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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}mb.au.dk


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   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)
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   Abstract »    Full Text »    PDF »
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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 »
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G. E. van Noorden, T. Kerim, N. Goffard, R. Wiblin, F. I. Pellerone, B. G. Rolfe, and U. Mathesius (2007)
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   Abstract »    Full Text »    PDF »
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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 »

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