This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Cheng, H.-P.
Right arrow Articles by Walker, G. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Cheng, H.-P.
Right arrow Articles by Walker, G. C.

 Previous Article  |  Next Article 

Journal of Bacteriology, October 1998, p. 5183-5191, Vol. 180, No. 19
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Succinoglycan Is Required for Initiation and Elongation of Infection Threads during Nodulation of Alfalfa by Rhizobium meliloti

Hai-Ping Cheng and Graham C. Walker*

Biology Department, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Received 17 April 1998/Accepted 28 July 1998

Rhizobium meliloti Rm1021 must be able to synthesize succinoglycan in order to invade successfully the nodules which it elicits on alfalfa and to establish an effective nitrogen-fixing symbiosis. Using R. meliloti cells that express green fluorescent protein (GFP), we have examined the nature of the symbiotic deficiency of exo mutants that are defective or altered in succinoglycan production. Our observations indicate that an exoY mutant, which does not produce succinoglycan, is symbiotically defective because it cannot initiate the formation of infection threads. An exoZ mutant, which produces succinoglycan without the acetyl modification, forms nitrogen-fixing nodules on plants, but it exhibits a reduced efficiency in the initiation and elongation of infection threads. An exoH mutant, which produces symbiotically nonfunctional high-molecular-weight succinoglycan that lacks the succinyl modification, cannot form extended infection threads. Infection threads initiate at a reduced rate and then abort before they reach the base of the root hairs. Overproduction of succinoglycan by the exoS96::Tn5 mutant does not reduce the efficiency of infection thread initiation and elongation, but it does significantly reduce the ability of this mutant to colonize the curled root hairs, which is the first step of the invasion process. The exoR95::Tn5 mutant, which overproduces succinoglycan to an even greater extent than the exoS96::Tn5 mutant, has completely lost its ability to colonize the curled root hairs. These new observations lead us to propose that succinoglycan is required for both the initiation and elongation of infection threads during nodule invasion and that excess production of succinoglycan interferes with the ability of the rhizobia to colonize curled root hairs.


* Corresponding author. Mailing address: 68-633, Biology Department, Massachusetts Institute of Technology, 77 Massachusetts Ave., Cambridge, MA 02139. Phone: (617) 253-6716. Fax: (617) 253-2643. E-mail: gwalker{at}mit.edu.


Journal of Bacteriology, October 1998, p. 5183-5191, Vol. 180, No. 19
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Rinaudi, L. V., Gonzalez, J. E. (2009). The Low-Molecular-Weight Fraction of Exopolysaccharide II from Sinorhizobium meliloti Is a Crucial Determinant of Biofilm Formation. J. Bacteriol. 191: 7216-7224 [Abstract] [Full Text]  
  • Muller, M. G., Forsberg, L. S., Keating, D. H. (2009). The rkp-1 Cluster Is Required for Secretion of Kdo Homopolymeric Capsular Polysaccharide in Sinorhizobium meliloti Strain Rm1021. J. Bacteriol. 191: 6988-7000 [Abstract] [Full Text]  
  • Chen, E. J., Fisher, R. F., Perovich, V. M., Sabio, E. A., Long, S. R. (2009). Identification of Direct Transcriptional Target Genes of ExoS/ChvI Two-Component Signaling in Sinorhizobium meliloti. J. Bacteriol. 191: 6833-6842 [Abstract] [Full Text]  
