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 28 August 2003
Science 24 October 2003:
Vol. 302. no. 5645, pp. 630 - 633
DOI: 10.1126/science.1090074
Prev | Table of Contents | Next

Reports

LysM Domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection

Erik Limpens, Carolien Franken, Patrick Smit, Joost Willemse, Ton Bisseling,* René Geurts

The rhizobial infection of legumes has the most stringent demand toward Nod factor structure of all host responses, and therefore a specific Nod factor entry receptor has been proposed. The SYM2 gene identified in certain ecotypes of pea (Pisum sativum) is a good candidate for such an entry receptor. We exploited the close phylogenetic relationship of pea and the model legume Medicago truncatula to identify genes specifically involved in rhizobial infection. The SYM2 orthologous region of M. truncatula contains 15 putative receptor-like genes, of which 7 are LysM domain–containing receptor-like kinases (LYKs). Using reverse genetics in M. truncatula, we show that two LYK genes are specifically involved in infection thread formation. This, as well as the properties of the LysM domains, strongly suggests that they are Nod factor entry receptors.

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, Dreijenlaan 3, 6703HA, Wageningen, Netherlands.

* To whom correspondence should be addressed. E-mail: ton.bisseling{at}wur.nl

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 »
The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection.
J.-F. Arrighi, O. Godfroy, F. de Billy, O. Saurat, A. Jauneau, and C. Gough (2008)
PNAS 105, 9817-9822
   Abstract »    Full Text »    PDF »
A new type of plant chitinase containing LysM domains from a fern (Pteris ryukyuensis): Roles of LysM domains in chitin binding and antifungal activity.
S. Onaga and T. Taira (2008)
Glycobiology 18, 414-423
   Abstract »    Full Text »    PDF »
LysM Domains from Pteris ryukyuensis Chitinase-A: A STABILITY STUDY AND CHARACTERIZATION OF THE CHITIN-BINDING SITE.
T. Ohnuma, S. Onaga, K. Murata, T. Taira, and E. Katoh (2008)
J. Biol. Chem. 283, 5178-5187
   Abstract »    Full Text »    PDF »
A LysM Receptor-Like Kinase Plays a Critical Role in Chitin Signaling and Fungal Resistance in Arabidopsis.
J. Wan, X.-C. Zhang, D. Neece, K. M. Ramonell, S. Clough, S.-y. Kim, M. G. Stacey, and G. Stacey (2008)
PLANT CELL 20, 471-481
   Abstract »    Full Text »    PDF »
Chitin Signaling in Plants: Insights into the Perception of Fungal Pathogens and Rhizobacterial Symbionts.
N. A. Eckardt (2008)
PLANT CELL 20, 241-243
   Full Text »    PDF »
Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant.
K. M. Jones, N. Sharopova, D. P. Lohar, J. Q. Zhang, K. A. VandenBosch, and G. C. Walker (2008)
PNAS 105, 704-709
   Abstract »    Full Text »    PDF »
CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis.
A. Miya, P. Albert, T. Shinya, Y. Desaki, K. Ichimura, K. Shirasu, Y. Narusaka, N. Kawakami, H. Kaku, and N. Shibuya (2007)
PNAS 104, 19613-19618
   Abstract »    Full Text »    PDF »
H2O2 Is Required for Optimal Establishment of the Medicago sativa/Sinorhizobium meliloti Symbiosis.
A. Jamet, K. Mandon, A. Puppo, and D. Herouart (2007)
J. Bacteriol. 189, 8741-8745
   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 »
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 »
Rhizobial Factors Required for Stem Nodule Maturation and Maintenance in Sesbania rostrata-Azorhizobium caulinodans ORS571 Symbiosis.
S. Suzuki, T. Aono, K.-B. Lee, T. Suzuki, C.-T. Liu, H. Miwa, S. Wakao, T. Iki, and H. Oyaizu (2007)
Appl. Envir. Microbiol. 73, 6650-6659
   Abstract »    Full Text »    PDF »
Medicago LYK3, an Entry Receptor in Rhizobial Nodulation Factor Signaling.
P. Smit, E. Limpens, R. Geurts, E. Fedorova, E. Dolgikh, C. Gough, and T. Bisseling (2007)
Plant Physiology 145, 183-191
   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 »
