Fast induction of biosynthetic polysaccharide genes lpxA, lpxE, and rkpI of Rhizobium sp. strain PRF 81 by common bean seed exudates is indicative of a key role in symbiosis

Functional and Integrative Genomics

Volumn 13, Issue 2, 2013, Pages 275-283

  Oliveira, Luciana Ruano ^a,b   Rodrigues, Elisete Pains ^b   Marcelino Guimarães, Francismar Corrêa ^a   Oliveira, André Luiz Martinez ^b   Hungria, Mariangela ^a,b  

^a EMBRAPA CERRADOS   (Brazil)

^b STATE UNIVERSITY OF LONDRINA   (Brazil)

Author keywords

Biological nitrogen fixation; K Antigen polysaccharide; LPS; Rhizobium tropici; RT qPCR; Symbiosis

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; IPXA GENE; IPXE GENE; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHIZOBIUM; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM RADIOBACTER; RKPI GENE; SINORHIZOBIUM; SYMBIOSIS; UPREGULATION;

GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; PHASEOLUS; PHYLOGENY; PLANT EXUDATES; POLYSACCHARIDES, BACTERIAL; RHIZOBIUM; SEEDS; SYMBIOSIS;

AGROBACTERIUM TUMEFACIENS; PHASEOLUS VULGARIS; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM SP.; RHIZOBIUM TROPICI; SINORHIZOBIUM SP.;

EID: 84878770280     PISSN: 1438793X     EISSN: 14387948     Source Type: Journal    
DOI: 10.1007/s10142-013-0322-7     Document Type: Article

