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 315 (5808): 104-107

Copyright © 2007 by the American Association for the Advancement of Science

A Gain-of-Function Mutation in a Cytokinin Receptor Triggers Spontaneous Root Nodule Organogenesis

Leïla Tirichine,1 Niels Sandal,1 Lene H. Madsen,1 Simona Radutoiu,1 Anita S. Albrektsen,1 Shusei Sato,2 Erika Asamizu,2 Satoshi Tabata,2 Jens Stougaard1*

Abstract: Legume root nodules originate from differentiated cortical cells that reenter the cell cycle and form organ primordia. We show that perception of the phytohormone cytokinin is a key element in this switch. Mutation of a Lotus japonicus cytokinin receptor gene leads to spontaneous development of root nodules in the absence of rhizobia or rhizobial signal molecules. The mutant histidine kinase receptor has cytokinin-independent activity and activates an Escherichia coli two-component phosphorelay system in vivo. Mutant analysis shows that cytokinin signaling is required for cell divisions that initiate nodule development and defines an autoregulated process where cytokinin induction of nodule stem cells is controlled by shoots.

1 Laboratory of Gene Expression, Department of Molecular Biology, University of Aarhus, Gustav Wieds Vej 10, DK-8000 Aarhus C, Denmark.
2 Kazusa DNA Research Institute, Kisarazu, Chiba, 292-0818, Japan.

