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Science 17 June 2005:
Vol. 308. no. 5729, pp. 1786 - 1789
DOI: 10.1126/science.1110951
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Reports

Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators

Péter Kaló,1,2 Cynthia Gleason,1 Anne Edwards,1 John Marsh,1 Raka M. Mitra,4* Sibylle Hirsch,1 Júlia Jakab,2 Sarah Sims,3 Sharon R. Long,4 Jane Rogers,3 György B. Kiss,2 J. Allan Downie,1 Giles E. D. Oldroyd1{dagger}

Rhizobial bacteria enter a symbiotic interaction with legumes, activating diverse responses in roots through the lipochito oligosaccharide signaling molecule Nod factor. Here, we show that NSP2 from Medicago truncatula encodes a GRAS protein essential for Nod-factor signaling. NSP2 functions downstream of Nod-factor–induced calcium spiking and a calcium/calmodulin-dependent protein kinase. We show that NSP2-GFP expressed from a constitutive promoter is localized to the endoplasmic reticulum/nuclear envelope and relocalizes to the nucleus after Nod-factor elicitation. This work provides evidence that a GRAS protein transduces calcium signals in plants and provides a possible regulator of Nod-factor–inducible gene expression.

1 Departments of Disease and Stress Biology and Molecular Microbiology, John Innes Centre, Norwich NR4 7UH, UK.
2 Institute of Genetics, Agricultural Biotechnology Center, Szent-Györgyi A. utca 4, 2100 Gödöllö, Hungary.
3 Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
4 Department of Biological Sciences, Stanford University, Stanford, CA 94305, USA.

* Present address: Department of Plant Biology, University of Minnesota, St. Paul, MN 55108, USA.

{dagger} To whom correspondence should be addressed. E-mail: giles.oldroyd{at}bbsrc.ac.uk

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THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
GRAS Proteins Form a DNA Binding Complex to Induce Gene Expression during Nodulation Signaling in Medicago truncatula.
S. Hirsch, J. Kim, A. Munoz, A. B. Heckmann, J. A. Downie, and G. E.D. Oldroyd (2009)
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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)
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How CYCLOPS keeps an eye on plant symbiosis.
W. Capoen and G. Oldroyd (2008)
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De Novo Organ Formation from Differentiated Cells: Root Nodule Organogenesis.
M. Crespi and F. Frugier (2008)
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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
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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)
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A Positive Regulatory Role for LjERF1 in the Nodulation Process Is Revealed by Systematic Analysis of Nodule-Associated Transcription Factors of Lotus japonicus.
E. Asamizu, Y. Shimoda, H. Kouchi, S. Tabata, and S. Sato (2008)
Plant Physiology 147, 2030-2040
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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
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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
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AP2-ERF Transcription Factors Mediate Nod Factor Dependent Mt ENOD11 Activation in Root Hairs via a Novel cis-Regulatory Motif.
A. Andriankaja, A. Boisson-Dernier, L. Frances, L. Sauviac, A. Jauneau, D. G. Barker, and F. de Carvalho-Niebel (2007)
PLANT CELL 19, 2866-2885
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Comparative Transcriptome Analysis Reveals Common and Specific Tags for Root Hair and Crack-Entry Invasion in Sesbania rostrata.
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Legume Transcription Factors: Global Regulators of Plant Development and Response to the Environment.
M. K. Udvardi, K. Kakar, M. Wandrey, O. Montanari, J. Murray, A. Andriankaja, J.-Y. Zhang, V. Benedito, J. M.I. Hofer, F. Chueng, et al. (2007)
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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
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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
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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
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NUCLEOPORIN85 Is Required for Calcium Spiking, Fungal and Bacterial Symbioses, and Seed Production in Lotus japonicus.
K. Saito, M. Yoshikawa, K. Yano, H. Miwa, H. Uchida, E. Asamizu, S. Sato, S. Tabata, H. Imaizumi-Anraku, Y. Umehara, et al. (2007)
PLANT CELL 19, 610-624
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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
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Lotus japonicus Nodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume.
A. B. Heckmann, F. Lombardo, H. Miwa, J. A. Perry, S. Bunnewell, M. Parniske, T. L. Wang, and J. A. Downie (2006)
Plant Physiology 142, 1739-1750
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The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti.
S. Gonzalez-Rizzo, M. Crespi, and F. Frugier (2006)
PLANT CELL 18, 2680-2693
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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 »
Nitrogen Fixation Mutants of Medicago truncatula Fail to Support Plant and Bacterial Symbiotic Gene Expression.
C. G. Starker, A. L. Parra-Colmenares, L. Smith, R. M. Mitra, and S. R. Long (2006)
Plant Physiology 140, 671-680
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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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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 »


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