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Microbiology and Molecular Biology Reviews, March 2000, p. 180-201, Vol. 64, No. 1
1092-2172/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Molecular Basis of Symbiotic Promiscuity
Xavier
Perret,1
Christian
Staehelin,2 and
William J.
Broughton1,*
Laboratoire de Biologie Moléculaire des
Plantes Supérieures, Université de Genève, 1292 Chambésy/Geneva,1 and
Botanisches Institut der Universität, 4056 Basel,2 Switzerland
Eukaryotes often form symbioses with microorganisms. Among these, associations between plants and nitrogen-fixing bacteria are responsible for the nitrogen input into various ecological niches. Plants of many different families have evolved the capacity to develop root or stem nodules with diverse genera of soil bacteria. Of these, symbioses between legumes and rhizobia (Azorhizobium, Bradyrhizobium, Mesorhizobium, and Rhizobium) are the most important from an agricultural perspective. Nitrogen-fixing nodules arise when symbiotic rhizobia penetrate their hosts in a strictly controlled and coordinated manner. Molecular codes are exchanged between the symbionts in the rhizosphere to select compatible rhizobia from pathogens. Entry into the plant is restricted to bacteria that have the "keys" to a succession of legume "doors". Some symbionts intimately associate with many different partners (and are thus promiscuous), while others are more selective and have a narrow host range. For historical reasons, narrow host range has been more intensively investigated than promiscuity. In our view, this has given a false impression of specificity in legume-Rhizobium associations. Rather, we suggest that restricted host ranges are limited to specific niches and represent specialization of widespread and more ancestral promiscuous symbioses. Here we analyze the molecular mechanisms governing symbiotic promiscuity in rhizobia and show that it is controlled by a number of molecular keys.
*
Corresponding author. Mailing address: LBMPS,
Université de Genève, 1 ch. de l'Impératrice, 1292 Chambésy/Geneva, Switzerland. Phone: 41 (22) 906-1740. Fax: 41 (22) 906-1741. E-mail: broughtw{at}sc2a.unige.ch.
Microbiology and Molecular Biology Reviews, March 2000, p. 180-201, Vol. 64, No. 1
1092-2172/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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-
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[Full Text]
-
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-
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[Full Text]
-
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[Abstract]
[Full Text]
-
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[Full Text]
-
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[Full Text]
-
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-
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[Abstract]
[Full Text]
-
Ausmees, N., Kobayashi, H., Deakin, W. J., Marie, C., Krishnan, H. B., Broughton, W. J., Perret, X.
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[Abstract]
[Full Text]
-
Bartsev, A. V., Deakin, W. J., Boukli, N. M., McAlvin, C. B., Stacey, G., Malnoe, P., Broughton, W. J., Staehelin, C.
(2004). NopL, an Effector Protein of Rhizobium sp. NGR234, Thwarts Activation of Plant Defense Reactions. Plant Physiol.
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
Gonzalez, J. E., Marketon, M. M.
(2003). Quorum Sensing in Nitrogen-Fixing Rhizobia. Microbiol. Mol. Biol. Rev.
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[Abstract]
[Full Text]
-
D'Haeze, W., De Rycke, R., Mathis, R., Goormachtig, S., Pagnotta, S., Verplancke, C., Capoen, W., Holsters, M.
(2003). Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. Proc. Natl. Acad. Sci. USA
100: 11789-11794
[Abstract]
[Full Text]
-
Broughton, W. J.
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185: 2975-2979
[Full Text]
-
Catford, J.-G., Staehelin, C., Lerat, S., Piche, Y., Vierheilig, H.
(2003). Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot
54: 1481-1487
[Abstract]
[Full Text]
-
He, X., Chang, W., Pierce, D. L., Seib, L. O., Wagner, J., Fuqua, C.
(2003). Quorum Sensing in Rhizobium sp. Strain NGR234 Regulates Conjugal Transfer (tra) Gene Expression and Influences Growth Rate. J. Bacteriol.
185: 809-822
[Abstract]
[Full Text]
-
Hattori, Y., Omori, H., Hanyu, M., Kaseda, N., Mishima, E., Kaneko, T., Tabata, S., Saeki, K.
(2002). Ordered Cosmid Library of the Mesorhizobium loti MAFF303099 Genome for Systematic Gene Disruption and Complementation Analysis. Plant Cell Physiol
43: 1542-1557
[Abstract]
[Full Text]
-
Sullivan, J. T., Trzebiatowski, J. R., Cruickshank, R. W., Gouzy, J., Brown, S. D., Elliot, R. M., Fleetwood, D. J., McCallum, N. G., Rossbach, U., Stuart, G. S., Weaver, J. E., Webby, R. J., de Bruijn, F. J., Ronson, C. W.
(2002). Comparative Sequence Analysis of the Symbiosis Island of Mesorhizobium loti Strain R7A. J. Bacteriol.
184: 3086-3095
[Abstract]
[Full Text]
-
D'Haeze, W., Holsters, M.
