA]
E. Kiss (2009)
10.1007/s00497-009-0118-z
The regulation of vesicle trafficking by small GTPases and phospholipids during pollen tube growth
Y. Zhang (2009)
10.1073/pnas.0811539106
Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux
M. Pernisová (2009)
10.1104/pp.108.135160
The Temperature-Sensitive brush Mutant of the Legume Lotus japonicus Reveals a Link between Root Development and Nodule Infection by Rhizobia[C][W][OA]
Makoto Maekawa-Yoshikawa (2009)
10.1016/j.pbi.2009.09.010
Actin and microtubule cytoskeleton interactions.
J. Petrášek (2009)
10.1073/pnas.0910081107
Plant flotillins are required for infection by nitrogen-fixing bacteria
C. H. Haney (2009)
10.1128/JB.00165-09
Transcriptomic Analysis of Rhizobium leguminosarum Biovar viciae in Symbiosis with Host Plants Pisum sativum and Vicia cracca
R. Karunakaran (2009)
10.1105/tpc.108.064279
Remorin, a Solanaceae Protein Resident in Membrane Rafts and Plasmodesmata, Impairs Potato virus X Movement[W]
S. Raffaele (2009)
10.1016/j.tplants.2009.05.002
Arabidopsis lateral root development: an emerging story.
B. Péret (2009)
10.1038/nature08594
Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation
T. Hakoyama (2009)
10.1105/tpc.108.063693
Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti[C][W]
Keisuke Yokota (2009)
10.1111/j.1365-313X.2009.03943.x
CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis.
K. Yano (2009)
10.1128/JB.00926-08
Characterization of a γ-Aminobutyric Acid Transport System of Rhizobium leguminosarum bv. viciae 3841
J. P. White (2009)
10.1073/pnas.0903653106
Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids
J. Prell (2009)
10.1016/j.cub.2009.01.054
AvrPtoB Targets the LysM Receptor Kinase CERK1 to Promote Bacterial Virulence on Plants
Selena Giménez-Ibañez (2009)
10.1105/tpc.109.069617
Manipulation of Auxin Transport in Plant Roots during Rhizobium Symbiosis and Nematode Parasitism
W. Grunewald (2009)
10.1128/JB.01661-08
Essential Role for the BacA Protein in the Uptake of a Truncated Eukaryotic Peptide in Sinorhizobium meliloti
Victoria L. Marlow (2009)
10.1111/j.1365-313X.2009.04072.x
Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis.
N. Pumplin (2010)
10.1111/j.1365-313X.2010.04228.x
A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts
T. Hayashi (2010)
10.1016/j.pbi.2010.08.006
Cytokinin signaling and transcriptional networks.
Cristiana T Argueso (2010)
10.1128/JB.00020-10
BacA Is Essential for Bacteroid Development in Nodules of Galegoid, but not Phaseoloid, Legumes
R. Karunakaran (2010)
10.1094/MPMI-06-10-0144
Conservation in function of a SCAR/WAVE component during infection thread and root hair growth in Medicago truncatula.
A. Miyahara (2010)
10.1126/science.1184057
Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis
W. Van de Velde (2010)
10.1126/science.1191937
Oscillating Gene Expression Determines Competence for Periodic Arabidopsis Root Branching
M. A. Moreno-Risueno (2010)
10.1105/tpc.109.069807
NENA, a Lotus japonicus Homolog of Sec13, Is Required for Rhizodermal Infection by Arbuscular Mycorrhiza Fungi and Rhizobia but Dispensable for Cortical Endosymbiotic Development[C][W]
M. Groth (2010)
10.1016/j.pbi.2010.09.006
Lateral root organogenesis - from cell to organ.
E. Benková (2010)
10.1111/j.1365-313X.2010.04134.x
A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula.
Craig R. Yendrek (2010)
10.1111/j.1399-3054.2009.01313.x
ROS in plant development.