* To whom correspondence should be addressed. E-mail: stougaard{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 »
The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection.
P. Laporte, A. Lepage, J. Fournier, O. Catrice, S. Moreau, M.-F. Jardinaud, J.-H. Mun, E. Larrainzar, D. R. Cook, P. Gamas, et al. (2014)
J. Exp. Bot. 65, 481-494
   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 »
Knockdown of LjIPT3 influences nodule development in Lotus japonicus.
Y. Chen, W. Chen, X. Li, H. Jiang, P. Wu, K. Xia, Y. Yang, and G. Wu (2014)
Plant Cell Physiol.
   Abstract »    Full Text »    PDF »
Comparative Genomics Suggests That an Ancestral Polyploidy Event Leads to Enhanced Root Nodule Symbiosis in the Papilionoideae.
Q.-G. Li, L. Zhang, C. Li, J. M. Dunwell, and Y.-M. Zhang (2013)
Mol. Biol. Evol. 30, 2602-2611
   Abstract »    Full Text »    PDF »
Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system.
S. Okazaki, T. Kaneko, S. Sato, and K. Saeki (2013)
PNAS 110, 17131-17136
   Abstract »    Full Text »    PDF »
Ectopic Expression of miR160 Results in Auxin Hypersensitivity, Cytokinin Hyposensitivity, and Inhibition of Symbiotic Nodule Development in Soybean.
M. Turner, N. R. Nizampatnam, M. Baron, S. Coppin, S. Damodaran, S. Adhikari, S. P. Arunachalam, O. Yu, and S. Subramanian (2013)
Plant Physiology 162, 2042-2055
   Abstract »    Full Text »    PDF »
Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins.
E. Foo, J. J. Ross, W. T. Jones, and J. B. Reid (2013)
Ann. Bot. 111, 769-779
   Abstract »    Full Text »    PDF »
Rhizobial Infection Is Associated with the Development of Peripheral Vasculature in Nodules of Medicago truncatula.
D. Guan, N. Stacey, C. Liu, J. Wen, K. S. Mysore, I. Torres-Jerez, T. Vernie, M. Tadege, C. Zhou, Z.-y. Wang, et al. (2013)
Plant Physiology 162, 107-115
   Abstract »    Full Text »    PDF »
TOO MUCH LOVE, a Novel Kelch Repeat-Containing F-box Protein, Functions in the Long-Distance Regulation of the Legume-Rhizobium Symbiosis.
M. Takahara, S. Magori, T. Soyano, S. Okamoto, C. Yoshida, K. Yano, S. Sato, S. Tabata, K. Yamaguchi, S. Shigenobu, et al. (2013)
Plant Cell Physiol. 54, 433-447
   Abstract »    Full Text »    PDF »
Down-Regulation of NSP2 Expression in Developmentally Young Regions of Lotus japonicus Roots in Response to Rhizobial Inoculation.
Y. Murakami, H. Yokoyama, R. Fukui, and M. Kawaguchi (2013)
Plant Cell Physiol. 54, 518-527
   Abstract »    Full Text »    PDF »
TRICOT encodes an AMP1-related carboxypeptidase that regulates root nodule development and shoot apical meristem maintenance in Lotus japonicus.
T. Suzaki, C. S. Kim, N. Takeda, K. Szczyglowski, and M. Kawaguchi (2013)
Development 140, 353-361
   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 »
Two MicroRNAs Linked to Nodule Infection and Nitrogen-Fixing Ability in the Legume Lotus japonicus.
A. De Luis, K. Markmann, V. Cognat, D. B. Holt, M. Charpentier, M. Parniske, J. Stougaard, and O. Voinnet (2012)
Plant Physiology 160, 2137-2154
   Abstract »    Full Text »    PDF »
Effects of Engineered Sinorhizobium meliloti on Cytokinin Synthesis and Tolerance of Alfalfa to Extreme Drought Stress.
J. Xu, X.-L. Li, and L. Luo (2012)
Appl. Envir. Microbiol. 78, 8056-8061
   Abstract »    Full Text »    PDF »
Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response.
T. Suzaki, K. Yano, M. Ito, Y. Umehara, N. Suganuma, and M. Kawaguchi (2012)
Development 139, 3997-4006
   Abstract »    Full Text »    PDF »
Lotus japonicus ARPC1 Is Required for Rhizobial Infection.
M. S. Hossain, J. Liao, E. K. James, S. Sato, S. Tabata, A. Jurkiewicz, L. H. Madsen, J. Stougaard, L. Ross, and K. Szczyglowski (2012)
Plant Physiology 160, 917-928
   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 »
Two Direct Targets of Cytokinin Signaling Regulate Symbiotic Nodulation in Medicago truncatula.
F. Ariel, M. Brault-Hernandez, C. Laffont, E. Huault, M. Brault, J. Plet, M. Moison, S. Blanchet, J. L. Ichante, M. Chabaud, et al. (2012)
PLANT CELL 24, 3838-3852
   Abstract »    Full Text »    PDF »
Agrobacterium tumefaciens Tumor Morphology Root Plastid Localization and Preferential Usage of Hydroxylated Prenyl Donor Is Important for Efficient Gall Formation.
N. Ueda, M. Kojima, K. Suzuki, and H. Sakakibara (2012)
Plant Physiology 159, 1064-1072
   Abstract »    Full Text »    PDF »
Thiol synthetases of legumes: immunogold localization and differential gene regulation by phytohormones.
