The Nodulation of Alfalfa by the Acid-Tolerant Rhizobium sp. Strain LPU83 Does Not Require Sulfated Forms of Lipochitooligosaccharide Nodulation Signals

Torres Tejerizo G, Florencia Del Papa M, Eugenia Soria-Diaz M, Draghi W, Lozano M, de los Angeles Giusti M, Manyani H, Megias M, Gil Serrano A, Pühler A, Niehaus K, et al. (2011)
Journal of Bacteriology 193(1): 30-39.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Torres Tejerizo, Gonzalo; Florencia Del Papa, Maria; Eugenia Soria-Diaz, M.; Draghi, Walter; Lozano, Mauricio; de los Angeles Giusti, Maria; Manyani, Hamid; Megias, Manuel; Gil Serrano, Antonio; Pühler, AlfredUniBi ; Niehaus, KarstenUniBi; Lagares, Antonio
Alle
Abstract / Bemerkung
The induction of root nodules by the majority of rhizobia has a strict requirement for the secretion of symbiosis-specific lipochitooligosaccharides (nodulation factors [NFs]). The nature of the chemical substitution on the NFs depends on the particular rhizobium and contributes to the host specificity imparted by the NFs. We present here a description of the genetic organization of the nod gene cluster and the characterization of the chemical structure of the NFs associated with the broad-host-range Rhizobium sp. strain LPU83, a bacterium capable of nodulating at least alfalfa, bean, and Leucena leucocephala. The nod gene cluster was located on the plasmid pLPU83b. The organization of the cluster showed synteny with those of the alfalfa-nodulating rhizobia, Sinorhizobium meliloti and Sinorhizobium medicae. Interestingly, the strongest sequence similarity observed was between the partial nod sequences of Rhizobium mongolense USDA 1844 and the corresponding LPU83 nod genes sequences. The phylogenetic analysis of the intergenic region nodEG positions strain LPU83 and the type strain R. mongolense 1844 in the same branch, which indicates that Rhizobium sp. strain LPU83 might represent an early alfalfa-nodulating genotype. The NF chemical structures obtained for the wild-type strain consist of a trimeric, tetrameric, and pentameric chitin backbone that shares some substitutions with both alfalfa-and bean-nodulating rhizobia. Remarkably, while in strain LPU83 most of the NFs were sulfated in their reducing terminal residue, none of the NFs isolated from the nodH mutant LPU83-H were sulfated. The evidence obtained supports the notion that the sulfate decoration of NFs in LPU83 is not necessary for alfalfa nodulation.
Erscheinungsjahr
2011
Zeitschriftentitel
Journal of Bacteriology
Band
193
Ausgabe
1
Seite(n)
30-39
ISSN
0021-9193
Page URI
https://pub.uni-bielefeld.de/record/1968039

