Plant Hormones Differentially Control the Sub-Cellular Localization of Plasma Membrane Microdomains during the Early Stage of Soybean Nodulation
Abstract
Phytohormones regulate the mutualistic symbiotic interaction between legumes and rhizobia, nitrogen-fixing soil bacteria, notably by controlling the formation of the infection thread in the root hair (RH). At the cellular level, the formation of the infection thread is promoted by the translocation of plasma membrane microdomains at the tip of the RH. We hypothesize that phytohormones regulate the translocation of plasma membrane microdomains to regulate infection thread formation. Accordingly, we treated with hormone and hormone inhibitors transgenic soybean roots expressing fusions between the Green Fluorescent Protein (GFP) and GmFWL1 or GmFLOT2/4, two microdomain-associated proteins translocated at the tip of the soybean RH in response to rhizobia. Auxin and cytokinin treatments are sufficient to trigger or inhibit the translocation of GmFWL1 and GmFLOT2/4 to the RH tip independently of the presence of rhizobia, respectively. Unexpectedly, the application of salicylic acid, a phytohormone regulating the plant defense system, also promotes the translocation of GmFWL1 and GmFLOT2/4 to the RH tip regardless of the presence of rhizobia. These results suggest that phytohormones are playing a central role in controlling the early stages of rhizobia infection by regulating the translocation of plasma membrane microdomains. They also support the concept of crosstalk of phytohormones tomore »
- Authors:
-
- Univ. of Oklahoma, Norman, OK (United States). Dept. of Microbiology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
- Univ. of Nebraska, Lincoln, NE (United States). Dept. of Agronomy and Horticulture
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1628321
- Grant/Contract Number:
- AC05-00OR22725; NSF IOS 1854326
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genes
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 12; Journal ID: ISSN 2073-4425
- Publisher:
- MDPI
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Genetics & Heredity; root hair; legume; nodulation; plasma membrane microdomains; phytohormones
Citation Formats
Qiao, Zhenzhen, Zogli, Prince, and Libault, Marc. Plant Hormones Differentially Control the Sub-Cellular Localization of Plasma Membrane Microdomains during the Early Stage of Soybean Nodulation. United States: N. p., 2019.
Web. doi:10.3390/genes10121012.
Qiao, Zhenzhen, Zogli, Prince, & Libault, Marc. Plant Hormones Differentially Control the Sub-Cellular Localization of Plasma Membrane Microdomains during the Early Stage of Soybean Nodulation. United States. https://doi.org/10.3390/genes10121012
Qiao, Zhenzhen, Zogli, Prince, and Libault, Marc. Thu .
"Plant Hormones Differentially Control the Sub-Cellular Localization of Plasma Membrane Microdomains during the Early Stage of Soybean Nodulation". United States. https://doi.org/10.3390/genes10121012. https://www.osti.gov/servlets/purl/1628321.
@article{osti_1628321,
title = {Plant Hormones Differentially Control the Sub-Cellular Localization of Plasma Membrane Microdomains during the Early Stage of Soybean Nodulation},
author = {Qiao, Zhenzhen and Zogli, Prince and Libault, Marc},
abstractNote = {Phytohormones regulate the mutualistic symbiotic interaction between legumes and rhizobia, nitrogen-fixing soil bacteria, notably by controlling the formation of the infection thread in the root hair (RH). At the cellular level, the formation of the infection thread is promoted by the translocation of plasma membrane microdomains at the tip of the RH. We hypothesize that phytohormones regulate the translocation of plasma membrane microdomains to regulate infection thread formation. Accordingly, we treated with hormone and hormone inhibitors transgenic soybean roots expressing fusions between the Green Fluorescent Protein (GFP) and GmFWL1 or GmFLOT2/4, two microdomain-associated