M. R. Clemente, P. Bustos-Sanmamed, J. Loscos, E. K. James, C. Perez-Rontome, J. Navascues, M. Gay, and M. Becana (2012)
J. Exp. Bot. 63, 3923-3934
   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 »
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 »
Molecular mechanisms controlling legume autoregulation of nodulation.
D. E. Reid, B. J. Ferguson, S. Hayashi, Y.-H. Lin, and P. M. Gresshoff (2011)
Ann. Bot. 108, 789-795
   Abstract »    Full Text »    PDF »
Soybean Nodule-Enhanced CLE Peptides in Roots Act as Signals in GmNARK-Mediated Nodulation Suppression.
C. W. Lim, Y. W. Lee, and C. H. Hwang (2011)
Plant Cell Physiol. 52, 1613-1627
   Abstract »    Full Text »    PDF »
Search for nodulation-related CLE genes in the genome of Glycine max.
V. Mortier, B. A. Fenta, C. Martens, S. Rombauts, M. Holsters, K. Kunert, and S. Goormachtig (2011)
J. Exp. Bot. 62, 2571-2583
   Abstract »    Full Text »    PDF »
The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus.
H. Miyazawa, E. Oka-Kira, N. Sato, H. Takahashi, G.-J. Wu, S. Sato, M. Hayashi, S. Betsuyaku, M. Nakazono, S. Tabata, et al. (2010)
Development 137, 4317-4325
   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 »
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 »
CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically.
V. Mortier, G. Den Herder, R. Whitford, W. Van de Velde, S. Rombauts, K. D'haeseleer, M. Holsters, and S. Goormachtig (2010)
Plant Physiology 153, 222-237
   Abstract »    Full Text »    PDF »
Enhanced Nodulation and Nitrogen Fixation in the Abscisic Acid Low-Sensitive Mutant enhanced nitrogen fixation1 of Lotus japonicus.
A. Tominaga, M. Nagata, K. Futsuki, H. Abe, T. Uchiumi, M. Abe, K.-i. Kucho, M. Hashiguchi, R. Akashi, A. M. Hirsch, et al. (2009)
Plant Physiology 151, 1965-1976
   Abstract »    Full Text »    PDF »
A Small GTPase of the Rab Family Is Required for Root Hair Formation and Preinfection Stages of the Common Bean-Rhizobium Symbiotic Association.
F. A. Blanco, E. Peltzer Meschini, M. E. Zanetti, and O. M. Aguilar (2009)
PLANT CELL 21, 2797-2810
   Abstract »    Full Text »    PDF »
A Genome-Wide Compilation of the Two-Component Systems in Lotus japonicus.
K. Ishida, Y. Niwa, T. Yamashino, and T. Mizuno (2009)
DNA Res 16, 237-247
   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 »
The Temperature-Sensitive brush Mutant of the Legume Lotus japonicus Reveals a Link between Root Development and Nodule Infection by Rhizobia.
M. Maekawa-Yoshikawa, J. Muller, N. Takeda, T. Maekawa, S. Sato, S. Tabata, J. Perry, T. L. Wang, M. Groth, A. Brachmann, et al. (2009)
Plant Physiology 149, 1785-1796
   Abstract »    Full Text »    PDF »
Roles for Auxin, Cytokinin, and Strigolactone in Regulating Shoot Branching.
B. J. Ferguson and C. A. Beveridge (2009)
Plant Physiology 149, 1929-1944
   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 »
An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses.
S. Slavikova, S. Ufaz, T. Avin-Wittenberg, H. Levanony, and G. Galili (2008)
J. Exp. Bot.
   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 »
EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation in Medicago truncatula.
T. Vernie, S. Moreau, F. de Billy, J. Plet, J.-P. Combier, C. Rogers, G. Oldroyd, F. Frugier, A. Niebel, and P. Gamas (2008)
PLANT CELL 20, 2696-2713
   Abstract »    Full Text »    PDF »
Genome Structure of the Legume, Lotus japonicus.
S. Sato, Y. Nakamura, T. Kaneko, E. Asamizu, T. Kato, M. Nakao, S. Sasamoto, A. Watanabe, A. Ono, K. Kawashima, et al. (2008)
DNA Res 15, 227-239
   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 »
PLANT SCIENCE: Infectious Heresy.
J. A. Downie (2007)
Science 316, 1296-1297
   Abstract »    Full Text »    PDF »
Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia.
E. Giraud, L. Moulin, D. Vallenet, V. Barbe, E. Cytryn, J.-C. Avarre, M. Jaubert, D. Simon, F. Cartieaux, Y. Prin, et al. (2007)
Science 316, 1307-1312
   Abstract »    Full Text »    PDF »
Overlap of Proteome Changes in Medicago truncatula in Response to Auxin and Sinorhizobium meliloti.
G. E. van Noorden, T. Kerim, N. Goffard, R. Wiblin, F. I. Pellerone, B. G. Rolfe, and U. Mathesius (2007)
Plant Physiology 144, 1115-1131
   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 »
PLANT SCIENCE: Nodules and Hormones.
G. E. D. Oldroyd (2007)
Science 315, 52-53
   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 »

To Advertise     Find Products

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