Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

Science 303 (5662): 1361-1364

Copyright © 2004 by the American Association for the Advancement of Science

A Putative Ca2+ and Calmodulin-Dependent Protein Kinase Required for Bacterial and Fungal Symbioses

Julien Lévy,1* Cécile Bres,1* René Geurts,2 Boulos Chalhoub,3 Olga Kulikova,2 Gérard Duc,4 Etienne-Pascal Journet,1 Jean-Michel Ané,1 Emmanuelle Lauber,1 Ton Bisseling,2 Jean Dénarié,1 Charles Rosenberg,1 Frédéric Debellé1{dagger}

Abstract: Legumes can enter into symbiotic relationships with both nitrogen-fixing bacteria (rhizobia) and mycorrhizal fungi. Nodulation by rhizobia results from a signal transduction pathway induced in legume roots by rhizobial Nod factors. DMI3, a Medicago truncatula gene that acts immediately downstream of calcium spiking in this signaling pathway and is required for both nodulation and mycorrhizal infection, has high sequence similarity to genes encoding calcium and calmodulin-dependent protein kinases (CCaMKs). This indicates that calcium spiking is likely an essential component of the signaling cascade leading to nodule development and mycorrhizal infection, and sheds light on the biological role of plant CCaMKs.

1 Laboratoire des Interactions Plantes–Microorganismes INRA-CNRS, BP27, 31326 Castanet-Tolosan Cedex, France.
2 Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, Dreijenlaan 3, 6703HA Wageningen, Netherlands.
3 Unité de Recherches en Génomique Végétale INRA, 2 rue Gaston Crémieux, CP 5708, F-91057 Evry Cedex, France.
4 Unité de Recherche de Génétique et Ecophysiologie des Légumineuses INRA, BP 86510, 21065 Dijon Cedex, France.

Back to Top

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: debelle{at}

Synthetic biology approaches to engineering the nitrogen symbiosis in cereals.
C. Rogers and G. E. D. Oldroyd (2014)
J. Exp. Bot. 65, 1939-1946
   Abstract »    Full Text »    PDF »
A Rice Gene for Microbial Symbiosis, Oryza sativa CCaMK, Reduces CH4 Flux in a Paddy Field with Low Nitrogen Input.
Z. Bao, A. Watanabe, K. Sasaki, T. Okubo, T. Tokida, D. Liu, S. Ikeda, H. Imaizumi-Anraku, S. Asakawa, T. Sato, et al. (2014)
Appl. Envir. Microbiol. 80, 1995-2003
   Abstract »    Full Text »    PDF »
Isolation and Phenotypic Characterization of Lotus japonicus Mutants Specifically Defective in Arbuscular Mycorrhizal Formation.
T. Kojima, K. Saito, H. Oba, Y. Yoshida, J. Terasawa, Y. Umehara, N. Suganuma, M. Kawaguchi, and R. Ohtomo (2014)
Plant Cell Physiol.
   Abstract »    Full Text »    PDF »
Lotus japonicus Cytokinin Receptors Work Partially Redundantly to Mediate Nodule Formation.
M. Held, H. Hou, M. Miri, C. Huynh, L. Ross, M. S. Hossain, S. Sato, S. Tabata, J. Perry, T. L. Wang, et al. (2014)
PLANT CELL 26, 678-694
   Abstract »    Full Text »    PDF »
DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis.
D. S. Floss, J. G. Levy, V. Levesque-Tremblay, N. Pumplin, and M. J. Harrison (2013)
PNAS 110, E5025-E5034
   Abstract »    Full Text »    PDF »
Calcium/Calmodulin-Dependent Protein Kinase Is Negatively and Positively Regulated by Calcium, Providing a Mechanism for Decoding Calcium Responses during Symbiosis Signaling.
J. B. Miller, A. Pratap, A. Miyahara, L. Zhou, S. Bornemann, R. J. Morris, and G. E. D. Oldroyd (2013)
PLANT CELL 25, 5053-5066
   Abstract »    Full Text »    PDF »
CERBERUS and NSP1 of Lotus japonicus are Common Symbiosis Genes that Modulate Arbuscular Mycorrhiza Development.
N. Takeda, S. Tsuzuki, T. Suzaki, M. Parniske, and M. Kawaguchi (2013)
Plant Cell Physiol. 54, 1711-1723
   Abstract »    Full Text »    PDF »
Nuclear Calcium Signaling in Plants.