(2002). Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology
12: 79R-105R
[Abstract]
[Full Text]
-
Bruns, T. D., Bidartondo, M. I., Taylor, D. L.
(2002). Host Specificity in Ectomycorrhizal Communities: What Do the Exceptions Tell Us?. Integr. Comp. Biol.
42: 352-359
[Abstract]
[Full Text]
-
Simms, E. L., Taylor, D. L.
(2002). Partner Choice in Nitrogen-Fixation Mutualisms of Legumes and Rhizobia. Integr. Comp. Biol.
42: 369-380
[Abstract]
[Full Text]
-
Staehelin, C., Charon, C., Boller, T., Crespi, M., Kondorosi, A.
(2001). Medicago truncatula plants overexpressing the early nodulin gene enod40 exhibit accelerated mycorrhizal colonization and enhanced formation of arbuscules. Proc. Natl. Acad. Sci. USA
98: 15366-15371
[Abstract]
[Full Text]
-
Chazalet, V., Uehara, K., Geremia, R. A., Breton, C.
(2001). Identification of Essential Amino Acids in the Azorhizobium caulinodans Fucosyltransferase NodZ. J. Bacteriol.
183: 7067-7075
[Abstract]
[Full Text]
-
Hirsch, A. M., Lum, M. R., Downie, J. A.
(2001). What Makes the Rhizobia-Legume Symbiosis So Special?. Plant Physiol.
127: 1484-1492
[Full Text]
-
Elbeltagy, A., Nishioka, K., Sato, T., Suzuki, H., Ye, B., Hamada, T., Isawa, T., Mitsui, H., Minamisawa, K.
(2001). Endophytic Colonization and In Planta Nitrogen Fixation by a Herbaspirillum sp. Isolated from Wild Rice Species. Appl. Environ. Microbiol.
67: 5285-5293
[Abstract]
[Full Text]
-
Galibert, F., Finan, T. M., Long, S. R., Puhler, A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A., Boistard, P., Bothe, G., Boutry, M., Bowser, L., Buhrmester, J., Cadieu, E., Capela, D., Chain, P., Cowie, A., Davis, R. W., Dreano, S., Federspiel, N. A., Fisher, R. F., Gloux, S., Godrie, T., Goffeau, A., Golding, B., Gouzy, J., Gurjal, M., Hernandez-Lucas, I., Hong, A., Huizar, L., Hyman, R. W., Jones, T., Kahn, D., Kahn, M. L., Kalman, S., Keating, D. H., Kiss, E., Komp, C., Lelaure, V., Masuy, D., Palm, C., Peck, M. C., Pohl, T. M, Portetelle, D., Purnelle, B., Ramsperger, U., Surzycki, R., Thebault, P., Vandenbol, M., Vorholter, F.-J., Weidner, S., Wells, D. H., Wong, K., Yeh, K.-C., Batut, J.
(2001). The Composite Genome of the Legume Symbiont Sinorhizobium meliloti. Science
293: 668-672
[Abstract]
[Full Text]
-
Rogel, M. A., Hernandez-Lucas, I., Kuykendall, L. D., Balkwill, D. L., Martinez-Romero, E.
(2001). Nitrogen-Fixing Nodules with Ensifer adhaerens Harboring Rhizobium tropici Symbiotic Plasmids. Appl. Environ. Microbiol.
67: 3264-3268
[Abstract]
[Full Text]
-
Poinsot, V., Belanger, E., Laberge, S., Yang, G.-P., Antoun, H., Cloutier, J., Treilhou, M., Denarie, J., Prome, J.-C., Debelle, F.
(2001). Unusual Methyl-Branched {alpha},{beta}-Unsaturated Acyl Chain Substitutions in the Nod Factors of an Arctic Rhizobium, Mesorhizobium sp. Strain N33 (Oxytropis arctobia). J. Bacteriol.
183: 3721-3728
[Abstract]
[Full Text]
-
Hooper, L. V., Gordon, J. I.
(2001). Commensal Host-Bacterial Relationships in the Gut. Science
292: 1115-1118
[Abstract]
[Full Text]
-
Laguerre, G., Nour, S. M., Macheret, V., Sanjuan, J., Drouin, P., Amarger, N.
(2001). Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology
147: 981-993
[Abstract]
[Full Text]
-
Fales, L., Kryszak, L., Zeilstra-Ryalls, J.
(2001). Control of hemA Expression in Rhodobacter sphaeroides 2.4.1: Effect of a Transposon Insertion in the hbdA Gene. J. Bacteriol.
183: 1568-1576
[Abstract]
[Full Text]
-
Ulrich, A., Zaspel, I.
(2000). Phylogenetic diversity of rhizobial strains nodulating Robinia pseudoacacia L.. Microbiology
146: 2997-3005
[Abstract]
[Full Text]
-
Broughton, W. J., Jabbouri, S., Perret, X.
(2000). Keys to Symbiotic Harmony. J. Bacteriol.
182: 5641-5652
[Full Text]