S. Swanson (2010)
10.1105/tpc.110.075861
The Medicago truncatula E3 Ubiquitin Ligase PUB1 Interacts with the LYK3 Symbiotic Receptor and Negatively Regulates Infection and Nodulation[W][OA]
Malick Mbengue (2010)
10.1186/gb-2011-12-2-r17
Stress response regulators identified through genome-wide transcriptome analysis of the (p)ppGpp-dependent response in Rhizobium etli
M. Vercruysse (2010)
10.1073/pnas.0913320107
A remorin protein interacts with symbiotic receptors and regulates bacterial infection
B. Lefebvre (2010)
10.1111/j.1469-8137.2010.03261.x
Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation.
Ryoko Oono (2010)
10.1038/ncomms1009
The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus
L. Madsen (2010)
10.1126/science.1184096
A Nodule-Specific Protein Secretory Pathway Required for Nitrogen-Fixing Symbiosis
Dong Wang (2010)
10.1111/j.1365-313X.2010.04447.x
MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula.
Julien R. H. Plet (2011)
10.1111/j.1365-313X.2010.04415.x
Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula.
Jeremy D Murray (2011)
10.1016/j.pbi.2010.08.001
Plant stem cell niches: from signalling to execution.
R. Sablowski (2011)
10.1094/MPMI-01-11-0004
Natural variation in host-specific nodulation of pea is associated with a haplotype of the SYM37 LysM-type receptor-like kinase.
Ronghui Li (2011)
10.1128/JB.01260-10
Role of BacA in Lipopolysaccharide Synthesis, Peptide Transport, and Nodulation by Rhizobium sp. Strain NGR234
S. Ardissone (2011)
10.1038/nature09622
Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza
F. Maillet (2011)
10.1016/j.mib.2010.12.002
Innate immunity effectors and virulence factors in symbiosis.
A. Kereszt (2011)
10.1111/j.1365-2958.2011.07565.x
Mutation of GOGAT prevents pea bacteroid formation and N2 fixation by globally downregulating transport of organic nitrogen sources
G. Mulley (2011)



This paper is referenced by
10.1016/J.CJ.2021.03.019
GmNMHC5 may promote nodulation via interaction with GmGAI in soybean
Wenting Wang (2021)
10.1007/s00122-021-03791-5
Nitrogen fixation in maize: breeding opportunities.
Seema Sheoran (2021)
10.3389/fpls.2021.699590
Differential Expression of Paraburkholderia phymatum Type VI Secretion Systems (T6SS) Suggests a Role of T6SS-b in Early Symbiotic Interaction
S. Hug (2021)
10.3389/fpls.2021.683601
Nitrogen and Phosphorus Signaling and Transport During Legume–Rhizobium Symbiosis
Yanlin Ma (2021)
10.1093/jxb/erab008
Molecular responses of legumes to abiotic stress: post-translational modifications of proteins and redox signaling
M. Matamoros (2021)
10.1007/s11427-021-1925-1
Exploring marine endosymbiosis systems with omics techniques.
Yisi Hu (2021)
10.3389/fagro.2021.654576
Why Should Nodule Cysteine-Rich (NCR) Peptides Be Absent From Nodules of Some Groups of Legumes but Essential for Symbiotic N-Fixation in Others?
J. Downie (2021)
10.1007/978-3-030-61153-8_19
Rhizobia: A Potent Tool for Amelioration of Drought Stress in Legumes
Pratibha Singh (2021)
10.1007/978-981-15-9758-9_11
Understanding Rhizosphere Through Metatranscriptomic Approaches
R. Thakur (2021)
10.3389/fpls.2021.690567
Competition, Nodule Occupancy, and Persistence of Inoculant Strains: Key Factors in the Rhizobium-Legume Symbioses
Marcela Mendoza-Suárez (2021)
10.1088/1755-1315/788/1/012055
Macronutrient management for the cultivation of Soybean (Glycine max L.): A review
P. Saranraj (2021)
10.1038/s41598-021-81598-6
Rhizobia use a pathogenic-like effector to hijack leguminous nodulation signalling
S. T. N. Ratu (2021)
10.1111/jipb.13148
Phosphorylation of MtRopGEF2 by LYK3 mediates MtROP activity to regulate rhizobial infection in Medicago truncatula.