M. Charpentier and G. E. D. Oldroyd (2013)
Plant Physiology 163, 496-503
   Full Text »    PDF »
Recent Advances in Calcium/Calmodulin-Mediated Signaling with an Emphasis on Plant-Microbe Interactions.
B. W. Poovaiah, L. Du, H. Wang, and T. Yang (2013)
Plant Physiology 163, 531-542
   Full Text »    PDF »
Rhizobial and Mycorrhizal Symbioses in Lotus japonicus Require Lectin Nucleotide Phosphohydrolase, Which Acts Upstream of Calcium Signaling.
N. J. Roberts, G. Morieri, G. Kalsi, A. Rose, J. Stiller, A. Edwards, F. Xie, P. M. Gresshoff, G. E. D. Oldroyd, J. A. Downie, et al. (2013)
Plant Physiology 161, 556-567
   Abstract »    Full Text »    PDF »
Buffering Capacity Explains Signal Variation in Symbiotic Calcium Oscillations.
E. Granqvist, D. Wysham, S. Hazledine, W. Kozlowski, J. Sun, M. Charpentier, T. V. Martins, P. Haleux, K. Tsaneva-Atanasova, J. A. Downie, et al. (2012)
Plant Physiology 160, 2300-2310
   Abstract »    Full Text »    PDF »
Medicago truncatula ERN Transcription Factors: Regulatory Interplay with NSP1/NSP2 GRAS Factors and Expression Dynamics throughout Rhizobial Infection.
M. R. Cerri, L. Frances, T. Laloum, M.-C. Auriac, A. Niebel, G. E. D. Oldroyd, D. G. Barker, J. Fournier, and F. de Carvalho-Niebel (2012)
Plant Physiology 160, 2155-2172
   Abstract »    Full Text »    PDF »
Mapping the Genetic Basis of Symbiotic Variation in Legume-Rhizobium Interactions in Medicago truncatula.
A. J. Gorton, K. D. Heath, M.-L. Pilet-Nayel, A. Baranger, and J. R. Stinchcombe (2012)
g3 2, 1291-1303
   Abstract »    Full Text »    PDF »
OsDMI3 Is a Novel Component of Abscisic Acid Signaling in the Induction of Antioxidant Defense in Leaves of Rice.
B. Shi, L. Ni, A. Zhang, J. Cao, H. Zhang, T. Qin, M. Tan, J. Zhang, and M. Jiang (2012)
Mol Plant 5, 1359-1374
   Abstract »    Full Text »    PDF »
Quantitative Phosphoproteomic Analysis of Soybean Root Hairs Inoculated with Bradyrhizobium japonicum.
T. H. N. Nguyen, L. Brechenmacher, J. T. Aldrich, T. R. Clauss, M. A. Gritsenko, K. K. Hixson, M. Libault, K. Tanaka, F. Yang, Q. Yao, et al. (2012)
Mol. Cell. Proteomics 11, 1140-1155
   Abstract »    Full Text »    PDF »
Epidermal and cortical roles of NFP and DMI3 in coordinating early steps of nodulation in Medicago truncatula.
P. Rival, F. de Billy, J.-J. Bono, C. Gough, C. Rosenberg, and S. Bensmihen (2012)
Development 139, 3383-3391
   Abstract »    Full Text »    PDF »
Rapid Phosphoproteomic and Transcriptomic Changes in the Rhizobia-legume Symbiosis.
C. M. Rose, M. Venkateshwaran, J. D. Volkening, P. A. Grimsrud, J. Maeda, D. J. Bailey, K. Park, M. Howes-Podoll, D. den Os, L. H. Yeun, et al. (2012)
Mol. Cell. Proteomics 11, 724-744
   Abstract »    Full Text »    PDF »
Nitric oxide-activated calcium/calmodulin-dependent protein kinase regulates the abscisic acid-induced antioxidant defence in maize.
F. Ma, R. Lu, H. Liu, B. Shi, J. Zhang, M. Tan, A. Zhang, and M. Jiang (2012)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
A Medicago truncatula Tobacco Retrotransposon Insertion Mutant Collection with Defects in Nodule Development and Symbiotic Nitrogen Fixation.