References (55)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402
2. Aziz R, Bartels D, Best A, DeJongh M, Disz T, Edwards R, Formsma K, Gerdes S, Glass E, Kubal M (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75
3. Becker A, Bergès H, Krol E, Bruand C, Rüberg S, Capela D, Lauber E, Meilhoc E, Ampe F, de Bruijn FJ (2004) Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol Plant-Microbe Interact 17:292-303. doi: 10.1094/MPMI.2004.17.3. 292
4. Becker A, Fraysse N, Sharypova L (2005) Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol Plant-Microbe Interact 18:899-905. doi: 10.1094/mpmi-18-0899
5. Beringer J (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188-198. doi: 10.1099/00221287-84-1-188
6. Broughton W, Hanin M, Relić B, Kopciñska J, Golinowski W, Şimşek Ş, Ojanen-Reuhs T, Reuhs B, Marie C, Kobayashi H (2006) Flavonoid-inducible modifications to rhamnan O antigens are necessary for Rhizobium sp. strain NGR234-legume symbioses. J Bacteriol 188:3654-3663. doi: 10.1128/JB.188.10.3654-3663.2006
7. Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355-1365. doi: 10.1111/j.1365-2672.2007.03366.x
8. D'Haeze W, Holsters M (2004) Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol 12:555-561. doi: 10.1016/j.tim.2004.10. 009
9. Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150-170. doi: 10.1111/j.1574-6976.2009.00205.x
10. Farrell RE Jr (1998) RNA methodologies: a laboratory guide for isolation and characterization. Academic, San Diego, p 533
11. Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol Lett 285:1-9. doi: 10.1111/j.1574-6968.2008.01254.x
12. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution:783-791
13. Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, Gresshoff PM (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52:61-76. doi: 10.1111/j.1744-7909.2010. 00899.x
14. Fraysse N, Jabbouri S, Treilhou M, Couderc F, Poinsot V (2002) Symbiotic conditions induce structural modifications of Sinorhizobium sp. NGR234 surface polysaccharides. Glycobiology 12:741-748. doi: 10.1093/glycob/cwf078
15. Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur J Biochem 270:1365-1380. doi: 10.1046/j.1432-1033.2003.03492.x
16. Gil Serrano AM, Franco-Rodríguez G, González-Jiménez I, Tejero-Mateo P, Molina JM, Dobado J, Megías M, Romero MJ (1993) The structure and molecular mechanics calculations of the cyclic (1 → 2)-β-D-glucan secreted by Rhizobium tropici CIAT 899. J Mol Struct 301:211-226. doi: 10.1016/0022-2860(93)80246-R
17. Gil-Serrano A, del Junco AS, Tejero-Mateo P, Megias M, Caviedes MA (1990) Structure of the extracellular polysaccharide secreted by Rhizobium leguminosarum var. phaseoli CIAT 899. Carbohydr Res 204:103-107. doi: 10.1016/0008-6215(90)84025-p
18. Gil-Serrano A, González-Jiménez I, Tejero-Mateo P, Megias M, Romero-Vazquez M (1994) Analysis of the lipid moiety of lipopolysaccharide from Rhizobium tropici CIAT899: identification of 29-hydroxytriacontanoic acid. J Bacteriol 176:2454-2457
19. Gil-Serrano AM, González-Jiménez I, Tejero Mateo P, Bernabé M, Jiménez-Barbero J, Megías M, Jesús Romero-Vázquez M (1995) Structural analysis of the O-antigen of the lipopolysaccharide of Rhizobium tropici CIAT899. Carbohydr Res 275:285-294. doi: 10.1016/0008-6215(95)00178-v
20. Grange L, Hungria M (2004) Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol Biochem 36:1389-1398
21. Hungria M, Neves MCP (1987) Cultivar and Rhizobium strain effect on nitrogen fixation and transport in Phaseolus vulgaris L. Plant Soil 103:111-121. doi: 10.1007/BF02370675
22. Hungria M, Joseph CM, Phillips DA (1991a) Anthocyanidins and flavonols, major nod gene inducers from seeds of a black-seeded common bean (Phaseolus vulgaris L.). Plant Physiol 97:751. doi: 10.1104/pp.97.2.751
23. Hungria M, Joseph CM, Phillips DA (1991b) Rhizobium nod gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris L.). Plant Physiol 97:759. doi: 10.1104/pp.97.2.759
24. Hungria M, Johnston A, Phillips DA (1992) Effects of flavonoids released naturally from bean (Phaseolus vulgaris) on nodD-regulated gene transcription in Rhizobium leguminosarum bv. phaseoli. Mol Plant-Microbe Interact 5:199-203
25. Hungria M, DdS A, Chueire LMO, Probanza A, Guttierrez-Mañero FJ, Megías M (2000) Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biol Biochem 32:1515-1528. doi: 10.1016/s0038-0717(00)00063-8
26. Hungria M, Campo RJ, Mendes IC (2003) Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biol Fertil Soils 39:88-93. doi: 10.1007/s00374-003-0682-6
27. Ingram BO, Sohlenkamp C, Geiger O, Raetz CRH (2010) Altered lipid A structures and polymyxin hypersensitivity of Rhizobium etli mutants lacking the LpxE and LpxF phosphatases. Biochim Biophys Acta 1801:593-604. doi: 10.1016/j.bbalip.2010.02.001
28. Kannenberg EL, Carlson RW (2001) Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol Microbiol 39:379-392. doi: 10.1046/j.1365-2958.2001.02225.x
29. Karbarz MJ, Kalb SR, Cotter RJ, Raetz CRH (2003) Expression cloning and biochemical characterization of a Rhizobium leguminosarum lipid A 1-phosphatase. J Biol Chem 278:39269-39279. doi: 10.1074/jbc.M305830200
