Previous Article | Next Article 
J Bacteriol. 1990 August; 172(8): 4295-4306
Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules.
J Vasse,
F de Billy,
S Camut and
G Truchet
Laboratoire de Biologie Moléculaire des Relations Plantes-Microorganismes, Céntre National de la Recherche Scientifique-Institut National de la Recherche Agronomique, Castanet-Tolosan, France.
ABSTRACT
Bacteroid differentiation was examined in developing and mature alfalfa nodules elicited by wild-type or Fix- mutant strains of Rhizobium meliloti. Ultrastructural studies of wild-type nodules distinguished five steps in bacteroid differentiation (types 1 to 5), each being restricted to a well-defined histological region of the nodule. Correlative studies between nodule development, bacteroid differentiation, and acetylene reduction showed that nitrogenase activity was always associated with the differentiation of the distal zone III of the nodule. In this region, the invaded cells were filled with heterogeneous type 4 bacteroids, the cytoplasm of which displayed an alternation of areas enriched with ribosomes or with DNA fibrils. Cytological studies of complementary halves of transversally sectioned mature nodules confirmed that type 4 bacteroids were always observed in the half of the nodule expressing nitrogenase activity, while the presence of type 5 bacteroids could never be correlated with acetylene reduction. Bacteria with a transposon Tn5 insertion in pSym fix genes elicited the development of Fix- nodules in which bacteroids could not develop into the last two ultrastructural types. The use of mutant strains deleted of DNA fragments bearing functional reiterated pSym fix genes and complemented with recombinant plasmids, each carrying one of these fragments, strengthened the correlation between the occurrence of type 4 bacteroids and acetylene reduction. A new nomenclature is proposed to distinguish the histological areas in alfalfa nodules which account for and are correlated with the multiple stages of bacteroid development.
J Bacteriol. 1990 August; 172(8): 4295-4306
This article has been cited by other articles:
-
Kuppusamy, K. T., Ivashuta, S., Bucciarelli, B., Vance, C. P., Gantt, J. S., VandenBosch, K. A.
(2009). Knockdown of CELL DIVISION CYCLE16 Reveals an Inverse Relationship between Lateral Root and Nodule Numbers and a Link to Auxin in Medicago truncatula. Plant Physiol.
151: 1155-1166
[Abstract]
[Full Text]
-
Limpens, E., Ivanov, S., van Esse, W., Voets, G., Fedorova, E., Bisseling, T.
(2009). Medicago N2-Fixing Symbiosomes Acquire the Endocytic Identity Marker Rab7 but Delay the Acquisition of Vacuolar Identity. Plant Cell
21: 2811-2828
[Abstract]
[Full Text]
-
Lelandais-Briere, C., Naya, L., Sallet, E., Calenge, F., Frugier, F., Hartmann, C., Gouzy, J., Crespi, M.
(2009). Genome-Wide Medicago truncatula Small RNA Analysis Revealed Novel MicroRNAs and Isoforms Differentially Regulated in Roots and Nodules. Plant Cell
21: 2780-2796
[Abstract]
[Full Text]
-
Redondo, F. J., de la Pena, T. C., Morcillo, C. N., Lucas, M. M., Pueyo, J. J.
(2009). Overexpression of Flavodoxin in Bacteroids Induces Changes in Antioxidant Metabolism Leading to Delayed Senescence and Starch Accumulation in Alfalfa Root Nodules. Plant Physiol.
149: 1166-1178
[Abstract]
[Full Text]
-
Vernie, T., Moreau, S., de Billy, F., Plet, J., Combier, J.-P., Rogers, C., Oldroyd, G., Frugier, F., Niebel, A., Gamas, P.
(2008). EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation in Medicago truncatula. Plant Cell
20: 2696-2713
[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]
-
Combier, J. P., de Billy, F., Gamas, P., Niebel, A., Rivas, S.
(2008). Trans-regulation of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development. Genes Dev.
22: 1549-1559
[Abstract]
[Full Text]
-
Elliott, G. N., Chen, W.-M., Bontemps, C., Chou, J.-H., Young, J. P. W., Sprent, J. I., James, E. K.
(2007). Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. ANN BOT (LOND)
100: 1403-1411
[Abstract]
[Full Text]
-
Strozycki, P. M., Szczurek, A., Lotocka, B., Figlerowicz, M., Legocki, A. B.