  • Morris, J., Gonzalez, J. E. (2009). The Novel Genes emmABC Are Associated with Exopolysaccharide Production, Motility, Stress Adaptation, and Symbiosis in Sinorhizobium meliloti. J. Bacteriol. 191: 5890-5900 [Abstract] [Full Text]  
  • Peleg, A. Y., Jara, S., Monga, D., Eliopoulos, G. M., Moellering, R. C. Jr., Mylonakis, E. (2009). Galleria mellonella as a Model System To Study Acinetobacter baumannii Pathogenesis and Therapeutics. Antimicrob. Agents Chemother. 53: 2605-2609 [Abstract] [Full Text]  
  • Marlow, V. L., Haag, A. F., Kobayashi, H., Fletcher, V., Scocchi, M., Walker, G. C., Ferguson, G. P. (2009). Essential Role for the BacA Protein in the Uptake of a Truncated Eukaryotic Peptide in Sinorhizobium meliloti. J. Bacteriol. 191: 1519-1527 [Abstract] [Full Text]  
  • Pinedo, C. A., Gage, D. J. (2009). HPrK Regulates Succinate-Mediated Catabolite Repression in the Gram-Negative Symbiont Sinorhizobium meliloti. J. Bacteriol. 191: 298-309 [Abstract] [Full Text]  
  • Fournier, J., Timmers, A. C.J., Sieberer, B. J., Jauneau, A., Chabaud, M., Barker, D. G. (2008). Mechanism of Infection Thread Elongation in Root Hairs of Medicago truncatula and Dynamic Interplay with Associated Rhizobial Colonization. Plant Physiol. 148: 1985-1995 [Abstract] [Full Text]  
  • Den Herder, G., De Keyser, A., De Rycke, R., Rombauts, S., Van de Velde, W., Clemente, M. R., Verplancke, C., Mergaert, P., Kondorosi, E., Holsters, M., Goormachtig, S. (2008). Seven in Absentia Proteins Affect Plant Growth and Nodulation in Medicago truncatula. Plant Physiol. 148: 369-382 [Abstract] [Full Text]  
  • McIntosh, M., Krol, E., Becker, A. (2008). Competitive and Cooperative Effects in Quorum-Sensing-Regulated Galactoglucan Biosynthesis in Sinorhizobium meliloti. J. Bacteriol. 190: 5308-5317 [Abstract] [Full Text]  
  • Williams, A., Wilkinson, A., Krehenbrink, M., Russo, D. M., Zorreguieta, A., Downie, J. A. (2008). Glucomannan-Mediated Attachment of Rhizobium leguminosarum to Pea Root Hairs Is Required for Competitive Nodule Infection. J. Bacteriol. 190: 4706-4715 [Abstract] [Full Text]  
  • Pinedo, C. A., Bringhurst, R. M., Gage, D. J. (2008). Sinorhizobium meliloti Mutants Lacking Phosphotransferase System Enzyme HPr or EIIA Are Altered in Diverse Processes, Including Carbon Metabolism, Cobalt Requirements, and Succinoglycan Production. J. Bacteriol. 190: 2947-2956 [Abstract] [Full Text]  
  • Matthysse, A. G., Deora, R., Mishra, M., Torres, A. G. (2008). Polysaccharides Cellulose, Poly-{beta}-1,6-N-Acetyl-D-Glucosamine, and Colanic Acid Are Required for Optimal Binding of Escherichia coli O157:H7 Strains to Alfalfa Sprouts and K-12 Strains to Plastic but Not for Binding to Epithelial Cells. Appl. Environ. Microbiol. 74: 2384-2390 [Abstract] [Full Text]  
  • Jones, K. M., Sharopova, N., Lohar, D. P., Zhang, J. Q., VandenBosch, K. A., Walker, G. C. (2008). Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc. Natl. Acad. Sci. USA 105: 704-709 [Abstract] [Full Text]  
  • Jamet, A., Mandon, K., Puppo, A., Herouart, D. (2007). H2O2 Is Required for Optimal Establishment of the Medicago sativa/Sinorhizobium meliloti Symbiosis. J. Bacteriol. 189: 8741-8745 [Abstract] [Full Text]  
  • Simsek, S., Ojanen-Reuhs, T., Stephens, S. B., Reuhs, B. L. (2007). Strain-Ecotype Specificity in Sinorhizobium meliloti-Medicago truncatula Symbiosis Is Correlated to Succinoglycan Oligosaccharide Structure. J. Bacteriol. 189: 7733-7740 [Abstract] [Full Text]  
