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Science 24 January 1997:
Vol. 275. no. 5299, pp. 527 - 530
DOI: 10.1126/science.275.5299.527
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Reports

A Legume Ethylene-Insensitive Mutant Hyperinfected by Its Rhizobial Symbiont

R. Varma Penmetsa and Douglas R. Cook *

Development of the Rhizobium-legume symbiosis is controlled by the host plant, although the underlying mechanisms have remained obscure. A mutant in the annual legume Medicago truncatula exhibits an increase of more than an order of magnitude in the number of persistent rhizobial infections. Physiological and genetic analyses indicate that this same mutation confers insensitivity to the plant hormone ethylene for multiple aspects of plant development, including nodulation. These data support the hypothesis that ethylene is a component of the signaling pathway controlling rhizobial infection of legumes.

Department of Plant Pathology and Microbiology, Crop Biotechnology Center, and Graduate Program in Genetics, Texas A&M University, College Station, TX 77843, USA.
*   To whom correspondence should be addressed.

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Expression Islands Clustered on the Symbiosis Island of the Mesorhizobium loti Genome.
T. Uchiumi, T. Ohwada, M. Itakura, H. Mitsui, N. Nukui, P. Dawadi, T. Kaneko, S. Tabata, T. Yokoyama, K. Tejima, et al. (2004)
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J. J. Esseling, F. G.P. Lhuissier, and A. M. C. Emons (2004)
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Unraveling the mystery of Nod factor signaling by a genomic approach in Medicago trunactula.
D. R. Cook (2004)
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A Sequence-Based Genetic Map of Medicago truncatula and Comparison of Marker Colinearity with M. sativa.
H.-K. Choi, D. Kim, T. Uhm, E. Limpens, H. Lim, J.-H. Mun, P. Kalo, R. V. Penmetsa, A. Seres, O. Kulikova, et al. (2004)
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Plant and Bacterial Symbiotic Mutants Define Three Transcriptionally Distinct Stages in the Development of the Medicago truncatula/Sinorhizobium meliloti Symbiosis.
R. M. Mitra and S. R. Long (2004)
Plant Physiology 134, 595-604
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Bradyrhizobium elkanii rtxC Gene Is Required for Expression of Symbiotic Phenotypes in the Final Step of Rhizobitoxine Biosynthesis.
S. Okazaki, M. Sugawara, and K. Minamisawa (2004)
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M.-T. Navarro-Gochicoa, S. Camut, A. C.J. Timmers, A. Niebel, C. Herve, E. Boutet, J.-J. Bono, A. Imberty, and J. V. Cullimore (2003)
Plant Physiology 133, 1893-1910
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A method for the isolation of root hairs from the model legume Medicago truncatula.
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J. Exp. Bot. 54, 2245-2250
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Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume.
W. D'Haeze, R. De Rycke, R. Mathis, S. Goormachtig, S. Pagnotta, C. Verplancke, W. Capoen, and M. Holsters (2003)
PNAS 100, 11789-11794
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Structural motifs in the RNA encoded by the early nodulation gene enod40 of soybean.
G. Girard, A. Roussis, A. P. Gultyaev, C. W. A. Pleij, and H. P. Spaink (2003)
Nucleic Acids Res. 31, 5003-5015
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Rhizobium leguminosarum Biovar viciae 1-Aminocyclopropane-1-Carboxylate Deaminase Promotes Nodulation of Pea Plants.
W. Ma, F. C. Guinel, and B. R. Glick (2003)
Appl. Envir. Microbiol. 69, 4396-4402
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Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors.
J.-G. Catford, C. Staehelin, S. Lerat, Y. Piche, and H. Vierheilig (2003)
J. Exp. Bot. 54, 1481-1487
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Summaries of Legume Genomics Projects from around the Globe. Community Resources for Crops and Models.
K. A. VandenBosch and G. Stacey (2003)
Plant Physiology 131, 840-865
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Nod Factor Elicits Two Separable Calcium Responses in Medicago truncatula Root Hair Cells.
S. L. Shaw and S. R. Long (2003)
Plant Physiology 131, 976-984
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Identification and Characterization of Nodulation-Signaling Pathway 2, a Gene of Medicago truncatula Involved in Nod Factor Signaling.
G. E.D. Oldroyd and S. R. Long (2003)
Plant Physiology 131, 1027-1032
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Expression of the Apyrase-Like APY1 Genes in Roots of Medicago truncatula Is Induced Rapidly and Transiently by Stress and Not by Sinorhizobium meliloti or Nod Factors.
M.-T. Navarro-Gochicoa, S. Camut, A. Niebel, and J. V. Cullimore (2003)
Plant Physiology 131, 1124-1136
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A Diffusible Factor from Arbuscular Mycorrhizal Fungi Induces Symbiosis-Specific MtENOD11 Expression in Roots of Medicago truncatula.
S. Kosuta, M. Chabaud, G. Lougnon, C. Gough, J. Denarie, D. G. Barker, and G. Becard (2003)
Plant Physiology 131, 952-962
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Dual Genetic Pathways Controlling Nodule Number in Medicago truncatula.
R. V. Penmetsa, J. A. Frugoli, L. S. Smith, S. R. Long, and D. R. Cook (2003)
Plant Physiology 131, 998-1008
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M. L. Tansengco, M. Hayashi, M. Kawaguchi, H. Imaizumi-Anraku, and Y. Murooka (2003)
Plant Physiology 131, 1054-1063
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Shedding light on an underground problem.
J. Harris (2002)
PNAS 99, 14616-14618
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R. Nishimura, M. Ohmori, H. Fujita, and M. Kawaguchi (2002)
PNAS 99, 15206-15210