proteins translocated at the tip of the soybean RH in response to rhizobia. Auxin and cytokinin treatments are sufficient to trigger or inhibit the translocation of GmFWL1 and GmFLOT2/4 to the RH tip independently of the presence of rhizobia, respectively. Unexpectedly, the application of salicylic acid, a phytohormone regulating the plant defense system, also promotes the translocation of GmFWL1 and GmFLOT2/4 to the RH tip regardless of the presence of rhizobia. These results suggest that phytohormones are playing a central role in controlling the early stages of rhizobia infection by regulating the translocation of plasma membrane microdomains. They also support the concept of crosstalk of phytohormones to control nodulation.},
doi = {10.3390/genes10121012},
journal = {Genes},
number = 12,
volume = 10,
place = {United States},
year = {2019},
month = {12}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 1 work
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Mini-Review: Nod Factor Regulation of Phytohormone Signaling and Homeostasis During Rhizobia-Legume Symbiosis
journal, September 2018
- Buhian, William P.; Bensmihen, Sandra
- Frontiers in Plant Science, Vol. 9
Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume-Rhizobium Interactions
journal, March 2018
- Wang, Qi; Liu, Jinge; Zhu, Hongyan
- Frontiers in Plant Science, Vol. 9
Salicylic acid interferes with clathrin-mediated endocytic protein trafficking
journal, April 2013
- Du, Y.; Tejos, R.; Beck, M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 19
Challenges and progress towards understanding the role of effectors in plant–fungal interactions
journal, August 2012
- Rafiqi, Maryam; Ellis, Jeffrey G.; Ludowici, Victoria A.
- Current Opinion in Plant Biology, Vol. 15, Issue 4
Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants
journal, March 2013
- Oldroyd, Giles E. D.
- Nature Reviews Microbiology, Vol. 11, Issue 4
Effects of Endogenous Salicylic Acid on Nodulation in the Model Legumes Lotus japonicus and Medicago truncatula
journal, June 2006
- Stacey, Gary; McAlvin, Crystal Bickley; Kim, Sung-Yong
- Plant Physiology, Vol. 141, Issue 4
Lotus japonicus Clathrin Heavy Chain1 Is Associated with Rho-Like GTPase ROP6 and Involved in Nodule Formation
journal, February 2015
- Wang, Chao; Zhu, Maosheng; Duan, Liujiang
- Plant Physiology, Vol. 167, Issue 4
Silencing the Flavonoid Pathway in Medicago truncatula Inhibits Root Nodule Formation and Prevents Auxin Transport Regulation by Rhizobia
journal, June 2006
- Wasson, Anton P.; Pellerone, Flavia I.; Mathesius, Ulrike
- The Plant Cell, Vol. 18, Issue 7
Auxin transporters and binding proteins at a glance
journal, January 2015
- Grones, P.; Friml, J.
- Journal of Cell Science, Vol. 128, Issue 1
GmYUC2a mediates auxin biosynthesis during root development and nodulation in soybean
journal, April 2019
- Wang, Youning; Yang, Wei; Zuo, Yanyan
- Journal of Experimental Botany, Vol. 70, Issue 12
Expression analysis of DIO2, EYA3, KISS1 and GPR54 genes in year-round estrous and seasonally estrous rams
journal, January 2020
- Xia, Qing; Di, Ran; He, Xiao-Yun
- Archives Animal Breeding, Vol. 63, Issue 2
Synthesis, release, and transmission of alfalfa signals to rhizobial symbionts
journal, April 1994
- Phillips, D. A.; Dakora, F. D.; Sande, E.
- Plant and Soil, Vol. 161, Issue 1
Lipochitin Oligosaccharides from Rhizobium leguminosarum bv. viciae Reduce Auxin Transport Capacity in Vicia sativa subsp. nigra Roots
journal, October 1999
- Boot, Kees J. M.; van Brussel, Anton A. N.; Tak, Teun
- Molecular Plant-Microbe Interactions®, Vol. 12, Issue 10
Transmissible Resistance to Penicillin G, Neomycin, and Chloramphenicol in Rhizobium japonicum
journal, September 1973
- Cole, M. A.; Elkan, G. H.
- Antimicrobial Agents and Chemotherapy, Vol. 4, Issue 3
Nonlegumes Respond to Rhizobial Nod Factors by Suppressing the Innate Immune Response
journal, September 2013
- Liang, Y.; Cao, Y.; Tanaka, K.