  • Perrine-Walker, F. M., Prayitno, J., Rolfe, B. G., Weinman, J. J., Hocart, C. H. (2007). Infection process and the interaction of rice roots with rhizobia. J Exp Bot 0: erm181v1-erm181 [Abstract] [Full Text]  
  • Gibson, K. E., Barnett, M. J., Toman, C. J., Long, S. R., Walker, G. C. (2007). The Symbiosis Regulator CbrA Modulates a Complex Regulatory Network Affecting the Flagellar Apparatus and Cell Envelope Proteins. J. Bacteriol. 189: 3591-3602 [Abstract] [Full Text]  
  • Jones, K. M., Lloret, J., Daniele, J. R., Walker, G. C. (2007). The Type IV Secretion System of Sinorhizobium meliloti Strain 1021 Is Required for Conjugation but Not for Intracellular Symbiosis. J. Bacteriol. 189: 2133-2138 [Abstract] [Full Text]  
  • Davies, B. W., Walker, G. C. (2007). Disruption of sitA Compromises Sinorhizobium meliloti for Manganese Uptake Required for Protection against Oxidative Stress. J. Bacteriol. 189: 2101-2109 [Abstract] [Full Text]  
  • Russo, D. M., Williams, A., Edwards, A., Posadas, D. M., Finnie, C., Dankert, M., Downie, J. A., Zorreguieta, A. (2006). Proteins Exported via the PrsD-PrsE Type I Secretion System and the Acidic Exopolysaccharide Are Involved in Biofilm Formation by Rhizobium leguminosarum.. J. Bacteriol. 188: 4474-4486 [Abstract] [Full Text]  
  • Gibson, K. E., Campbell, G. R., Lloret, J., Walker, G. C. (2006). CbrA Is a Stationary-Phase Regulator of Cell Surface Physiology and Legume Symbiosis in Sinorhizobium meliloti.. J. Bacteriol. 188: 4508-4521 [Abstract] [Full Text]  
  • Zhang, X.-S., Cheng, H.-P. (2006). Identification of Sinorhizobium meliloti Early Symbiotic Genes by Use of a Positive Functional Screen. Appl. Environ. Microbiol. 72: 2738-2748 [Abstract] [Full Text]  
  • Chi, F., Shen, S.-H., Cheng, H.-P., Jing, Y.-X., Yanni, Y. G., Dazzo, F. B. (2005). Ascending Migration of Endophytic Rhizobia, from Roots to Leaves, inside Rice Plants and Assessment of Benefits to Rice Growth Physiology. Appl. Environ. Microbiol. 71: 7271-7278 [Abstract] [Full Text]  
  • Takeda, N., Okamoto, S., Hayashi, M., Murooka, Y. (2005). Expression of LjENOD40 Genes in Response to Symbiotic and Non-symbiotic Signals: LjENOD40-1 and LjENOD40-2 are Differentially Regulated in Lotus japonicus. Plant Cell Physiol 46: 1291-1298 [Abstract] [Full Text]  
  • Luo, L., Yao, S.-Y., Becker, A., Ruberg, S., Yu, G.-Q., Zhu, J.-B., Cheng, H.-P. (2005). Two New Sinorhizobium meliloti LysR-Type Transcriptional Regulators Required for Nodulation. J. Bacteriol. 187: 4562-4572 [Abstract] [Full Text]  
  • Vicre, M., Santaella, C., Blanchet, S., Gateau, A., Driouich, A. (2005). Root Border-Like Cells of Arabidopsis. Microscopical Characterization and Role in the Interaction with Rhizobacteria. Plant Physiol. 138: 998-1008 [Abstract] [Full Text]  
  • Villacieros, M., Whelan, C., Mackova, M., Molgaard, J., Sanchez-Contreras, M., Lloret, J., Aguirre de Carcer, D., Oruezabal, R. I., Bolanos, L., Macek, T., Karlson, U., Dowling, D. N., Martin, M., Rivilla, R. (2005). Polychlorinated Biphenyl Rhizoremediation by Pseudomonas fluorescens F113 Derivatives, Using a Sinorhizobium meliloti nod System To Drive bph Gene Expression. Appl. Environ. Microbiol. 71: 2687-2694 [Abstract] [Full Text]  
