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.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Originally published in Science Express on 12 February 2004
Science 27 February 2004:
Vol. 303. no. 5662, pp. 1361 - 1364
DOI: 10.1126/science.1093038
Prev | Table of Contents | Next

Reports

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}

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.


* These authors contributed equally to this work.

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

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
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 »
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 »
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 »
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 »


ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)