C. I. Pislariu, J. D. Murray, J. Wen, V. Cosson, R. R. D. Muni, M. Wang, V. A. Benedito, A. Andriankaja, X. Cheng, I. T. Jerez, et al. (2012)
Plant Physiology 159, 1686-1699
   Abstract »    Full Text »    PDF »
WUSCHEL-RELATED HOMEOBOX5 Gene Expression and Interaction of CLE Peptides with Components of the Systemic Control Add Two Pieces to the Puzzle of Autoregulation of Nodulation.
M. A. Osipova, V. Mortier, K. N. Demchenko, V. E. Tsyganov, I. A. Tikhonovich, L. A. Lutova, E. A. Dolgikh, and S. Goormachtig (2012)
Plant Physiology 158, 1329-1341
   Abstract »    Full Text »    PDF »
Nuclear-Localized and Deregulated Calcium- and Calmodulin-Dependent Protein Kinase Activates Rhizobial and Mycorrhizal Responses in Lotus japonicus.
N. Takeda, T. Maekawa, and M. Hayashi (2012)
PLANT CELL 24, 810-822
   Abstract »    Full Text »    PDF »
Rhizobial and Fungal Symbioses Show Different Requirements for Calmodulin Binding to Calcium Calmodulin-Dependent Protein Kinase in Lotus japonicus.
Y. Shimoda, L. Han, T. Yamazaki, R. Suzuki, M. Hayashi, and H. Imaizumi-Anraku (2012)
PLANT CELL 24, 304-321
   Abstract »    Full Text »    PDF »
A Phylogenetic Strategy Based on a Legume-Specific Whole Genome Duplication Yields Symbiotic Cytokinin Type-A Response Regulators.
R. H. M. Op den Camp, S. De Mita, A. Lillo, Q. Cao, E. Limpens, T. Bisseling, and R. Geurts (2011)
Plant Physiology 157, 2013-2022
   Abstract »    Full Text »    PDF »
Translational Genomics in Legumes Allowed Placing In Silico 5460 Unigenes on the Pea Functional Map and Identified Candidate Genes in Pisum sativum L..
A. Bordat, V. Savois, M. Nicolas, J. Salse, A. Chauveau, M. Bourgeois, J. Potier, H. Houtin, C. Rond, F. Murat, et al. (2011)
g3 1, 93-103
   Abstract »    Full Text »    PDF »
Symbiotic Rhizobia Bacteria Trigger a Change in Localization and Dynamics of the Medicago truncatula Receptor Kinase LYK3.
C. H. Haney, B. K. Riely, D. M. Tricoli, D. R. Cook, D. W. Ehrhardt, and S. R. Long (2011)
PLANT CELL 23, 2774-2787
   Abstract »    Full Text »    PDF »
Structure-Function Similarities between a Plant Receptor-like Kinase and the Human Interleukin-1 Receptor-associated Kinase-4.
D. Klaus-Heisen, A. Nurisso, A. Pietraszewska-Bogiel, M. Mbengue, S. Camut, T. Timmers, C. Pichereaux, M. Rossignol, T. W. J. Gadella, A. Imberty, et al. (2011)
J. Biol. Chem. 286, 11202-11210
   Abstract »    Full Text »    PDF »
A Novel Interaction between CCaMK and a Protein Containing the Scythe_N Ubiquitin-Like Domain in Lotus japonicus.
H. Kang, H. Zhu, X. Chu, Z. Yang, S. Yuan, D. Yu, C. Wang, Z. Hong, and Z. Zhang (2011)
Plant Physiology 155, 1312-1324
   Abstract »    Full Text »    PDF »
plenty, a Novel Hypernodulation Mutant in Lotus japonicus.
C. Yoshida, S. Funayama-Noguchi, and M. Kawaguchi (2010)
Plant Cell Physiol. 51, 1425-1435
   Abstract »    Full Text »    PDF »
How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground.
H. Kouchi, H. Imaizumi-Anraku, M. Hayashi, T. Hakoyama, T. Nakagawa, Y. Umehara, N. Suganuma, and M. Kawaguchi (2010)
Plant Cell Physiol. 51, 1381-1397
   Abstract »    Full Text »    PDF »
Cross-Talk between ROS and Calcium in Regulation of Nuclear Activities.