- Science, Vol. 341, Issue 6152
The Gm FWL1 ( FW2-2-like ) nodulation gene encodes a plasma membrane microdomain-associated protein: A FW2-2-like protein is located in plasma membrane microdomains
journal, April 2017
- Qiao, Zhenzhen; Brechenmacher, Laurent; Smith, Benjamin
- Plant, Cell & Environment, Vol. 40, Issue 8
Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes
journal, June 2004
- Gage, D. J.
- Microbiology and Molecular Biology Reviews, Vol. 68, Issue 2
Commonalities and differences of T3SSs in rhizobia and plant pathogenic bacteria
journal, March 2014
- Tampakaki, Anastasia P.
- Frontiers in Plant Science, Vol. 5
Phytohormone Regulation of Legume-Rhizobia Interactions
journal, July 2014
- Ferguson, Brett J.; Mathesius, Ulrike
- Journal of Chemical Ecology, Vol. 40, Issue 7
Temporal and Spatial Order of Events During the Induction of Cortical Cell Divisions in White Clover by Rhizobium leguminosarum bv. trifolii Inoculation or Localized Cytokinin Addition
journal, June 2000
- Mathesius, Ulrike; Charon, Celine; Rolfe, Barry G.
- Molecular Plant-Microbe Interactions®, Vol. 13, Issue 6
Remorin, a Solanaceae Protein Resident in Membrane Rafts and Plasmodesmata, Impairs Potato virus X Movement
journal, May 2009
- Raffaele, Sylvain; Bayer, Emmanuelle; Lafarge, David
- The Plant Cell, Vol. 21, Issue 5
Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal
journal, April 1990
- Lerouge, Patrice; Roche, Philippe; Faucher, Catherine
- Nature, Vol. 344, Issue 6268
The PIN-FORMED (PIN) protein family of auxin transporters
journal, January 2009
- Křeček, Pavel; Skůpa, Petr; Libus, Jiří
- Genome Biology, Vol. 10, Issue 12
MicroRNA167-Directed Regulation of the Auxin Response Factors GmARF8a and GmARF8b Is Required for Soybean Nodulation and Lateral Root Development
journal, May 2015
- Wang, Youning; Li, Kexue; Chen, Liang
- Plant Physiology, Vol. 168, Issue 3
Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species
journal, April 2007
- Peleg-Grossman, S.; Volpin, H.; Levine, A.
- Journal of Experimental Botany, Vol. 58, Issue 7
Salicylic Acid Affects Root Meristem Patterning via Auxin Distribution in a Concentration-Dependent Manner
journal, April 2019
- Pasternak, Taras; Groot, Edwin P.; Kazantsev, Fedor V.
- Plant Physiology, Vol. 180, Issue 3
RNAi Phenotypes and the Localization of a Protein::GUS Fusion Imply a Role for Medicago truncatula PIN Genes in Nodulation
journal, June 2006
- Huo, Xiuyan; Schnabel, Elise; Hughes, Kelley
- Journal of Plant Growth Regulation, Vol. 25, Issue 2
Mutational and Transcriptional Analysis of the Type III Secretion System of Bradyrhizobium japonicum
journal, December 2002
- Krause, Andrea; Doerfel, Anke; Göttfert, Michael
- Molecular Plant-Microbe Interactions, Vol. 15, Issue 12
MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula: Hormonal interactions in nodulation
journal, January 2011
- Plet, Julie; Wasson, Anton; Ariel, Federico
- The Plant Journal, Vol. 65, Issue 4
Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors
journal, February 1989
- Hirsch, A. M.; Bhuvaneswari, T. V.; Torrey, J. G.
- Proceedings of the National Academy of Sciences, Vol. 86, Issue 4
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
Endocytosis and its regulation in plants
journal, June 2015
- Fan, Lusheng; Li, Ruili; Pan, Jianwei
- Trends in Plant Science, Vol. 20, Issue 6
Nitrate-induced ethylene biosynthesis and the control of nodulation in alfalfa
journal, January 1998
- Caba, J. M.; Recalde, L.; Ligero, F.