(2007). Ferritins and nodulation in Lupinus luteus: iron management in indeterminate type nodules. J Exp Bot
0: erm152v1-erm152
[Abstract]
[Full Text]
-
Wan, X., Hontelez, J., Lillo, A., Guarnerio, C., van de Peut, D., Fedorova, E., Bisseling, T., Franssen, H.
(2007). Medicago truncatula ENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development. J Exp Bot
58: 2033-2041
[Abstract]
[Full Text]
-
Pislariu, C. I., Dickstein, R.
(2007). An IRE-Like AGC Kinase Gene, MtIRE, Has Unique Expression in the Invasion Zone of Developing Root Nodules in Medicago truncatula. Plant Physiol.
144: 682-694
[Abstract]
[Full Text]
-
Combier, J.-P., Vernie, T., de Billy, F., El Yahyaoui, F., Mathis, R., Gamas, P.
(2007). The MtMMPL1 Early Nodulin Is a Novel Member of the Matrix Metalloendoproteinase Family with a Role in Medicago truncatula Infection by Sinorhizobium meliloti. Plant Physiol.
144: 703-716
[Abstract]
[Full Text]
-
Cheng, J., Sibley, C. D., Zaheer, R., Finan, T. M.
(2007). A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis. Microbiology
153: 375-387
[Abstract]
[Full Text]
-
Wang, C., Saldanha, M., Sheng, X., Shelswell, K. J., Walsh, K. T., Sobral, B. W. S., Charles, T. C.
(2007). Roles of poly-3-hydroxybutyrate (PHB) and glycogen in symbiosis of Sinorhizobium meliloti with Medicago sp.. Microbiology
153: 388-398
[Abstract]
[Full Text]
-
Combier, J.-P., Frugier, F., de Billy, F., Boualem, A., El-Yahyaoui, F., Moreau, S., Vernie, T., Ott, T., Gamas, P., Crespi, M., Niebel, A.
(2006). MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula.. Genes Dev.
20: 3084-3088
[Abstract]
[Full Text]
-
Young, K. D.
(2006). The Selective Value of Bacterial Shape. Microbiol. Mol. Biol. Rev.
70: 660-703
[Abstract]
[Full Text]
-
Chou, M.-X., Wei, X.-Y., Chen, D.-S., Zhou, J.-C.
(2006). Thirteen nodule-specific or nodule-enhanced genes encoding products homologous to cysteine cluster proteins or plant lipid transfer proteins are identified in Astragalus sinicus L. by suppressive subtractive hybridization. J Exp Bot
57: 2673-2685
[Abstract]
[Full Text]
-
Bobik, C., Meilhoc, E., Batut, J.
(2006). FixJ: a Major Regulator of the Oxygen Limitation Response and Late Symbiotic Functions of Sinorhizobium meliloti. J. Bacteriol.
188: 4890-4902
[Abstract]
[Full Text]
-
Matamoros, M. A., Loscos, J., Coronado, M. J., Ramos, J., Sato, S., Testillano, P. S., Tabata, S., Becana, M.
(2006). Biosynthesis of Ascorbic Acid in Legume Root Nodules. Plant Physiol.
141: 1068-1077
[Abstract]
[Full Text]
-
Liu, J., Miller, S. S., Graham, M., Bucciarelli, B., Catalano, C. M., Sherrier, D. J., Samac, D. A., Ivashuta, S., Fedorova, M., Matsumoto, P., Gantt, J. S., Vance, C. P.
(2006). Recruitment of Novel Calcium-Binding Proteins for Root Nodule Symbiosis in Medicago truncatula. Plant Physiol.
141: 167-177
[Abstract]
[Full Text]
-
Mergaert, P., Uchiumi, T., Alunni, B., Evanno, G., Cheron, A., Catrice, O., Mausset, A.-E., Barloy-Hubler, F., Galibert, F., Kondorosi, A., Kondorosi, E.
(2006). Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc. Natl. Acad. Sci. USA
103: 5230-5235
[Abstract]
[Full Text]
-
Campbell, G. R. O., Taga, M. E., Mistry, K., Lloret, J., Anderson, P. J., Roth, J. R., Walker, G. C.
(2006). Sinorhizobium meliloti bluB is necessary for production of 5,6-dimethylbenzimidazole, the lower ligand of B12. Proc. Natl. Acad. Sci. USA
103: 4634-4639
[Abstract]
[Full Text]
-
Monahan-Giovanelli, H., Pinedo, C. A., Gage, D. J.