C. Mazars, P. Thuleau, O. Lamotte, and S. Bourque (2010)
Mol Plant 3, 706-718
   Abstract »    Full Text »    PDF »
NENA, a Lotus japonicus Homolog of Sec13, Is Required for Rhizodermal Infection by Arbuscular Mycorrhiza Fungi and Rhizobia but Dispensable for Cortical Endosymbiotic Development.
M. Groth, N. Takeda, J. Perry, H. Uchida, S. Draxl, A. Brachmann, S. Sato, S. Tabata, M. Kawaguchi, T. L. Wang, et al. (2010)
PLANT CELL 22, 2509-2526
   Abstract »    Full Text »    PDF »
GsCBRLK, a calcium/calmodulin-binding receptor-like kinase, is a positive regulator of plant tolerance to salt and ABA stress.
L. Yang, W. Ji, Y. Zhu, P. Gao, Y. Li, H. Cai, X. Bai, and D. Guo (2010)
J. Exp. Bot. 61, 2519-2533
   Abstract »    Full Text »    PDF »
Large-Scale Phosphoprotein Analysis in Medicago truncatula Roots Provides Insight into in Vivo Kinase Activity in Legumes.
P. A. Grimsrud, D. den Os, C. D. Wenger, D. L. Swaney, D. Schwartz, M. R. Sussman, J.-M. Ane, and J. J. Coon (2010)
Plant Physiology 152, 19-28
   Abstract »    Full Text »    PDF »
A Nuclear-Targeted Cameleon Demonstrates Intranuclear Ca2+ Spiking in Medicago truncatula Root Hairs in Response to Rhizobial Nodulation Factors.
B. J. Sieberer, M. Chabaud, A. C. Timmers, A. Monin, J. Fournier, and D. G. Barker (2009)
Plant Physiology 151, 1197-1206
   Abstract »    Full Text »    PDF »
LIN, a Novel Type of U-Box/WD40 Protein, Controls Early Infection by Rhizobia in Legumes.
E. Kiss, B. Olah, P. Kalo, M. Morales, A. B. Heckmann, A. Borbola, A. Lozsa, K. Kontar, P. Middleton, J. A. Downie, et al. (2009)
Plant Physiology 151, 1239-1249
   Abstract »    Full Text »    PDF »
Calcium Spiking Patterns and the Role of the Calcium/Calmodulin-Dependent Kinase CCaMK in Lateral Root Base Nodulation of Sesbania rostrata.
W. Capoen, J. Den Herder, J. Sun, C. Verplancke, A. De Keyser, R. De Rycke, S. Goormachtig, G. Oldroyd, and M. Holsters (2009)
PLANT CELL 21, 1526-1540
   Abstract »    Full Text »    PDF »
Biotic and Abiotic Stimulation of Root Epidermal Cells Reveals Common and Specific Responses to Arbuscular Mycorrhizal Fungi.
A. Genre, G. Ortu, C. Bertoldo, E. Martino, and P. Bonfante (2009)
Plant Physiology 149, 1424-1434
   Abstract »    Full Text »    PDF »
GRAS Proteins Form a DNA Binding Complex to Induce Gene Expression during Nodulation Signaling in Medicago truncatula.
S. Hirsch, J. Kim, A. Munoz, A. B. Heckmann, J. A. Downie, and G. E.D. Oldroyd (2009)
PLANT CELL 21, 545-557
   Abstract »    Full Text »    PDF »
Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti.
K. Yokota, E. Fukai, L. H. Madsen, A. Jurkiewicz, P. Rueda, S. Radutoiu, M. Held, M. S. Hossain, K. Szczyglowski, G. Morieri, et al. (2009)
PLANT CELL 21, 267-284
   Abstract »    Full Text »    PDF »
Antiquity and Function of CASTOR and POLLUX, the Twin Ion Channel-Encoding Genes Key to the Evolution of Root Symbioses in Plants.
C. Chen, C. Fan, M. Gao, and H. Zhu (2009)
Plant Physiology 149, 306-317
   Abstract »    Full Text »    PDF »
CYCLOPS, a mediator of symbiotic intracellular accommodation.
K. Yano, S. Yoshida, J. Muller, S. Singh, M. Banba, K. Vickers, K. Markmann, C. White, B. Schuller, S. Sato, et al. (2008)
PNAS 105, 20540-20545
   Abstract »    Full Text »    PDF »
De Novo Organ Formation from Differentiated Cells: Root Nodule Organogenesis.