Recent Advances in Legume-Microbe Interactions: Recognition, Defense Response, and Symbiosis from a Genomic Perspective.
D. A. Samac and M. A. Graham (2007)
Plant Physiology 144, 582-587
   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 »
The MtMMPL1 Early Nodulin Is a Novel Member of the Matrix Metalloendoproteinase Family with a Role in Medicago truncatula Infection by Sinorhizobium meliloti.
J.-P. Combier, T. Vernie, F. de Billy, F. El Yahyaoui, R. Mathis, and P. Gamas (2007)
Plant Physiology 144, 703-716
   Abstract »    Full Text »    PDF »
Molecular Evolution of Lysin Motif-Type Receptor-Like Kinases in Plants.
X.-C. Zhang, X. Wu, S. Findley, J. Wan, M. Libault, H. T. Nguyen, S. B. Cannon, and G. Stacey (2007)
Plant Physiology 144, 623-636
   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 »
Receptor-like protein kinase HvLysMR1 of barley (Hordeum vulgare L.) is induced during leaf senescence and heavy metal stress.
A. Ouelhadj, M. Kaminski, M. Mittag, and K. Humbeck (2007)
J. Exp. Bot. 58, 1381-1396
   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 »
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 »
Interaction between Coat Morphogenetic Proteins SafA and SpoVID.
T. Costa, A. L. Isidro, C. P. Moran Jr., and A. O. Henriques (2006)
J. Bacteriol. 188, 7731-7741
   Abstract »    Full Text »    PDF »
MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula..
J.-P. Combier, F. Frugier, F. de Billy, A. Boualem, F. El-Yahyaoui, S. Moreau, T. Vernie, T. Ott, P. Gamas, M. Crespi, et al. (2006)
Genes & Dev. 20, 3084-3088
   Abstract »    Full Text »    PDF »
LjnsRING, a Novel RING Finger Protein, is Required for Symbiotic Interactions Between Mesorhizobium loti and Lotus japonicus.
K. Shimomura, M. Nomura, S. Tajima, and H. Kouchi (2006)
Plant Cell Physiol. 47, 1572-1581
   Abstract »    Full Text »    PDF »
LysM domains of Medicago truncatula NFP protein involved in Nod factor perception. Glycosylation state, molecular modeling and docking of chitooligosaccharides and Nod factors.
L. Mulder, B. Lefebvre, J. Cullimore, and A. Imberty (2006)
Glycobiology 16, 801-809
   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 »
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 »
Distribution of Microsatellites in the Genome of Medicago truncatula: A Resource of Genetic Markers That Integrate Genetic and Physical Maps.
J.-H. Mun, D.-J. Kim, H.-K. Choi, J. Gish, F. Debelle, J. Mudge, R. Denny, G. Endre, O. Saurat, A.-M. Dudez, et al. (2006)
Genetics 172, 2541-2555
   Abstract »    Full Text »    PDF »
A sulfated metabolite produced by stf3 negatively regulates the virulence of Mycobacterium tuberculosis..
J. D. Mougous, R. H. Senaratne, C. J. Petzold, M. Jain, D. H. Lee, M. W. Schelle, M. D. Leavell, J. S. Cox, J. A. Leary, L. W. Riley, et al. (2006)
PNAS 103, 4258-4263
   Abstract »    Full Text »    PDF »
A Segment of the Apospory-Specific Genomic Region Is Highly Microsyntenic Not Only between the Apomicts Pennisetum squamulatum and Buffelgrass, But Also with a Rice Chromosome 11 Centromeric-Proximal Genomic Region.
G. Gualtieri, J. A. Conner, D. T. Morishige, L. D. Moore, J. E. Mullet, and P. Ozias-Akins (2006)
Plant Physiology 140, 963-971
   Abstract »    Full Text »    PDF »
Novel Surface Display System for Proteins on Non-Genetically Modified Gram-Positive Bacteria.
T. Bosma, R. Kanninga, J. Neef, S. A. L. Audouy, M. L. van Roosmalen, A. Steen, G. Buist, J. Kok, O. P. Kuipers, G. Robillard, et al. (2006)
Appl. Envir. Microbiol. 72, 880-889
   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 »
Transcript Analysis of Early Nodulation Events in Medicago truncatula.
D. P. Lohar, N. Sharopova, G. Endre, S. Penuela, D. Samac, C. Town, K. A.T. Silverstein, and K. A. VandenBosch (2006)
Plant Physiology 140, 221-234
   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 »
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 »
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 »