(2006). Architecture of Infection Thread Networks in Developing Root Nodules Induced by the Symbiotic Bacterium Sinorhizobium meliloti on Medicago truncatula. Plant Physiol.
140: 661-670
[Abstract]
[Full Text]
-
Chen, W.-M., de Faria, S. M., Straliotto, R., Pitard, R. M., Simoes-Araujo, J. L., Chou, J.-H., Chou, Y.-J., Barrios, E., Prescott, A. R., Elliott, G. N., Sprent, J. I., Young, J. P. W., James, E. K.
(2005). Proof that Burkholderia Strains Form Effective Symbioses with Legumes: a Study of Novel Mimosa-Nodulating Strains from South America. Appl. Environ. Microbiol.
71: 7461-7471
[Abstract]
[Full Text]
-
Capoen, W., Goormachtig, S., De Rycke, R., Schroeyers, K., Holsters, M.
(2005). SrSymRK, a plant receptor essential for symbiosome formation. Proc. Natl. Acad. Sci. USA
102: 10369-10374
[Abstract]
[Full Text]
-
Kondorosi, E., Redondo-Nieto, M., Kondorosi, A.
(2005). Ubiquitin-Mediated Proteolysis. To Be in the Right Place at the Right Moment during Nodule Development. Plant Physiol.
137: 1197-1204
[Full Text]
-
Yurgel, S. N., Kahn, M. L.
(2005). Sinorhizobium meliloti dctA Mutants with Partial Ability To Transport Dicarboxylic Acids. J. Bacteriol.
187: 1161-1172
[Abstract]
[Full Text]
-
Harrison, J., Jamet, A., Muglia, C. I., Van de Sype, G., Aguilar, O. M., Puppo, A., Frendo, P.
(2005). Glutathione Plays a Fundamental Role in Growth and Symbiotic Capacity of Sinorhizobium meliloti. J. Bacteriol.
187: 168-174
[Abstract]
[Full Text]
-
El Yahyaoui, F., Kuster, H., Ben Amor, B., Hohnjec, N., Puhler, A., Becker, A., Gouzy, J., Vernie, T., Gough, C., Niebel, A., Godiard, L., Gamas, P.
(2004). Expression Profiling in Medicago truncatula Identifies More Than 750 Genes Differentially Expressed during Nodulation, Including Many Potential Regulators of the Symbiotic Program. Plant Physiol.
136: 3159-3176
[Abstract]
[Full Text]
-
Trinchant, J.-C., Boscari, A., Spennato, G., Van de Sype, G., Le Rudulier, D.
(2004). Proline Betaine Accumulation and Metabolism in Alfalfa Plants under Sodium Chloride Stress. Exploring Its Compartmentalization in Nodules. Plant Physiol.
135: 1583-1594
[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]
-
Martinez, M., Brito, B., Imperial, J., Ruiz-Argueso, T.
(2004). Characterization of a new internal promoter (P3) for Rhizobium leguminosarum hydrogenase accessory genes hupGHIJ. Microbiology
150: 665-675
[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]
-
Vinardell, J. M., Fedorova, E., Cebolla, A., Kevei, Z., Horvath, G., Kelemen, Z., Tarayre, S., Roudier, F., Mergaert, P., Kondorosi, A., Kondorosi, E.
(2003). Endoreduplication Mediated by the Anaphase-Promoting Complex Activator CCS52A Is Required for Symbiotic Cell Differentiation in Medicago truncatula Nodules. Plant Cell
15: 2093-2105
[Abstract]
[Full Text]
-
Mergaert, P., Nikovics, K., Kelemen, Z., Maunoury, N., Vaubert, D., Kondorosi, A., Kondorosi, E.
(2003). A Novel Family in Medicago truncatula Consisting of More Than 300 Nodule-Specific Genes Coding for Small, Secreted Polypeptides with Conserved Cysteine Motifs. Plant Physiol.
132: 161-173
[Abstract]
[Full Text]
-
Denison, R. F., Okano, Y.
(2003). Leghaemoglobin oxygenation gradients in alfalfa and yellow sweetclover nodules. J Exp Bot
54: 1085-1091
[Abstract]
[Full Text]
-
Varkonyi-Gasic, E., White, D. W. R.
(2002). The White Clover enod40 Gene Family. Expression Patterns of Two Types of Genes Indicate a Role in Vascular Function. Plant Physiol.
129: 1107-1118
[Abstract]
[Full Text]
-
Patriarca, E. J., Tate, R., Iaccarino, M.