M. Crespi and F. Frugier (2008)
Science Signaling 1, re11
   Abstract »    Full Text »    PDF »
Arbuscular Mycorrhiza-Specific Signaling in Rice Transcends the Common Symbiosis Signaling Pathway.
C. Gutjahr, M. Banba, V. Croset, K. An, A. Miyao, G. An, H. Hirochika, H. Imaizumi-Anraku, and U. Paszkowski (2008)
PLANT CELL 20, 2989-3005
   Abstract »    Full Text »    PDF »
Abscisic Acid Coordinates Nod Factor and Cytokinin Signaling during the Regulation of Nodulation in Medicago truncatula.
Y. Ding, P. Kalo, C. Yendrek, J. Sun, Y. Liang, J. F. Marsh, J. M. Harris, and G. E.D. Oldroyd (2008)
PLANT CELL 20, 2681-2695
   Abstract »    Full Text »    PDF »
Soybean Nodule Autoregulation Receptor Kinase Phosphorylates Two Kinase-associated Protein Phosphatases in Vitro.
A. Miyahara, T. A. Hirani, M. Oakes, A. Kereszt, B. Kobe, M. A. Djordjevic, and P. M. Gresshoff (2008)
J. Biol. Chem. 283, 25381-25391
   Abstract »    Full Text »    PDF »
Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes.
S. Kosuta, S. Hazledine, J. Sun, H. Miwa, R. J. Morris, J. A. Downie, and G. E. D. Oldroyd (2008)
PNAS 105, 9823-9828
   Abstract »    Full Text »    PDF »
Investigation of the Demographic and Selective Forces Shaping the Nucleotide Diversity of Genes Involved in Nod Factor Signaling in Medicago truncatula.
S. De Mita, J. Ronfort, H. I. McKhann, C. Poncet, R. El Malki, and T. Bataillon (2007)
Genetics 177, 2123-2133
   Abstract »    Full Text »    PDF »
3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase1 Interacts with NORK and Is Crucial for Nodulation in Medicago truncatula.
Z. Kevei, G. Lougnon, P. Mergaert, G. V. Horvath, A. Kereszt, D. Jayaraman, N. Zaman, F. Marcel, K. Regulski, G. B. Kiss, et al. (2007)
PLANT CELL 19, 3974-3989
   Abstract »    Full Text »    PDF »
Fungal Symbiosis in Rice Requires an Ortholog of a Legume Common Symbiosis Gene Encoding a Ca2+/Calmodulin-Dependent Protein Kinase.
C. Chen, M. Gao, J. Liu, and H. Zhu (2007)
Plant Physiology 145, 1619-1628
   Abstract »    Full Text »    PDF »
AP2-ERF Transcription Factors Mediate Nod Factor Dependent Mt ENOD11 Activation in Root Hairs via a Novel cis-Regulatory Motif.
A. Andriankaja, A. Boisson-Dernier, L. Frances, L. Sauviac, A. Jauneau, D. G. Barker, and F. de Carvalho-Niebel (2007)
PLANT CELL 19, 2866-2885
   Abstract »    Full Text »    PDF »
Comparative Transcriptome Analysis Reveals Common and Specific Tags for Root Hair and Crack-Entry Invasion in Sesbania rostrata.
W. Capoen, J. Den Herder, S. Rombauts, J. De Gussem, A. De Keyser, M. Holsters, and S. Goormachtig (2007)
Plant Physiology 144, 1878-1889
   Abstract »    Full Text »    PDF »
Transcriptome Analysis of Arbuscular Mycorrhizal Roots during Development of the Prepenetration Apparatus.
V. Siciliano, A. Genre, R. Balestrini, G. Cappellazzo, P. J.G.M. deWit, and P. Bonfante (2007)
Plant Physiology 144, 1455-1466
   Abstract »    Full Text »    PDF »
A Diffusible Signal from Arbuscular Mycorrhizal Fungi Elicits a Transient Cytosolic Calcium Elevation in Host Plant Cells.
L. Navazio, R. Moscatiello, A. Genre, M. Novero, B. Baldan, P. Bonfante, and P. Mariani (2007)
Plant Physiology 144, 673-681
   Abstract »    Full Text »    PDF »
Mastoparan Activates Calcium Spiking Analogous to Nod Factor-Induced Responses in Medicago truncatula Root Hair Cells.