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Torres Tejerizo G, Florencia Del Papa M, Eugenia Soria-Diaz M, et al. The Nodulation of Alfalfa by the Acid-Tolerant Rhizobium sp. Strain LPU83 Does Not Require Sulfated Forms of Lipochitooligosaccharide Nodulation Signals. Journal of Bacteriology. 2011;193(1):30-39.
Torres Tejerizo, G., Florencia Del Papa, M., Eugenia Soria-Diaz, M., Draghi, W., Lozano, M., de los Angeles Giusti, M., Manyani, H., et al. (2011). The Nodulation of Alfalfa by the Acid-Tolerant Rhizobium sp. Strain LPU83 Does Not Require Sulfated Forms of Lipochitooligosaccharide Nodulation Signals. Journal of Bacteriology, 193(1), 30-39. doi:10.1128/JB.01009-10
Torres Tejerizo, G., Florencia Del Papa, M., Eugenia Soria-Diaz, M., Draghi, W., Lozano, M., de los Angeles Giusti, M., Manyani, H., Megias, M., Gil Serrano, A., Pühler, A., et al. (2011). The Nodulation of Alfalfa by the Acid-Tolerant Rhizobium sp. Strain LPU83 Does Not Require Sulfated Forms of Lipochitooligosaccharide Nodulation Signals. Journal of Bacteriology 193, 30-39.
Torres Tejerizo, G., et al., 2011. The Nodulation of Alfalfa by the Acid-Tolerant Rhizobium sp. Strain LPU83 Does Not Require Sulfated Forms of Lipochitooligosaccharide Nodulation Signals. Journal of Bacteriology, 193(1), p 30-39.
G. Torres Tejerizo, et al., “The Nodulation of Alfalfa by the Acid-Tolerant Rhizobium sp. Strain LPU83 Does Not Require Sulfated Forms of Lipochitooligosaccharide Nodulation Signals”, Journal of Bacteriology, vol. 193, 2011, pp. 30-39.
Torres Tejerizo, G., Florencia Del Papa, M., Eugenia Soria-Diaz, M., Draghi, W., Lozano, M., de los Angeles Giusti, M., Manyani, H., Megias, M., Gil Serrano, A., Pühler, A., Niehaus, K., Lagares, A., Pistorio, M.: The Nodulation of Alfalfa by the Acid-Tolerant Rhizobium sp. Strain LPU83 Does Not Require Sulfated Forms of Lipochitooligosaccharide Nodulation Signals. Journal of Bacteriology. 193, 30-39 (2011).
Torres Tejerizo, Gonzalo, Florencia Del Papa, Maria, Eugenia Soria-Diaz, M., Draghi, Walter, Lozano, Mauricio, de los Angeles Giusti, Maria, Manyani, Hamid, Megias, Manuel, Gil Serrano, Antonio, Pühler, Alfred, Niehaus, Karsten, Lagares, Antonio, and Pistorio, Mariano. “The Nodulation of Alfalfa by the Acid-Tolerant Rhizobium sp. Strain LPU83 Does Not Require Sulfated Forms of Lipochitooligosaccharide Nodulation Signals”. Journal of Bacteriology 193.1 (2011): 30-39.

7 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Two Broad Host Range Rhizobial Strains Isolated From Relict Legumes Have Various Complementary Effects on Symbiotic Parameters of Co-inoculated Plants.
Safronova V, Belimov A, Sazanova A, Chirak E, Kuznetsova I, Andronov E, Pinaev A, Tsyganova A, Seliverstova E, Kitaeva A, Tsyganov V, Tikhonovich I., Front Microbiol 10(), 2019
PMID: 30930885
Characterization of Rhizobium grahamii extrachromosomal replicons and their transfer among rhizobia.
Althabegoiti MJ, Ormeño-Orrillo E, Lozano L, Torres Tejerizo G, Rogel MA, Mora J, Martínez-Romero E., BMC Microbiol 14(), 2014
PMID: 24397311
Genome sequence of the acid-tolerant strain Rhizobium sp. LPU83.
Wibberg D, Tejerizo GT, Del Papa MF, Martini C, Pühler A, Lagares A, Schlüter A, Pistorio M., J Biotechnol 176(), 2014
PMID: 24556327
Rhizobial plasmid pLPU83a is able to switch between different transfer machineries depending on its genomic background.
Torres Tejerizo G, Pistorio M, Althabegoiti MJ, Cervantes L, Wibberg D, Schlüter A, Pühler A, Lagares A, Romero D, Brom S., FEMS Microbiol Ecol 88(3), 2014
PMID: 24646299
Symbiont shift towards Rhizobium nodulation in a group of phylogenetically related Phaseolus species.
Servín-Garcidueñas LE, Zayas-Del Moral A, Ormeño-Orrillo E, Rogel MA, Delgado-Salinas A, Sánchez F, Martínez-Romero E., Mol Phylogenet Evol 79(), 2014
PMID: 24952318
Nonlegume Parasponia andersonii deploys a broad rhizobium host range strategy resulting in largely variable symbiotic effectiveness.
Op den Camp RH, Polone E, Fedorova E, Roelofsen W, Squartini A, Op den Camp HJ, Bisseling T, Geurts R., Mol Plant Microbe Interact 25(7), 2012
PMID: 22668002
Genome sequence of Rhizobium grahamii CCGE502, a broad-host-range symbiont with low nodulation competitiveness in Phaseolus vulgaris.
Althabegoiti MJ, Lozano L, Torres-Tejerizo G, Ormeño-Orrillo E, Rogel MA, González V, Martínez-Romero E., J Bacteriol 194(23), 2012
PMID: 23144400

59 References

Daten bereitgestellt von Europe PubMed Central.