- Plant, Cell and Environment, Vol. 21, Issue 1
Functional Domain Analysis of the Remorin Protein LjSYMREM1 in Lotus japonicus
journal, January 2012
- Tóth, Katalin; Stratil, Thomas F.; Madsen, Esben B.
- PLoS ONE, Vol. 7, Issue 1
Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism
journal, February 2013
- Löfke, Christian; Zwiewka, Marta; Heilmann, Ingo
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 9
Functional domain analysis of the Remorin protein LjSYMREM1 in Lotus japonicus.
text, January 2012
- Tóth, Katalin; Stratil, Thomas F.; Madsen, Esben B.
- Universitätsbibliothek der Ludwig-Maximilians-Universität München
A Cytokinin Perception Mutant Colonized by Rhizobium in the Absence of Nodule Organogenesis
journal, January 2007
- Murray, J. D.; Karas, B. J.; Sato, S.
- Science, Vol. 315, Issue 5808
ABP1 Mediates Auxin Inhibition of Clathrin-Dependent Endocytosis in Arabidopsis
text, January 2010
- Jürgen, Kleine-Vehn,; Elke, Barbez,; Eva, Zažímalová,
- The University of North Carolina at Chapel Hill University Libraries
Quantitative 3D imaging of cell level auxin and cytokinin response ratios in soybean roots and nodules: quantitative imaging of auxin and cytokinin
journal, March 2018
- Fisher, Jon; Gaillard, Paul; Fellbaum, Carl R.
- Plant, Cell & Environment
A Gain-of-Function Mutation in a Cytokinin Receptor Triggers Spontaneous Root Nodule Organogenesis
journal, January 2007
- Tirichine, L.; Sandal, N.; Madsen, L. H.
- Science, Vol. 315, Issue 5808
Cytokinins in Symbiotic Nodulation: When, Where, What For?
journal, September 2017
- Gamas, Pascal; Brault, Mathias; Jardinaud, Marie-Françoise
- Trends in Plant Science, Vol. 22, Issue 9
Control of leghaemoglobin synthesis in snake beans
journal, December 1971
- Broughton, W. J.; Dilworth, M. J.
- Biochemical Journal, Vol. 125, Issue 4
A remorin protein interacts with symbiotic receptors and regulates bacterial infection
journal, January 2010
- Lefebvre, B.; Timmers, T.; Mbengue, M.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
Rhizobial root hair infection requires auxin signaling
journal, June 2015
- Laplaze, Laurent; Lucas, Mikaël; Champion, Antony
- Trends in Plant Science, Vol. 20, Issue 6
Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system
journal, September 2013
- Okazaki, S.; Kaneko, T.; Sato, S.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 42
Cytokinin Controls Polarity of PIN1-Dependent Auxin Transport during Lateral Root Organogenesis
journal, May 2014
- Marhavý, Peter; Duclercq, Jérôme; Weller, Benjamin
- Current Biology, Vol. 24, Issue 9
The roles of flotillin microdomains - endocytosis and beyond
journal, December 2011
- Otto, G. P.; Nichols, B. J.
- Journal of Cell Science, Vol. 124, Issue 23
Cytokinin Induction of Root Nodule Primordia in Lotus japonicus Is Regulated by a Mechanism Operating in the Root Cortex
journal, November 2011
- Heckmann, Anne Birgitte; Sandal, Niels; Bek, Anita Søndergaard
- Molecular Plant-Microbe Interactions®, Vol. 24, Issue 11
PIN-Dependent Auxin Transport: Action, Regulation, and Evolution
journal, January 2015
- Adamowski, Maciek; Friml, Jiří
- The Plant Cell, Vol. 27, Issue 1
Salicylic Acid Inhibits Indeterminate-Type Nodulation But Not Determinate-Type Nodulation
journal, January 2003
- van Spronsen, Paulina C.; Tak, Teun; Rood, Anita M. M.