J. Sun, H. Miwa, J. A. Downie, and G. E.D. Oldroyd (2007)
Plant Physiology 144, 695-702
   Abstract »    Full Text »    PDF »
An IRE-Like AGC Kinase Gene, MtIRE, Has Unique Expression in the Invasion Zone of Developing Root Nodules in Medicago truncatula.
C. I. Pislariu and R. Dickstein (2007)
Plant Physiology 144, 682-694
   Abstract »    Full Text »    PDF »
Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase.
J. F. Marsh, A. Rakocevic, R. M. Mitra, L. Brocard, J. Sun, A. Eschstruth, S. R. Long, M. Schultze, P. Ratet, and G. E.D. Oldroyd (2007)
Plant Physiology 144, 324-335
   Abstract »    Full Text »    PDF »
An ERF Transcription Factor in Medicago truncatula That Is Essential for Nod Factor Signal Transduction.
P. H. Middleton, J. Jakab, R. V. Penmetsa, C. G. Starker, J. Doll, P. Kalo, R. Prabhu, J. F. Marsh, R. M. Mitra, A. Kereszt, et al. (2007)
PLANT CELL 19, 1221-1234
   Abstract »    Full Text »    PDF »
A Novel Ankyrin-Repeat Membrane Protein, IGN1, Is Required for Persistence of Nitrogen-Fixing Symbiosis in Root Nodules of Lotus japonicus.
H. Kumagai, T. Hakoyama, Y. Umehara, S. Sato, T. Kaneko, S. Tabata, and H. Kouchi (2007)
Plant Physiology 143, 1293-1305
   Abstract »    Full Text »    PDF »
NUCLEOPORIN85 Is Required for Calcium Spiking, Fungal and Bacterial Symbioses, and Seed Production in Lotus japonicus.
K. Saito, M. Yoshikawa, K. Yano, H. Miwa, H. Uchida, E. Asamizu, S. Sato, S. Tabata, H. Imaizumi-Anraku, Y. Umehara, et al. (2007)
PLANT CELL 19, 610-624
   Abstract »    Full Text »    PDF »
A Cytokinin Perception Mutant Colonized by Rhizobium in the Absence of Nodule Organogenesis.
J. D. Murray, B. J. Karas, S. Sato, S. Tabata, L. Amyot, and K. Szczyglowski (2007)
Science 315, 101-104
   Abstract »    Full Text »    PDF »
Lotus japonicus Nodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume.
A. B. Heckmann, F. Lombardo, H. Miwa, J. A. Perry, S. Bunnewell, M. Parniske, T. L. Wang, and J. A. Downie (2006)
Plant Physiology 142, 1739-1750
   Abstract »    Full Text »    PDF »
The Medicago truncatula Lysine Motif-Receptor-Like Kinase Gene Family Includes NFP and New Nodule-Expressed Genes.
J.-F. Arrighi, A. Barre, B. Ben Amor, A. Bersoult, L. C. Soriano, R. Mirabella, F. de Carvalho-Niebel, E.-P. Journet, M. Gherardi, T. Huguet, et al. (2006)
Plant Physiology 142, 265-279
   Abstract »    Full Text »    PDF »
Recruitment of Novel Calcium-Binding Proteins for Root Nodule Symbiosis in Medicago truncatula.
J. Liu, S. S. Miller, M. Graham, B. Bucciarelli, C. M. Catalano, D. J. Sherrier, D. A. Samac, S. Ivashuta, M. Fedorova, P. Matsumoto, et al. (2006)
Plant Physiology 141, 167-177
   Abstract »    Full Text »    PDF »
Tracing Nonlegume Orthologs of Legume Genes Required for Nodulation and Arbuscular Mycorrhizal Symbioses.
H. Zhu, B. K. Riely, N. J. Burns, and J.-M. Ane (2006)
Genetics 172, 2491-2499
   Abstract »    Full Text »    PDF »
From The Cover: A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis.
N. Kanamori, L. H. Madsen, S. Radutoiu, M. Frantescu, E. M. H. Quistgaard, H. Miwa, J. A. Downie, E. K. James, H. H. Felle, L. L. Haaning, et al. (2006)
PNAS 103, 359-364
   Abstract »    Full Text »    PDF »
Positional Cloning Identifies Lotus japonicus NSP2, A Putative Transcription Factor of the GRAS Family, Required for NIN and ENOD40 Gene Expression in Nodule Initiation.
