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Science 302 (5645): 630-633

Copyright © 2003 by the American Association for the Advancement of Science

LysM Domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection

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

Abstract: 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}

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Plant Physiology 143, 1293-1305
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J. D. Murray, B. J. Karas, S. Sato, S. Tabata, L. Amyot, and K. Szczyglowski (2007)
Science 315, 101-104
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J. Bacteriol. 188, 7731-7741
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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)
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K. Shimomura, M. Nomura, S. Tajima, and H. Kouchi (2006)
Plant Cell Physiol. 47, 1572-1581
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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
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The Medicago truncatula Lysine Motif-Receptor-Like Kinase Gene Family Includes NFP and New Nodule-Expressed Genes.
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Plant Physiology 142, 265-279
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Genetics 172, 2541-2555
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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
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A sulfated metabolite produced by stf3 negatively regulates the virulence of Mycobacterium tuberculosis..
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Plant Physiology 140, 963-971
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Novel Surface Display System for Proteins on Non-Genetically Modified Gram-Positive Bacteria.
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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
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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
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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
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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
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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
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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
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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 »

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