- Molecular Plant-Microbe Interactions®, Vol. 16, Issue 1
ABP1 Mediates Auxin Inhibition of Clathrin-Dependent Endocytosis in Arabidopsis
journal, October 2010
- Robert, Stéphanie; Kleine-Vehn, Jürgen; Barbez, Elke
- Cell, Vol. 143, Issue 1
A Small-Molecule Screen Identifies l-Kynurenine as a Competitive Inhibitor of TAA1/TAR Activity in Ethylene-Directed Auxin Biosynthesis and Root Growth in Arabidopsis
journal, November 2011
- He, Wenrong; Brumos, Javier; Li, Hongjiang
- The Plant Cell, Vol. 23, Issue 11
The auxin transport inhibitor 2,3,5-triiodobenzoic acid (TIBA) inhibits the stimulation of in vitro lateral root formation and the colonization of the tap-root cortex of Norway spruce (Picea abies) seedlings by the ectomycorrhizal fungus Laccaria bicolor
journal, December 1998
- Karabaghli-Degron, C.; Sotta, B.; Bonnet, M.
- New Phytologist, Vol. 140, Issue 4
The Rules of Engagement in the Legume-Rhizobial Symbiosis
journal, December 2011
- Oldroyd, Giles E. D.; Murray, Jeremy D.; Poole, Philip S.
- Annual Review of Genetics, Vol. 45, Issue 1
Expression Analysis of PIN Genes in Root Tips and Nodules of Lotus japonicus
journal, January 2019
- Sańko-Sawczenko, Izabela; Dmitruk, Dominika; Łotocka, Barbara
- International Journal of Molecular Sciences, Vol. 20, Issue 2
Overlap of Proteome Changes in Medicago truncatula in Response to Auxin and Sinorhizobium meliloti
journal, April 2007
- van Noorden, Giel E.; Kerim, Tursun; Goffard, Nicolas
- Plant Physiology, Vol. 144, Issue 2
Auxin inhibits endocytosis and promotes its own efflux from cells
journal, June 2005
- Paciorek, Tomasz; Zažímalová, Eva; Ruthardt, Nadia
- Nature, Vol. 435, Issue 7046
Rhizobium–legume symbioses: the crucial role of plant immunity
journal, March 2015
- Gourion, Benjamin; Berrabah, Fathi; Ratet, Pascal
- Trends in Plant Science, Vol. 20, Issue 3
Cytokinin Modulates Endocytic Trafficking of PIN1 Auxin Efflux Carrier to Control Plant Organogenesis
journal, October 2011
- Marhavý, Peter; Bielach, Agnieszka; Abas, Lindy
- Developmental Cell, Vol. 21, Issue 4
The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti
journal, October 2006
- Gonzalez-Rizzo, Silvina; Crespi, Martin; Frugier, Florian
- The Plant Cell, Vol. 18, Issue 10
Functional rafts in cell membranes
journal, June 1997
- Simons, Kai; Ikonen, Elina
- Nature, Vol. 387, Issue 6633
Overexpression of miR160 affects root growth and nitrogen-fixing nodule number in Medicago truncatula
journal, January 2013
- Bustos-Sanmamed, Pilar; Mao, Guohong; Deng, Ying
- Functional Plant Biology, Vol. 40, Issue 12
Function of plasma membrane microdomain-associated proteins during legume nodulation
journal, September 2017
- Qiao, Zhenzhen; Libault, Marc
- Plant Signaling & Behavior, Vol. 12, Issue 10
Rhizobial Infection Is Associated with the Development of Peripheral Vasculature in Nodules of Medicago truncatula
journal, March 2013
- Guan, Dian; Stacey, Nicola; Liu, Chengwu
- Plant Physiology, Vol. 162, Issue 1
Pseudonodule Formation by Wild-Type and Symbiotic Mutant Medicago truncatula in Response to Auxin Transport Inhibitors
journal, November 2011
- Rightmyer, Adriana P.; Long, Sharon R.
- Molecular Plant-Microbe Interactions®, Vol. 24, Issue 11
Auxin transport, metabolism, and signalling during nodule initiation: indeterminate and determinate nodules
journal, September 2017
- Kohlen, Wouter; Ng, Jason Liang Pin; Deinum, Eva E.