  • Kaufusi, P. H., Forsberg, L. S., Tittabutr, P., Borthakur, D. (2004). Regulation of exopolysaccharide synthesis in Rhizobium sp. strain TAL1145 involves an alternative sigma factor gene, rpoH2. Microbiology 150: 3473-3482 [Abstract] [Full Text]  
  • Svistoonoff, S., Laplaze, L., Liang, J., Ribeiro, A., Gouveia, M. C., Auguy, F., Fevereiro, P., Franche, C., Bogusz, D. (2004). Infection-Related Activation of the cg12 Promoter Is Conserved between Actinorhizal and Legume-Rhizobia Root Nodule Symbiosis. Plant Physiol. 136: 3191-3197 [Abstract] [Full Text]  
  • Yao, S.-Y., Luo, L., Har, K. J., Becker, A., Ruberg, S., Yu, G.-Q., Zhu, J.-B., Cheng, H.-P. (2004). Sinorhizobium meliloti ExoR and ExoS Proteins Regulate both Succinoglycan and Flagellum Production. J. Bacteriol. 186: 6042-6049 [Abstract] [Full Text]  
  • Hoang, H. H., Becker, A., Gonzalez, J. E. (2004). The LuxR Homolog ExpR, in Combination with the Sin Quorum Sensing System, Plays a Central Role in Sinorhizobium meliloti Gene Expression. J. Bacteriol. 186: 5460-5472 [Abstract] [Full Text]  
  • Gage, D. J. (2004). Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes. Microbiol. Mol. Biol. Rev. 68: 280-300 [Abstract] [Full Text]  
  • Mitra, R. M., Long, S. R. (2004). Plant and Bacterial Symbiotic Mutants Define Three Transcriptionally Distinct Stages in the Development of the Medicago truncatula/Sinorhizobium meliloti Symbiosis. Plant Physiol. 134: 595-604 [Abstract] [Full Text]  
  • Gonzalez, J. E., Marketon, M. M. (2003). Quorum Sensing in Nitrogen-Fixing Rhizobia. Microbiol. Mol. Biol. Rev. 67: 574-592 [Abstract] [Full Text]  
  • Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T., Geurts, R. (2003). LysM Domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection. Science 302: 630-633 [Abstract] [Full Text]  
  • Wells, D. H., Long, S. R. (2003). Mutations in rpoBC Suppress the Defects of a Sinorhizobium meliloti relA Mutant. J. Bacteriol. 185: 5602-5610 [Abstract] [Full Text]  
  • Zhou, R., Wolk, C. P. (2003). A Two-component System Mediates Developmental Regulation of Biosynthesis of a Heterocyst Polysaccharide. J. Biol. Chem. 278: 19939-19946 [Abstract] [Full Text]  
  • Mazur, A., Krol, J. E., Marczak, M., Skorupska, A. (2003). Membrane Topology of PssT, the Transmembrane Protein Component of the Type I Exopolysaccharide Transport System in Rhizobium leguminosarum bv. trifolii Strain TA1. J. Bacteriol. 185: 2503-2511 [Abstract] [Full Text]  
  • Marketon, M. M., Glenn, S. A., Eberhard, A., Gonzalez, J. E. (2003). Quorum Sensing Controls Exopolysaccharide Production in Sinorhizobium meliloti. J. Bacteriol. 185: 325-331 [Abstract] [Full Text]  
  • Keating, D. H., Willits, M. G., Long, S. R. (2002). A Sinorhizobium meliloti Lipopolysaccharide Mutant Altered in Cell Surface Sulfation. J. Bacteriol. 184: 6681-6689 [Abstract] [Full Text]  
  • Pellock, B. J., Teplitski, M., Boinay, R. P., Bauer, W. D., Walker, G. C. (2002). A LuxR Homolog Controls Production of Symbiotically Active Extracellular Polysaccharide II by Sinorhizobium meliloti. J. Bacteriol. 184: 5067-5076 [Abstract] [Full Text]  
  • TSYGANOV, V. E., VOROSHILOVA, V. A., PRIEFER, U. B., BORISOV, A. Y., TIKHONOVICH, I. A. (2002). Genetic Dissection of the Initiation of the Infection Process and Nodule Tissue Development in the Rhizobium-Pea (Pisum sativum L.) Symbiosis. ANN BOT (LOND) 89: 357-366 [Abstract] [Full Text]  