Y. Murakami, H. Miwa, H. Imaizumi-Anraku, H. Kouchi, J. A. Downie, M. Kawaguchi, and S. Kawasaki (2006)
DNA Res 13, 255-265
   Abstract »    Full Text »    PDF »
The DMI1 and DMI2 Early Symbiotic Genes of Medicago truncatula Are Required for a High-Affinity Nodulation Factor-Binding Site Associated to a Particulate Fraction of Roots.
B. V. Hogg, J. V. Cullimore, R. Ranjeva, and J.-J. Bono (2006)
Plant Physiology 140, 365-373
   Abstract »    Full Text »    PDF »
Arbuscular Mycorrhizal Fungi Elicit a Novel Intracellular Apparatus in Medicago truncatula Root Epidermal Cells before Infection.
A. Genre, M. Chabaud, T. Timmers, P. Bonfante, and D. G. Barker (2005)
PLANT CELL 17, 3489-3499
   Abstract »    Full Text »    PDF »
RNA Interference Identifies a Calcium-Dependent Protein Kinase Involved in Medicago truncatula Root Development.
S. Ivashuta, J. Liu, J. Liu, D. P. Lohar, S. Haridas, B. Bucciarelli, K. A. VandenBosch, C. P. Vance, M. J. Harrison, and J. S. Gantt (2005)
PLANT CELL 17, 2911-2921
   Abstract »    Full Text »    PDF »
Nod Factors Induce Nod Factor Cleaving Enzymes in Pea Roots. Genetic and Pharmacological Approaches Indicate Different Activation Mechanisms.
A. O. Ovtsyna, E. A. Dolgikh, A. S. Kilanova, V. E. Tsyganov, A. Y. Borisov, I. A. Tikhonovich, and C. Staehelin (2005)
Plant Physiology 139, 1051-1064
   Abstract »    Full Text »    PDF »
Pseudomonas fluorescens and Glomus mosseae Trigger DMI3-Dependent Activation of Genes Related to a Signal Transduction Pathway in Roots of Medicago truncatula.
L. Sanchez, S. Weidmann, C. Arnould, A. R. Bernard, S. Gianinazzi, and V. Gianinazzi-Pearson (2005)
Plant Physiology 139, 1065-1077
   Abstract »    Full Text »    PDF »
Seven Lotus japonicus Genes Required for Transcriptional Reprogramming of the Root during Fungal and Bacterial Symbiosis.
C. Kistner, T. Winzer, A. Pitzschke, L. Mulder, S. Sato, T. Kaneko, S. Tabata, N. Sandal, J. Stougaard, K. J. Webb, et al. (2005)
PLANT CELL 17, 2217-2229
   Abstract »    Full Text »    PDF »
SrSymRK, a plant receptor essential for symbiosome formation.
W. Capoen, S. Goormachtig, R. De Rycke, K. Schroeyers, and M. Holsters (2005)
PNAS 102, 10369-10374
   Abstract »    Full Text »    PDF »
Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2.
E. Limpens, R. Mirabella, E. Fedorova, C. Franken, H. Franssen, T. Bisseling, and R. Geurts (2005)
PNAS 102, 10375-10380
   Abstract »    Full Text »    PDF »
Biological costs and benefits to plant-microbe interactions in the rhizosphere.
J. A. W. Morgan, G. D. Bending, and P. J. White (2005)
J. Exp. Bot. 56, 1729-1739
   Abstract »    Full Text »    PDF »
Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators.
P. Kalo, C. Gleason, A. Edwards, J. Marsh, R. M. Mitra, S. Hirsch, J. Jakab, S. Sims, S. R. Long, J. Rogers, et al. (2005)
Science 308, 1786-1789
   Abstract »    Full Text »    PDF »
NSP1 of the GRAS Protein Family Is Essential for Rhizobial Nod Factor-Induced Transcription.
P. Smit, J. Raedts, V. Portyanko, F. Debelle, C. Gough, T. Bisseling, and R. Geurts (2005)
Science 308, 1789-1791
   Abstract »    Full Text »    PDF »
Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization.
S. Guimil, H.-S. Chang, T. Zhu, A. Sesma, A. Osbourn, C. Roux, V. Ioannidis, E. J. Oakeley, M. Docquier, P. Descombes, et al. (2005)
PNAS 102, 8066-8070
   Abstract »    Full Text »    PDF »
The Sulfate Transporter SST1 Is Crucial for Symbiotic Nitrogen Fixation in Lotus japonicus Root Nodules.