(2002). Key Role of Bacterial NH4+ Metabolism in Rhizobium-Plant Symbiosis. Microbiol. Mol. Biol. Rev.
66: 203-222
[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]
-
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]
-
Lambert, A., Osteras, M., Mandon, K., Poggi, M.-C., Le Rudulier, D.
(2001). Fructose Uptake in Sinorhizobium meliloti Is Mediated by a High-Affinity ATP-Binding Cassette Transport System. J. Bacteriol.
183: 4709-4717
[Abstract]
[Full Text]
-
Naito, Y., Fujie, M., Usami, S., Murooka, Y., Yamada, T.
(2000). The Involvement of a Cysteine Proteinase in the Nodule Development in Chinese Milk Vetch Infected with Mesorhizobium huakuii subsp. rengei. Plant Physiol.
124: 1087-1096
[Abstract]
[Full Text]
-
Tirichine, L., de Billy, F., Huguet, T.
(2000). Mtsym6, a Gene Conditioning Sinorhizobium Strain-Specific Nitrogen Fixation in Medicago truncatula. Plant Physiol.
123: 845-852
[Abstract]
[Full Text]
-
Frugier, F., Poirier, S., Satiat-Jeunemaître, B., Kondorosi, A., Crespi, M.
(2000). A Kruppel-like zinc finger protein is involved in nitrogen-fixing root nodule organogenesis. Genes Dev.
14: 475-482
[Abstract]
[Full Text]
-
Matamoros, M. A., Moran, J. F., Iturbe-Ormaetxe, I., Rubio, M. C., Becana, M.
(1999). Glutathione and Homoglutathione Synthesis in Legume Root Nodules. Plant Physiol.
121: 879-888
[Abstract]
[Full Text]
-
Willis, L. B., Walker, G. C.
(1999). A Novel Sinorhizobium meliloti Operon Encodes an alpha -Glucosidase and a Periplasmic-Binding-Protein-Dependent Transport System for alpha -Glucosides. J. Bacteriol.
181: 4176-4184
[Abstract]
[Full Text]
-
Demont-Caulet, N., Maillet, F., Tailler, D., Jacquinet, J.-C., Promé, J.-C., Nicolaou, K. C., Truchet, G., Beau, J.-M., Dénarié, J.
(1999). Nodule-Inducing Activity of Synthetic Sinorhizobium meliloti Nodulation Factors and Related Lipo-Chitooligosaccharides on Alfalfa. Importance of the Acyl Chain Structure. Plant Physiol.
120: 83-92
[Abstract]
[Full Text]
-
Trepp, G. B., van de Mortel, M., Yoshioka, H., Miller, S. S., Samac, D. A., Gantt, J. S., Vance, C. P.
(1999). NADH-Glutamate Synthase in Alfalfa Root Nodules. Genetic Regulation and Cellular Expression. Plant Physiol.
119: 817-828
[Abstract]
[Full Text]
-
Trepp, G. B., Plank, D. W., Stephen Gantt, J., Vance, C. P.
(1999). NADH-Glutamate Synthase in Alfalfa Root Nodules. Immunocytochemical Localization. Plant Physiol.
119: 829-838
[Abstract]
[Full Text]
-
Timmers, A., Auriac, M., Truchet, G
(1999). Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development
126: 3617-3628
[Abstract]
-
Wycoff, K. L., Hunt, S., Gonzales, M. B., VandenBosch, K. A., Layzell, D. B., Hirsch, A. M.
(1998). Effects of Oxygen on Nodule Physiology and Expression of Nodulins in Alfalfa. Plant Physiol.
117: 385-395
[Abstract]
[Full Text]
-
Timmers, A., Auriac, M., de Billy, F, Truchet, G
(1998). Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development
125: 339-349
[Abstract]
-
(1998). Multiple Genetic Controls on Rhizobium meliloti syrA, a Regulator of Exopolysaccharide Abundance. Genetics
148: 19-32
-
Arcondeguy, T, Huez, I, Tillard, P, Gangneux, C, de Billy, F, Gojon, A, Truchet, G, Kahn, D
(1997). The Rhizobium meliloti PII protein, which controls bacterial nitrogen metabolism, affects alfalfa nodule development.. Genes Dev.
11: 1194-1206
[Abstract]
-
Glazebrook, J, Ichige, A, Walker, G C
(1993). A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development.. Genes Dev.
7: 1485-1497
[Abstract]