30. Karbarz MJ, Six DA, Raetz CRH (2009) Purification and characterization of the lipid A 1-phosphatase LpxE of Rhizobium leguminosarum. J Biol Chem 284:414-425. doi: 10.1074/jbc.M808390200
31. Kiss E, Reuhs BL, Kim JS, Kereszt A, Petrovics G, Putnoky P, Dusha I, Carlson RW, Kondorosi A (1997) The rkpGHI and -J genes are involved in capsular polysaccharide production by Rhizobium meliloti. J Bacteriol 179:2132-2140
32. Le Quéré AJ-L, Deakin WJ, Schmeisser C, Carlson RW, Streit WR, Broughton WJ, Forsberg LS (2006) Structural characterization of a K-antigen capsular polysaccharide essential for normal symbiotic infection in Rhizobium sp. NGR234. J Biol Chem 281:28981-28992. doi: 10.1074/jbc.M513639200
33. Margaret-Oliver I, Lei W, Parada M, Rodríguez-Carvajal MA, Crespo-Rivas JC, Hidalgo Á, Gil-Serrano A, Moreno J, Rodríguez- Navarro DN, Buendía-Clavería A (2012) Sinorhizobium fredii HH103 does not strictly require KPS and/or EPS to nodulate Glycyrrhiza uralensis, an indeterminate nodule-forming legume. Arch Microbiol 194:87-102. doi: 10.1007/s00203-011-0729-2
34. Martinez-Romero E (2003) Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 252:11-23. doi: 10.1023/A:1024199013926
35. Metzger LE IV, Raetz CRH (2010) An alternative route for UDP-diacylglucosamine hydrolysis in bacterial lipid A biosynthesis. Biochemistry 49:6715-6726. doi: 10.1021/bi1008744
36. Michiels J, Dombrecht B, Vermeiren N, Xi C, Luyten E, Vanderleyden J (1998) Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiol Ecol 26:193-205. doi: 10.1016/S0168-6496(98)00035-X
37. Noel KD, Duelli DM, Tao H, Brewin NJ (1996) Antigenic change in the lipopolysaccharide of Rhizobium etli CFN42 induced by exudates of Phaseolus vulgaris. Mol Plant-Microbe Interact 9:180-186
38. Noel KD, Box JM, Bonne VJ (2004) 2-O-Methylation of fucosyl residues of a rhizobial lipopolysaccharide is increased in response to host exudate and is eliminated in a symbiotically defective mutant. Appl Environ Microbiol 70:1537-1544. doi: 10.1128/AEM.70.3.1537-1544.2004
39. Oliveira LR, Marcelino FC, Barcellos FG, Rodrigues EP, Megías M, Hungria M (2010) The nodC, nodG, and glgX genes of Rhizobium tropici strain PRF 81. Funct Integr Genom 10:425-431. doi: 10.1007/s10142-009-0151-x
40. Ormeño-Orrillo E, Menna P, Almeida LGP, Ollero FJ, Nicolás MF, Rodrigues EP, Nakatani AS, Batista JSS, Chueire LMO, Souza RC (2012) Genomic basis of broad host range and environmental adaptability of Rhizobium tropici CIAT 899 and Rhizobium sp. PRF 81 which are used in inoculants for common bean (Phaseolus vulgaris L.). BMC Genom 13:735
41. Parada M, Vinardell JM, Ollero FJ, Hidalgo Á, Gutiérrez R, Buendía-Clavería AM, Lei W, Margaret I, López-Baena FJ, Gil-Serrano AM (2006) Sinorhizobium fredii HH103 mutants affected in capsular polysaccharide (KPS) are impaired for nodulation with soybean and Cajanus cajan. Mol Plant-Microbe Interact 19:43-52. doi: 10.1094/MPMI-19-0043
42. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36. doi: 10.1093/nar/30.9.e36
43. 2 with common bean (Phaseolus vulgaris L.). Soil Biol Biochem 39:1851-1864. doi: 10.1016/j.soilbio.2007.01.001
44. Pinto FGS, Chueire LMO, Vasconcelos ATR, Nicolás MF, Almeida LGP, Souza RC, Menna P, Barcellos FG, Megías M, Hungria M (2009) Novel genes related to nodulation, secretion systems, and surface structures revealed by a genome draft of Rhizobium tropici strain PRF 81. Funct Integr Genom 9:263-270. doi: 10.1007/s10142-009-0109-z
45. Que NLS, Ribeiro AA, Raetz CRH (2000) Two-dimensional NMR spectroscopy and structures of six lipid A species from Rhizobium etli CE3. J Biol Chem 275:28017-28027. doi: 10.1074/jbc.M004009200
46. Raetz CR, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76:295-329. doi: 10.1146/annurev.biochem.76.010307.145803
47. Reuhs BL, Kim JS, Badgett A, Carlson RW (1994) Production of cell-associated polysaccharides of Rhizobium fredii USDA205 is modulated by apigenin and host root extract. MPMI-Mol Plant Microbe Interact 7:240-247. doi: 10.1094/MPMI-7-0240
48. Ribeiro RA, Rogel MA, López-López A, Ormeño-Orrillo E, Barcellos FG, Martínez J, Thompson FL, Martínez-Romero E, Hungria M (2012) Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int J Syst Evol Microbiol 62:1179-1184
49. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
50. Schultze M, Kondorosi Á (1996) The role of lipochitooligosaccharides in root nodule organogenesis and plant cell growth. Curr Opin Genet Dev 6:631-638. doi: 10.1016/s0959-437x(96)80094-3
51. Simsek S, Ojanen-Reuhs T, Marie C, Reuhs BL (2009) An apigenin-induced decrease in K-antigen production by Sinorhizobium sp. NGR234 is y4gM- and nodD1-dependent. Carbohydr Res 344:1947-1950. doi: 10.1016/j.carres.2009.07.006
52. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030-11035
53. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
54. Vincent JM (1970) A manual for the practical study of the root-nodule bacteria. International biological programme handbook, 15. Blackwell Oxford pp. 164
55. Wang X, Quinn PJ (2010) Lipopolysaccharide: biosynthetic pathway and structure modification. Prog Lipid Res 49:97-107. doi: 10.1016/j.plipres.2009. 06.002