  • Lum, M. R., Li, Y., LaRue, T. A., David-Schwartz, R., Kapulnik, Y., Hirsch, A. M. (2002). Investigation of Four Classes of Non-nodulating White Sweetclover (Melilotus alba annua Desr.) Mutants and Their Responses to Arbuscular-Mycorrhizal Fungi. Integr. Comp. Biol. 42: 295-303 [Abstract] [Full Text]  
  • Campbell, G. R. O., Reuhs, B. L., Walker, G. C. (2002). Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc. Natl. Acad. Sci. USA 99: 3938-3943 [Abstract] [Full Text]  
  • Krishnan, H. B. (2002). NolX of Sinorhizobium fredii USDA257, a Type III-Secreted Protein Involved in Host Range Determination, Is Localized in the Infection Threads of Cowpea (Vigna unguiculata [L.] Walp) and Soybean (Glycine max [L.] Merr.) Nodules. J. Bacteriol. 184: 831-839 [Abstract] [Full Text]  
  • Bringhurst, R. M., Cardon, Z. G., Gage, D. J. (2001). Galactosides in the rhizosphere: Utilization by Sinorhizobium meliloti and development of a biosensor. Proc. Natl. Acad. Sci. USA 10.1073/pnas.071375898v1 [Abstract] [Full Text]  
  • Broughton, W. J., Jabbouri, S., Perret, X. (2000). Keys to Symbiotic Harmony. J. Bacteriol. 182: 5641-5652 [Full Text]  
  • Guerreiro, N., Ksenzenko, V. N., Djordjevic, M. A., Ivashina, T. V., Rolfe, B. G. (2000). Elevated Levels of Synthesis of over 20 Proteins Results after Mutation of the Rhizobium leguminosarum Exopolysaccharide Synthesis Gene pssA. J. Bacteriol. 182: 4521-4532 [Abstract] [Full Text]  
  • Pellock, B. J., Cheng, H.-P., Walker, G. C. (2000). Alfalfa Root Nodule Invasion Efficiency Is Dependent on Sinorhizobium meliloti Polysaccharides. J. Bacteriol. 182: 4310-4318 [Abstract] [Full Text]  
  • Zorreguieta, A., Finnie, C., Downie, J. A. (2000). Extracellular Glycanases of Rhizobium leguminosarum Are Activated on the Cell Surface by an Exopolysaccharide-Related Component. J. Bacteriol. 182: 1304-1312 [Abstract] [Full Text]  
  • Perret, X., Staehelin, C., Broughton, W. J. (2000). Molecular Basis of Symbiotic Promiscuity. Microbiol. Mol. Biol. Rev. 64: 180-201 [Abstract] [Full Text]  
  • Wang, L.-X., Wang, Y., Pellock, B., Walker, G. C. (1999). Structural Characterization of the Symbiotically Important Low-Molecular-Weight Succinoglycan of Sinorhizobium meliloti. J. Bacteriol. 181: 6788-6796 [Abstract] [Full Text]  
  • Bhagwat, A. A., Mithöfer, A., Pfeffer, P. E., Kraus, C., Spickers, N., Hotchkiss, A., Ebel, J., Keister, D. L. (1999). Further Studies of the Role of Cyclic beta -Glucans in Symbiosis. An ndvC Mutant of Bradyrhizobium japonicum Synthesizes Cyclodecakis-(1right-arrow3)-beta -Glucosyl. Plant Physiol. 119: 1057-1064 [Abstract] [Full Text]  
  • Lellouch, A. C., Geremia, R. A. (1999). Expression and Study of Recombinant ExoM, a beta 1-4 Glucosyltransferase Involved in Succinoglycan Biosynthesis in Sinorhizobium meliloti. J. Bacteriol. 181: 1141-1148 [Abstract] [Full Text]  
  • Liu, M., González, J. E., Willis, L. B., Walker, G. C. (1998). A Novel Screening Method for Isolating Exopolysaccharide-Deficient Mutants. Appl. Environ. Microbiol. 64: 4600-4602 [Abstract] [Full Text]  
  • Garinot-Schneider, C., Lellouch, A. C., Geremia, R. A. (2000). Identification of Essential Amino Acid Residues in the Sinorhizobium meliloti Glucosyltransferase ExoM. J. Biol. Chem. 275: 31407-31413 [Abstract] [Full Text]  
  • Bringhurst, R. M., Cardon, Z. G., Gage, D. J. (2001). Galactosides in the rhizosphere: Utilization by Sinorhizobium meliloti and development of a biosensor. Proc. Natl. Acad. Sci. USA 98: 4540-4545 [Abstract] [Full Text]