L. Krusell, K. Krause, T. Ott, G. Desbrosses, U. Kramer, S. Sato, Y. Nakamura, S. Tabata, E. K. James, N. Sandal, et al. (2005)
PLANT CELL 17, 1625-1636
   Abstract »    Full Text »    PDF »
Sequencing the Genespaces of Medicago truncatula and Lotus japonicus.
N. D. Young, S. B. Cannon, S. Sato, D. Kim, D. R. Cook, C. D. Town, B. A. Roe, and S. Tabata (2005)
Plant Physiology 137, 1174-1181
   Full Text »    PDF »
Bridging Model and Crop Legumes through Comparative Genomics.
H. Zhu, H.-K. Choi, D. R. Cook, and R. C. Shoemaker (2005)
Plant Physiology 137, 1189-1196
   Full Text »    PDF »
Peace Talks and Trade Deals. Keys to Long-Term Harmony in Legume-Microbe Symbioses.
G. E.D. Oldroyd, M. J. Harrison, and M. Udvardi (2005)
Plant Physiology 137, 1205-1210
   Full Text »    PDF »
Characterization of the Lotus japonicus Symbiotic Mutant lot1 That Shows a Reduced Nodule Number and Distorted Trichomes.
Y. Ooki, M. Banba, K. Yano, J. Maruya, S. Sato, S. Tabata, K. Saeki, M. Hayashi, M. Kawaguchi, K. Izui, et al. (2005)
Plant Physiology 137, 1261-1271
   Abstract »    Full Text »    PDF »
Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus.
R. R. Weerasinghe, D. McK. Bird, and N. S. Allen (2005)
PNAS 102, 3147-3152
   Abstract »    Full Text »    PDF »
Genome-wide Identification of the Rice Calcium-dependent Protein Kinase and its Closely Related Kinase Gene Families: Comprehensive Analysis of the CDPKs Gene Family in Rice.
T. Asano, N. Tanaka, G. Yang, N. Hayashi, and S. Komatsu (2005)
Plant Cell Physiol. 46, 356-366
   Abstract »    Full Text »    PDF »
Pharmacological Evidence That Multiple Phospholipid Signaling Pathways Link Rhizobium Nodulation Factor Perception in Medicago truncatula Root Hairs to Intracellular Responses, Including Ca2+ Spiking and Specific ENOD Gene Expression.
D. Charron, J.-L. Pingret, M. Chabaud, E.-P. Journet, and D. G. Barker (2004)
Plant Physiology 136, 3582-3593
   Abstract »    Full Text »    PDF »
LIN, a Medicago truncatula Gene Required for Nodule Differentiation and Persistence of Rhizobial Infections.
K. T. Kuppusamy, G. Endre, R. Prabhu, R. V. Penmetsa, H. Veereshlingam, D. R. Cook, R. Dickstein, and K. A. VandenBosch (2004)
Plant Physiology 136, 3682-3691
   Abstract »    Full Text »    PDF »
Calcium/Calmodulin Up-regulates a Cytoplasmic Receptor-like Kinase in Plants.
T. Yang, S. Chaudhuri, L. Yang, Y. Chen, and B. W. Poovaiah (2004)
J. Biol. Chem. 279, 42552-42559
   Abstract »    Full Text »    PDF »
Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume-rhizobia symbiosis.
R. M. Mitra, S. L. Shaw, and S. R. Long (2004)
PNAS 101, 10217-10222
   Abstract »    Full Text »    PDF »
Positioning Arabidopsis in Plant Biology. A Key Step Toward Unification of Plant Research.
M. Bevan and S. Walsh (2004)
Plant Physiology 135, 602-606
   Abstract »    Full Text »    PDF »
Unraveling the mystery of Nod factor signaling by a genomic approach in Medicago trunactula.
D. R. Cook (2004)
PNAS 101, 4339-4340
   Full Text »    PDF »
Medicago truncatula DMI1 Required for Bacterial and Fungal Symbioses in Legumes.
J.-M. Ane, G. B. Kiss, B. K. Riely, R. V. Penmetsa, G. E. D. Oldroyd, C. Ayax, J. Levy, F. Debelle, J.-M. Baek, P. Kalo, et al. (2004)
Science 303, 1364-1367
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882