Grafting between model legumes demonstrates roles for roots and shoots in determining nodule type and host/rhizobia specificity.
D. P. Lohar and K. A. VandenBosch (2005)
J. Exp. Bot. 56, 1643-1650
   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 »
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 »
Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti Involves the Nodulation Factor-Dependent Induction of Root Hairs.
B. Karas, J. Murray, M. Gorzelak, A. Smith, S. Sato, S. Tabata, and K. Szczyglowski (2005)
Plant Physiology 137, 1331-1344
   Abstract »    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 »
Regulation of Plant Symbiosis Receptor Kinase through Serine and Threonine Phosphorylation.
S. Yoshida and M. Parniske (2005)
J. Biol. Chem. 280, 9203-9209
   Abstract »    Full Text »    PDF »
Nitrogen-fixing bacterium Burkholderia brasiliensis produces a novel yersiniose A-containing O-polysaccharide.
K. A. Mattos, A. R. Todeschini, N. Heise, C. Jones, J. O. Previato, and L. Mendonca-Previato (2005)
Glycobiology 15, 313-321
   Abstract »    Full Text »    PDF »
The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots.
V. Fehlberg, M. F. Vieweg, E. M. N. Dohmann, N. Hohnjec, A. Puhler, A. M. Perlick, and H. Kuster (2005)
J. Exp. Bot. 56, 799-806
   Abstract »    Full Text »    PDF »
TRANSPARENT LEAF AREA1 Encodes a Secreted Proteolipid Required for Anther Maturation, Morphogenesis, and Differentiation during Leaf Development in Maize.
T. Dresselhaus, S. Amien, M. Marton, A. Strecke, R. Brettschneider, and S. Cordts (2005)
PLANT CELL 17, 730-745
   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 »
nip, a Symbiotic Medicago truncatula Mutant That Forms Root Nodules with Aberrant Infection Threads and Plant Defense-Like Response.
H. Veereshlingam, J. G. Haynes, R. V. Penmetsa, D. R. Cook, D. J. Sherrier, and R. Dickstein (2004)
Plant Physiology 136, 3692-3702
   Abstract »    Full Text »    PDF »
Endocytosis, Actin Cytoskeleton, and Signaling.
J. Samaj, F. Baluska, B. Voigt, M. Schlicht, D. Volkmann, and D. Menzel (2004)
Plant Physiology 135, 1150-1161
   Full Text »    PDF »
Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes.
D. J. Gage (2004)
Microbiol. Mol. Biol. Rev. 68, 280-300
   Abstract »    Full Text »    PDF »
RNA interference in Agrobacterium rhizogenes-transformed roots of Arabidopsis and Medicago truncatula.
E. Limpens, J. Ramos, C. Franken, V. Raz, B. Compaan, H. Franssen, T. Bisseling, and R. Geurts (2004)
J. Exp. Bot. 55, 983-992
   Abstract »    Full Text »    PDF »
Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice.
S.-H. Shiu, W. M. Karlowski, R. Pan, Y.-H. Tzeng, K. F. X. Mayer, and W.-H. Li (2004)
PLANT CELL 16, 1220-1234
   Abstract »    Full Text »    PDF »
Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation.
S. Goormachtig, W. Capoen, E. K. James, and M. Holsters (2004)
PNAS 101, 6303-6308
   Abstract »    Full Text »    PDF »
A Nonsymbiotic Root Hair Tip Growth Phenotype in NORK-Mutated Legumes: Implications for Nodulation Factor-Induced Signaling and Formation of a Multifaceted Root Hair Pocket for Bacteria.
J. J. Esseling, F. G.P. Lhuissier, and A. M. C. Emons (2004)
PLANT CELL 16, 933-944
   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 »
A Sequence-Based Genetic Map of Medicago truncatula and Comparison of Marker Colinearity with M. sativa.
H.-K. Choi, D. Kim, T. Uhm, E. Limpens, H. Lim, J.-H. Mun, P. Kalo, R. V. Penmetsa, A. Seres, O. Kulikova, et al. (2004)
Genetics 166, 1463-1502
   Abstract »    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 »
A Putative Ca2+ and Calmodulin-Dependent Protein Kinase Required for Bacterial and Fungal Symbioses.
J. Levy, C. Bres, R. Geurts, B. Chalhoub, O. Kulikova, G. Duc, E.-P. Journet, J.-M. Ane, E. Lauber, T. Bisseling, et al. (2004)
Science 303, 1361-1364
   Abstract »    Full Text »    PDF »


ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products

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