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): 101-104

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

A Cytokinin Perception Mutant Colonized by Rhizobium in the Absence of Nodule Organogenesis

Jeremy D. Murray,1 Bogumil J. Karas,1 Shusei Sato,2 Satoshi Tabata,2 Lisa Amyot,1 Krzysztof Szczyglowski1*

Abstract: In legumes, Nod-factor signaling by rhizobia initiates the development of the nitrogen-fixing nodule symbiosis, but the direct cell division stimulus that brings about nodule primordia inception in the root cortex remains obscure. We showed that Lotus japonicus plants homozygous for a mutation in the HYPERINFECTED 1 (HIT1) locus exhibit abundant infection-thread formation but fail to initiate timely cortical cell divisions in response to rhizobial signaling. We demonstrated that the corresponding gene encodes a cytokinin receptor that is required for the activation of the nodule inception regulator Nin and nodule organogenesis.

1 Agriculture and Agri-Food Canada, Southern Crop Protection and Food Research Centre, 1391 Sandford Street, London, Ontario N5V 4T3, Canada.
2 Kazusa DNA Research Institute, Kisarazu, Chiba, 292-0812, Japan.

* To whom correspondence should be addressed. E-mail: szczyglowskik{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 »
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 »
Photosynthetic Bradyrhizobium sp. Strain ORS285 Is Capable of Forming Nitrogen-Fixing Root Nodules on Soybeans (Glycine max).
E. Giraud, L. Xu, C. Chaintreuil, D. Gargani, D. Gully, and M. J. Sadowsky (2013)
Appl. Envir. Microbiol. 79, 2459-2462
   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 »
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 »
A Phaseolus vulgaris NADPH Oxidase Gene is Required for Root Infection by Rhizobia.
J. Montiel, N. Nava, L. Cardenas, R. Sanchez-Lopez, M.-K. Arthikala, O. Santana, F. Sanchez, and C. Quinto (2012)
Plant Cell Physiol. 53, 1751-1767
   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 »
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 »
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 »
Plant-activated bacterial receptor adenylate cyclases modulate epidermal infection in the Sinorhizobium meliloti-Medicago symbiosis.
C. F. Tian, A.-M. Garnerone, C. Mathieu-Demaziere, C. Masson-Boivin, and J. Batut (2012)
PNAS 109, 6751-6756
   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 »
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 »
The ROOT DETERMINED NODULATION1 Gene Regulates Nodule Number in Roots of Medicago truncatula and Defines a Highly Conserved, Uncharacterized Plant Gene Family.
E. L. Schnabel, T. K. Kassaw, L. S. Smith, J. F. Marsh, G. E. Oldroyd, S. R. Long, and J. A. Frugoli (2011)
Plant Physiology 157, 328-340
   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 »
Genomic Inventory and Transcriptional Analysis of Medicago truncatula Transporters.
V. A. Benedito, H. Li, X. Dai, M. Wandrey, J. He, R. Kaundal, I. Torres-Jerez, S. K. Gomez, M. J. Harrison, Y. Tang, et al. (2010)
Plant Physiology 152, 1716-1730
   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 »
Legume Transcription Factor Genes: What Makes Legumes So Special?.
M. Libault, T. Joshi, V. A. Benedito, D. Xu, M. K. Udvardi, and G. Stacey (2009)
Plant Physiology 151, 991-1001
   Full Text »    PDF »
Conservation of Lotus and Arabidopsis Basic Helix-Loop-Helix Proteins Reveals New Players in Root Hair Development.
B. Karas, L. Amyot, C. Johansen, S. Sato, S. Tabata, M. Kawaguchi, and K. Szczyglowski (2009)
Plant Physiology 151, 1175-1185
   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 »
The Cytokinin Type-B Response Regulator PtRR13 Is a Negative Regulator of Adventitious Root Development in Populus.
G. A. Ramirez-Carvajal, A. M. Morse, C. Dervinis, and J. M. Davis (2009)
Plant Physiology 150, 759-771
   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 »
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 »
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 Gain-of-Function Mutation in a Cytokinin Receptor Triggers Spontaneous Root Nodule Organogenesis.
L. Tirichine, N. Sandal, L. H. Madsen, S. Radutoiu, A. S. Albrektsen, S. Sato, E. Asamizu, S. Tabata, and J. Stougaard (2007)
Science 315, 104-107
   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