Horizontal gene transfer and homologous recombination drive the evolution of the nitrogen-fixing symbionts of Medicago species.
Bailly X, Olivieri I, Brunel B, Cleyet-Marel JC, Bena G., J. Bacteriol. 189(14), 2007
PMID: 17496100
Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid.
Barnett MJ, Fisher RF, Jones T, Komp C, Abola AP, Barloy-Hubler F, Bowser L, Capela D, Galibert F, Gouzy J, Gurjal M, Hong A, Huizar L, Hyman RW, Kahn D, Kahn ML, Kalman S, Keating DH, Palm C, Peck MC, Surzycki R, Wells DH, Yeh KC, Davis RW, Federspiel NA, Long SR., Proc. Natl. Acad. Sci. U.S.A. 98(17), 2001
PMID: 11481432
R factor transfer in Rhizobium leguminosarum.
Beringer JE., J. Gen. Microbiol. 84(1), 1974
PMID: 4612098
Characterization and mutational analysis of nodHPQ genes of Rhizobium sp. strain N33.
Cloutler J, Laberge S, Castonguay Y, Antoun H., Mol. Plant Microbe Interact. 9(8), 1996
PMID: 8870271
Sinorhizobium fredii HH103 cgs mutants are unable to nodulate determinate- and indeterminate nodule-forming legumes and overproduce an altered EPS.
Crespo-Rivas JC, Margaret I, Hidalgo A, Buendia-Claveria AM, Ollero FJ, Lopez-Baena FJ, del Socorro Murdoch P, Rodriguez-Carvajal MA, Soria-Diaz ME, Reguera M, Lloret J, Sumpton DP, Mosely JA, Thomas-Oates JE, van Brussel AA, Gil-Serrano A, Vinardell JM, Ruiz-Sainz JE., Mol. Plant Microbe Interact. 22(5), 2009
PMID: 19348575
Isolation and characterization of alfalfa-nodulating rhizobia present in acidic soils of central argentina and uruguay
del Papa MF , Balague LJ, Sowinski SC, Wegener C, Segundo E, Abarca FM, Toro N, Niehaus K, P hler A , Aguilar OM, Martinez-Drets G, Lagares A., Appl. Environ. Microbiol. 65(4), 1999
PMID: 10103231
Identification and characterization of a nodH ortholog from the alfalfa-nodulating Or191-like rhizobia.
Del Papa MF, Pistorio M, Draghi WO, Lozano MJ, Giusti MA, Medina C, van Dillewijn P, Martinez-Abarca F, Moron Flores B, Ruiz-Sainz JE, Megias M, Puhler A, Niehaus K, Toro N, Lagares A., Mol. Plant Microbe Interact. 20(2), 2007
PMID: 17313165
Species limits in Rhizobium populations that nodulate the common bean (Phaseolus vulgaris).
Eardly BD, Wang FS, Whittam TS, Selander RK., Appl. Environ. Microbiol. 61(2), 1995
PMID: 7574588
Rhizobium meliloti host range nodH gene determines production of an alfalfa-specific extracellular signal.
Faucher C, Maillet F, Vasse J, Rosenberg C, van Brussel AA, Truchet G, Denarie J., J. Bacteriol. 170(12), 1988
PMID: 3056902
Characterization of Rhizobium tropici CIAT899 nodulation factors: the role of nodH and nodPQ genes in their sulfation.
Folch-Mallol JL, Marroqui S, Sousa C, Manyani H, Lopez-Lara IM, van der Drift KM, Haverkamp J, Quinto C, Gil-Serrano A, Thomas-Oates J, Spaink HP, Megias M., Mol. Plant Microbe Interact. 9(3), 1996
PMID: 8850086
NodS is an S-adenosyl-L-methionine-dependent methyltransferase that methylates chitooligosaccharides deacetylated at the non-reducing end.
Geelen D, Leyman B, Mergaert P, Klarskov K, Van Montagu M, Geremia R, Holsters M., Mol. Microbiol. 17(2), 1995
PMID: 7494487
Nod factor signaling genes and their function in the early stages of Rhizobium infection.
Geurts R, Fedorova E, Bisseling T., Curr. Opin. Plant Biol. 8(4), 2005
PMID: 15955723
How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model.
Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC., Nat. Rev. Microbiol. 5(8), 2007
PMID: 17632573
Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts.
Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N., Microbiology (Reading, Engl.) 147(Pt 4), 2001
PMID: 11283294
Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal.
Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J., Nature 344(6268), 1990
PMID: 2330031
The nodulation protein NodG shows the enzymatic activity of an 3-oxoacyl-acyl carrier protein reductase.
Lopez-Lara IM, Geiger O., Mol. Plant Microbe Interact. 14(3), 2001
PMID: 11277432
Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti.
Lopez-Lara IM, van den Berg JD, Thomas-Oates JE, Glushka J, Lugtenberg BJ, Spaink HP., Mol. Microbiol. 15(4), 1995
PMID: 7783635