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The Novel Symbiotic Phenotype of Enhanced-Nodulating Mutant of Lotus japonicus: astray Mutant is an Early Nodulating Mutant with Wider Nodulation Zone.
R. Nishimura, M. Ohmori, and M. Kawaguchi (2002)
Plant Cell Physiol. 43, 853-859
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Ethylene Biosynthesis and Signaling Networks.
K. L.-C. Wang, H. Li, and J. R. Ecker (2002)
PLANT CELL 14, S131-151
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Rhizobium Nod Factor Perception and Signalling.
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PLANT CELL 14, S239-249
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Partner Choice in Nitrogen-Fixation Mutualisms of Legumes and Rhizobia.
E. L. Simms and D. L. Taylor (2002)
Integr. Comp. Biol. 42, 369-380
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DNA Sequence and Mutational Analysis of Rhizobitoxine Biosynthesis Genes in Bradyrhizobium elkanii.
T. Yasuta, S. Okazaki, H. Mitsui, K.-I. Yuhashi, H. Ezura, and K. Minamisawa (2001)
Appl. Envir. Microbiol. 67, 4999-5009
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Ethylene Inhibits the Nod Factor Signal Transduction Pathway of Medicago truncatula.
G. E. D. Oldroyd, E. M. Engstrom, and S. R. Long (2001)
PLANT CELL 13, 1835-1849
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Differential Regulation of a Family of Apyrase Genes from Medicago truncatula.
J. R. Cohn, T. Uhm, S. Ramu, Y.-W. Nam, D.-J. Kim, R. V. Penmetsa, T. C. Wood, R. L. Denny, N. D. Young, D. R. Cook, et al. (2001)
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The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling.
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Development 128, 1507-1518
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Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula.
R. J. Wais, C. Galera, G. Oldroyd, R. Catoira, R. V. Penmetsa, D. Cook, C. Gough, J. Dénarié, and S. R. Long (2000)
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Regulators and Regulation of Legume Root Nodule Development.
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Plant Physiology 124, 531-540
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Effects of Ethylene Precursor and Inhibitors for Ethylene Biosynthesis and Perception on Nodulation in Lotus japonicus and Macroptilium atropurpureum.
N. Nukui, H. Ezura, K.-I. Yuhashi, T. Yasuta, and K. Minamisawa (2000)
Plant Cell Physiol. 41, 893-897
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Mtsym6, a Gene Conditioning Sinorhizobium Strain-Specific Nitrogen Fixation in Medicago truncatula.
L. Tirichine, F. de Billy, and T. Huguet (2000)
Plant Physiology 123, 845-852
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Rhizobitoxine Production by Bradyrhizobium elkanii Enhances Nodulation and Competitiveness on Macroptilium atropurpureum.
K.-I. Yuhashi, N. Ichikawa, H. Ezura, S. Akao, Y. Minakawa, N. Nukui, T. Yasuta, and K. Minamisawa (2000)
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Ethylene is involved in the nodulation phenotype of Pisum sativum R50 (sym 16), a pleiotropic mutant that nodulates poorly and has pale green leaves.
F. C. Guinel and L. L. Sloetjes (2000)
J. Exp. Bot. 51, 885-894
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Alteration of enod40 Expression Modifies Medicago truncatula Root Nodule Development Induced by Sinorhizobium meliloti.
C. Charon, C. Sousa, M. Crespi, and A. Kondorosi (1999)
PLANT CELL 11, 1953-1966
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Regulation of Soybean Nodulation Independent of Ethylene Signaling.
J. S. Schmidt, J. E. Harper, T. K. Hoffman, and A. F. Bent (1999)
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New Assay for Rhizobitoxine Based on Inhibition of 1-Aminocyclopropane-1-Carboxylate Synthase.
T. Yasuta, S. Satoh, and K. Minamisawa (1999)
Appl. Envir. Microbiol. 65, 849-852
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Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements.
A. Timmers, M. Auriac, and G Truchet (1999)
Development 126, 3617-3628
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Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1.
R. Solano, A. Stepanova, Q. Chao, and J. R. Ecker (1998)
Genes & Dev. 12, 3703-3714
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Ethylene-mediated phenotypic plasticity in root nodule development on Sesbania rostrata.
M. Fernandez-Lopez, S. Goormachtig, M. Gao, W. D'Haeze, M. Van Montagu, and M. Holsters (1998)
PNAS 95, 12724-12728
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Succinoglycan Is Required for Initiation and Elongation of Infection Threads during Nodulation of Alfalfa by Rhizobium meliloti.
H.-P. Cheng and G. C. Walker (1998)
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Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant.
L. Zhou, J.-c. Jang, T. L. Jones, and J. Sheen (1998)
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EIN4 and ERS2 Are Members of the Putative Ethylene Receptor Gene Family in Arabidopsis.
J. Hua, H. Sakai, S. Nourizadeh, Q. G. Chen, A. B. Bleecker, J. R. Ecker, and E. M. Meyerowitz (1998)
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Expressed Sequence Tags from a Root-Hair-Enriched Medicago truncatula cDNA Library.
P. A. Covitz, L. S. Smith, and S. R. Long (1998)
Plant Physiology 117, 1325-1332
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Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi.
M. Knoester, L. C. van Loon, J. van den Heuvel, J. Hennig, J. F. Bol, and H. J. M. Linthorst (1998)
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   Abstract »    Full Text »    PDF »
Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula.
R. J. Wais, C. Galera, G. Oldroyd, R. Catoira, R. V. Penmetsa, D. Cook, C. Gough, J. Denarie, and S. R. Long (2000)
PNAS 97, 13407-13412
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Science. ISSN 0036-8075 (print), 1095-9203 (online)