Sinorhizobium fredii HH103 does not strictly require KPS and/or EPS to nodulate Glycyrrhiza uralensis, an indeterminate nodule-forming legume

Archives of Microbiology

Volumn 194, Issue 2, 2012, Pages 87-102

  Margaret Oliver, Isabel ^a   Lei, Wang ^b   Parada, Maribel ^a,d   Rodríguez Carvajal, Miguel A ^a   Crespo Rivas, Juan C ^a   Hidalgo, Ángeles ^a   Gil Serrano, Antonio ^a   Moreno, Javier ^a   Rodríguez Navarro, Dulce N ^c   Buendía Clavería, Ana ^a   Ollero, Javier ^a   Ruiz Sainz, José E ^a   Vinardell, José M ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c IFAPA CENTRO EL TORUÑO   (Spain)

^d UNIVERSIDAD DE LA FRONTERA   (Chile)

Author keywords

Glycine max; Glycyrrhiza uralensis; KPS mutants; rkp 1 region; Sinorhizobium fredii

Indexed keywords

BACTERIAL POLYSACCHARIDE; CAPSULAR POLYSACCHARIDE; EXOPOLYSACCHARIDE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; CULTIVAR; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GLYCYRRHIZA URALENSIS; NITROGEN DYNAMICS; NODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT MICROORGANISM INTERACTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RKPA GENE; RKPI GENE; SINORHIZOBIUM FREDII; SOYBEAN;

BACTERIAL PROTEINS; FLAVONOIDS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; GLYCYRRHIZA URALENSIS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; MUTATION; NITROGEN FIXATION; POLYSACCHARIDES, BACTERIAL; ROOT NODULES, PLANT; SINORHIZOBIUM; SINORHIZOBIUM FREDII; SOYBEANS; SYMBIOSIS;

BACTERIA (MICROORGANISMS); GLYCINE MAX; GLYCYRRHIZA URALENSIS; SINORHIZOBIUM; SINORHIZOBIUM FREDII;

EID: 84857058564     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-011-0729-2     Document Type: Article

References (47)