- Journal of Experimental Botany, Vol. 69, Issue 2
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
Unleashing the potential of the root hair cell as a single plant cell type model in root systems biology
journal, January 2013
- Qiao, Zhenzhen; Libault, Marc
- Frontiers in Plant Science, Vol. 4
Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type
journal, June 2000
- Caba, Juan M.; Centeno, M. Luz; Fernández, Belén
- Planta, Vol. 211, Issue 1
Complete Transcriptome of the Soybean Root Hair Cell, a Single-Cell Model, and Its Alteration in Response to Bradyrhizobium japonicum Infection
journal, November 2009
- Libault, Marc; Farmer, Andrew; Brechenmacher, Laurent
- Plant Physiology, Vol. 152, Issue 2
Symbiotic Rhizobia Bacteria Trigger a Change in Localization and Dynamics of the Medicago truncatula Receptor Kinase LYK3
journal, July 2011
- Haney, Cara H.; Riely, Brendan K.; Tricoli, David M.
- The Plant Cell, Vol. 23, Issue 7
The Root Hair “Infectome” of Medicago truncatula Uncovers Changes in Cell Cycle Genes and Reveals a Requirement for Auxin Signaling in Rhizobial Infection
journal, December 2014
- Breakspear, Andrew; Liu, Chengwu; Roy, Sonali
- The Plant Cell, Vol. 26, Issue 12
A member of the highly conserved FWL (tomato FW2.2-like) gene family is essential for soybean nodule organogenesis: A soybean FWL essential for nodulation
journal, March 2010
- Libault, Marc; Zhang, Xue-Cheng; Govindarajulu, Manjula
- The Plant Journal, Vol. 62, Issue 5
Enhancing Phenotyping and Molecular Analysis of Plant Root System Using Ultrasound Aeroponic Technology
journal, October 2018
- Pingault, Lise; Zogli, Prince; Brooks, Jennifer
- Current Protocols in Plant Biology, Vol. 3, Issue 4
Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response
journal, October 2012
- Suzaki, T.; Yano, K.; Ito, M.
- Development, Vol. 139, Issue 21
Genome-wide analysis and expression profiling of the PIN auxin transporter gene family in soybean (Glycine max)
journal, November 2015
- Wang, Yongqin; Chai, Chenglin; Valliyodan, Babu
- BMC Genomics, Vol. 16, Issue 1
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
Secretion systems and signal exchange between nitrogen-fixing rhizobia and legumes
journal, July 2015
- Nelson, Matthew S.; Sadowsky, Michael J.
- Frontiers in Plant Science, Vol. 6
Symbiotic root infections in Medicago truncatula require remorin-mediated receptor stabilization in membrane nanodomains
journal, April 2018
- Liang, Pengbo; Stratil, Thomas F.; Popp, Claudia
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 20
Modeling a Cortical Auxin Maximum for Nodulation: Different Signatures of Potential Strategies
journal, January 2012
- Deinum, Eva Elisabeth; Geurts, René; Bisseling, Ton
- Frontiers in Plant Science, Vol. 3
Ectopic Expression of miR160 Results in Auxin Hypersensitivity, Cytokinin Hyposensitivity, and Inhibition of Symbiotic Nodule Development in Soybean
journal, June 2013
- Turner, Marie; Nizampatnam, Narasimha Rao; Baron, Mathieu
- Plant Physiology, Vol. 162, Issue 4
Auxin transport during root gravitropism: transporters and techniques
journal, May 2013
- Geisler, M.; Wang, B.; Zhu, J.
- Plant Biology, Vol. 16
Plant flotillins are required for infection by nitrogen-fixing bacteria
journal, December 2009
- Haney, C. H.; Long, S. R.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 1
Epidermal auxin biosynthesis facilitates rhizobial infection in Lotus japonicus
journal, May 2018
- Nadzieja, Marcin; Kelly, Simon; Stougaard, Jens
- The Plant Journal, Vol. 95, Issue 1
microRNA160 dictates stage-specific auxin and cytokinin sensitivities and directs soybean nodule development
journal, October 2015
- Nizampatnam, Narasimha Rao; Schreier, Spencer John; Damodaran, Suresh
- The Plant Journal, Vol. 84, Issue 1