Mingxing Wang (2021)
10.1007/978-981-15-7142-8_8
Applications of CRISPR/Cas Beyond Simple Traits in Crops
S. Khan (2021)
10.3389/fpls.2021.659061
Auxin Response Factor 2 (ARF2), ARF3, and ARF4 Mediate Both Lateral Root and Nitrogen Fixing Nodule Development in Medicago truncatula
Cristina Kirolinko (2021)
10.1128/AEM.03004-20
Sinorhizobium medicae WSM419 Genes That Improve Symbiosis between Sinorhizobium meliloti Rm1021 and Medicago truncatula Jemalong A17 and in Other Symbiosis Systems
P. Ghosh (2021)
10.3389/fpls.2021.719987
Genetic Variation in Host-Specific Competitiveness of the Symbiont Rhizobium leguminosarum Symbiovar viciae
S. Boivin (2021)
10.1016/B978-0-12-818564-3.00001-9
Setting the context: Agriculture and crop/food sustainability
R. Hull (2021)
10.3390/microorganisms9030575
Transcriptome Signatures in Pseudomonas simiae WCS417 Shed Light on Role of Root-Secreted Coumarins in Arabidopsis-Mutualist Communication
K. Yu (2021)
10.1007/978-3-030-71206-8_2
Ecophysiology of Nitrogen in Symbiotic Relationships of Plants and Microorganisms
Isabelle Faria Matos (2021)
10.1101/2021.02.03.429583
Autoregulation dependent and independent mechanisms are responsible for the systemic control of nodule formation by the plant N demand
M. Pervent (2021)
10.3390/AGRICULTURE11030234
Relationship between Plant Roots, Rhizosphere Microorganisms, and Nitrogen and Its Special Focus on Rice
Qiangqiang Xiong (2021)
10.1007/s00425-020-03538-4
Specific tissue proteins 1 and 6 are involved in root biology during normal development and under symbiotic and pathogenic interactions in Medicago truncatula
L. Albornos (2021)
Tansley insight Theendodermal passage cell – just another brick in the wall ?
Julia Holbein (2021)
10.1093/femsre/fuab022
Microbial driven genetic variation in holobionts.
I. Zilber-Rosenberg (2021)
10.1101/2021.08.10.455861
Asymmetric Redundancy of Soybean Nodule Inception (NIN) Genes in Root Nodule Symbiosis
Mengdi Fu (2021)
10.1016/B978-0-12-821667-5.00005-1
Genomics and functional traits required for the successful use of biofertilizers
A. Novinscak (2021)
10.1101/2021.08.31.458470
Hopanoids confer robustness to physicochemical variability in the niche of the plant symbiont Bradyrhizobium diazoefficiens
E. Tookmanian (2021)
10.1186/s12870-021-03102-6
Chickpea shows genotype-specific nodulation responses across soil nitrogen environment and root disease resistance categories
K. Plett (2021)
10.1111/evo.14164
Decreased coevolutionary potential and increased symbiont fecundity during the biological invasion of a legume‐rhizobium mutualism
C. Wendlandt (2021)
10.1007/978-981-16-0889-6_6
Transcriptomics Analyses and the Relationship Between Plant and Plant Growth-Promoting Rhizobacteria (PGPR)
S. Moradi (2021)
10.1007/S11104-020-04795-8
Phylogenetic diversity of indigenous Rhizobium trapped from the natural habitat of Pisum sativum L. in eastern and central Algeria
Meriem Gaci (2021)
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