AUTHOR UNKNOWN, 1972
Coordinating nodule morphogenesis with rhizobial infection in legumes.
Oldroyd GE, Downie JA., Annu Rev Plant Biol 59(), 2008
PMID: 18444906
Reprogramming plant cells for endosymbiosis.
Oldroyd GE, Harrison MJ, Paszkowski U., Science 324(5928), 2009
PMID: 19423817
Molecular basis of symbiotic promiscuity.
Perret X, Staehelin C, Broughton WJ., Microbiol. Mol. Biol. Rev. 64(1), 2000
PMID: 10704479
Wild type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors.
Poupot R, Martinez-Romero E, Gautier N, Prome JC., J. Biol. Chem. 270(11), 1995
PMID: 7890737
In vitro insertional mutagenesis with a selectable DNA fragment.
Prentki P, Krisch HM., Gene 29(3), 1984
PMID: 6237955
Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated.
Price NP, Relic B, Talmont F, Lewin A, Prome D, Pueppke SG, Maillet F, Denarie J, Prome JC, Broughton WJ., Mol. Microbiol. 6(23), 1992
PMID: 1474899
The lipo-oligosaccharidic symbiotic signals of Rhizobium meliloti.
Roche P, Debelle F, Lerouge P, Vasse J, Truchet G, Prome JC, Denarie J., Biochem. Soc. Trans. 20(2), 1992
PMID: 1397613

AUTHOR UNKNOWN, 1989
A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum.
Sanjuan J, Carlson RW, Spaink HP, Bhat UR, Barbour WM, Glushka J, Stacey G., Proc. Natl. Acad. Sci. U.S.A. 89(18), 1992
PMID: 1528893
In vitro sulfotransferase activity of Rhizobium meliloti NodH protein: lipochitooligosaccharide nodulation signals are sulfated after synthesis of the core structure.
Schultze M, Staehelin C, Rohrig H, John M, Schmidt J, Kondorosi E, Schell J, Kondorosi A., Proc. Natl. Acad. Sci. U.S.A. 92(7), 1995
PMID: 7708710

AUTHOR UNKNOWN, 1999

AUTHOR UNKNOWN, 1983

AUTHOR UNKNOWN, 1989
Rhizobial lipo-oligosaccharides: answers and questions.
Spaink HP., Plant Mol. Biol. 20(5), 1992
PMID: 1463833
Detection and separation of Rhizobium and Bradyrhizobium Nod metabolites using thin-layer chromatography.
Spaink HP, Aarts A, Stacey G, Bloemberg GV, Lugtenberg BJ, Kennedy EP., Mol. Plant Microbe Interact. 5(1), 1992
PMID: 1600238
A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium.
Spaink HP, Sheeley DM, van Brussel AA, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJ., Nature 354(6349), 1991
PMID: 1944592
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.
Tamura K, Dudley J, Nei M, Kumar S., Mol. Biol. Evol. 24(8), 2007
PMID: 17488738

AUTHOR UNKNOWN, 2010
Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. medicaginis) of S. meliloti.
Villegas Mdel C, Rome S, Maure L, Domergue O, Gardan L, Bailly X, Cleyet-Marel JC, Brunel B., Syst. Appl. Microbiol. 29(7), 2006
PMID: 16413160

AUTHOR UNKNOWN, 2001

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