1. Becker A, Pühler A (1998) Production of exopolysaccharides. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae: molecular biology of model plant-associated bacteria. Kluwer, Dordrecht, pp 97-118
2. A Becker M Schimdt W Jäger A Pühler 1995 New gentamicin-resistance and lacZ promote-probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions Gene 162 37 39 7557413 10.1016/0378-1119(95)00313-U 1:CAS:528:DyaK2MXotFClurw%3D
3. A Becker N Fraysse L Sharypova 2005 Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides Mol Plant Microbe Interact 18 899 905 16167760 10.1094/MPMI-18-0899 1:CAS:528:DC%2BD2MXpsFGju7g%3D (Pubitemid 41170154)
4. JE Beringer 1974 R factor transfer in Rhizobium leguminosarum J Gen Microbiol 84 188 198 4612098 1:STN:280:DyaE2M%2FmtFeltA%3D%3D
5. J Bliss C Garon R Silver 1996 Polysialic acid export in Escherichia coli K1: the role of KpsT, the ATP-binding component of an ABC transporter, in chain translocation Glycobiology 6 445 452 8842709 10.1093/glycob/6.4.445 1:CAS:528:DyaK28XkslOgtbc%3D (Pubitemid 26281047)
6. AM Buendía-Clavería M Chamber JE Ruiz-Sainz 1989 A comparative study of the physiological characteristics, plasmid content and symbiotic properties of different Rhizobium fredii strains Syst Appl Microbiol 12 203 209 (Pubitemid 19284774)
7. AM Buendía-Clavería A Moussaid FJ Ollero JM Vinardell A Torres J Moreno AM Gil-Serrano MA Rodríguez-Carvajal P Tejero-Mateo JL Peart NJ Brewin JE Ruiz-Sainz 2003 A purL mutant of Sinorhizobium fredii HH103 is symbiotically defective and altered in its lipopolysaccharide Microbiology 149 1807 1818 12855732 10.1099/mic.0.26099-0 (Pubitemid 36874326)
8. G Chataigné F Conderc V Poinsot 2008 Polysaccharides analysis of sinorhizobial capside by on-line anion exchange chromatography with pulse amperiometric detection and mass spectrometry coupling J Chromatogr A 1185 241 250 18275965 10.1016/j.chroma.2008.01.065
9. Collmer A, Bauer DW, He SY, Lindeberg M, Kelemu S, Rodriguez-Palenzuela P, Burr TJ, Chatterjee AK (1991) Pectic enzyme production and bacterial plant pathogenicity. In: Hennecke H, Verma DPS (eds) Advances in molecular genetics of plant-microbe interactions, vol 1. Kluwer, Dordrecht, pp 65-72
10. JC Crespo-Rivas I Margaret F Pérez-Montaño FJ López-Baena JM Vinardell FJ Ollero J Moreno JE Ruiz-Sainz AM Buendía-Clavería 2007 A pyrF auxotrophic mutant of Sinorhizobium fredii HH103 is impaired in its symbiotic interactions with soybean and other legumes Int Microbiol 10 169 176 18075998 1:CAS:528:DC%2BD2sXht1emurvM (Pubitemid 47414666)
11. JC Crespo-Rivas I Margaret A Hidalgo AM Buendía-Clavería FJ Ollero FJ López-Baena PS Murdoch MA Rodríguez-Carvajal ME Soria-Díaz M Reguera J Lloret DP Sumpton JA Mosely JE Thomas-Oates AAN van Brussel A Gil-Serrano JM Vinardell JE Ruiz-Sainz 2009 Sinorhizobium fredii HH103 cgs mutants are unable to nodulate determinate- and indeterminate nodule-forming legumes and overproduce an altered EPS Mol Plant Microbe Interact 22 575 588 19348575 10.1094/MPMI-22-5-0575 1:CAS:528:DC%2BD1MXks1Wns7s%3D
12. MCCP De Lyra FJ López-Baena N Madinabeitia JM Vinardell MR Espuny MT Cubo RA Bellogín JE Ruiz-Sainz FJ Ollero 2006 Inactivation of the Sinorhizobium fredii HH103 rhcJ gene abolishes nodulation outer proteins (Nops) secretion and decreases the symbiotic capacity with soybean Int Microbiol 9 125 133 (Pubitemid 44047825)
13. JA Downie 2010 The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots FEMS Microbiol Rev 34 150 170 20070373 10.1111/j.1574-6976.2009.00205.x 1:CAS:528:DC%2BC3cXitFClsLc%3D
14. DH Figurski DR Helinski 1979 Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans Proc Natl Acad Sci USA 76 1648 1652 377280 10.1073/pnas.76.4.1648 1:CAS:528:DyaE1MXitVSitr0%3D (Pubitemid 9175374)
15. N Fraysse C Couderc V Poinsot 2003 Surface polysaccharides involvement in establishing the Rhizobium-legume symbiosis Eur J Biochem 270 1365 1380 12653992 10.1046/j.1432-1033.2003.03492.x 1:CAS:528:DC%2BD3sXivFWnsLo%3D (Pubitemid 36459575)
16. N Fraysse B Lindner Z Kaczynski L Sharypova O Holst K Niehaus V Poisont 2005 Sinorhizobium meliloti strain 1021 produces a low-molecular mass capsular polysaccharide that is a homopolymer of 3-deoxy-d-manno-oct-2-ulosonic acid harbouring a phospholipidic anchor Glycobiology 15 101 108 15355932 10.1093/glycob/cwh142 1:CAS:528:DC%2BD2cXhtVKqu7nI (Pubitemid 40202043)
17. AM Friedman SR Long SE Brown WJ Buikema FM Ausubel 1982 Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants Gene 18 289 296 6290332 10.1016/0378-1119(82)90167-6 1:CAS:528:DyaL38XlslKitbo%3D (Pubitemid 13233003)
18. DJ Gage 2004 Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes Mol Biol Rev 68 280 300 10.1128/MMBR.68.2.280-300.2004 1:CAS:528:DC%2BD2cXlsl2hu7o%3D (Pubitemid 38756866)
19. KE Gibson H Kobayasi GC Walker 2008 Molecular determinants of a symbiotic chronic infection Ann Rev Genet 42 413 441 18983260 10.1146/annurev.genet.42. 110807.091427 1:CAS:528:DC%2BD1cXhsFeqsrfE
20. AM Gil-Serrano MA Rodríguez-Carvajal P Tejero-Mateo JL Espartero M Menendez J Corzo JE Ruiz-Sainz AM Buendía-Clavería 1999 Structural determination of a 5-acetamido-3,5, 7,9-tetradeoxy-7-(3- hydroxybutyramido)-l-glycero-l-manno-nonusolonic acid-containing homopolysaccharide isolated from Sinorhizobium fredii HH103 Biochem J 342 527 535 10477263 10.1042/0264-6021:3420527 1:CAS:528:DyaK1MXmsVygsrw%3D (Pubitemid 29452637)
21. A Hidalgo I Margaret JC Crespo-Rivas M Parada PS Murdoch A Lopez AM Buendia-Claveria J Moreno M Albareda AM Gil-Serrano MA Rodriguez-Carvajal JM Palacios JE Ruiz-Sainz JM Vinardell 2010 The rkpU gene of Sinorhizobium fredii HH103 is required for bacterial KPS production and for efficient nodulation with soybean but not with Vigna unguiculata Microbiology 156 3398 3411 20688828 10.1099/mic.0.042499-0 1:CAS:528:DC%2BC3cXhsFCiurvK
22. KM Jones H Kobayashi BW Davies ME Taga G Walker 2007 How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model Nature 5 619 633 1:CAS:528:DC%2BD2sXns12htbc%3D (Pubitemid 47074117)
23. Kannenberg EL, Reuhs BL, Fosberg LS, Carlson RW (1998) Lipopolysaccharide and K-antigens: their structures, biosynthesis and functions. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae: molecular biology of model plant-associated bacteria. Kluwer, Dordrecht, pp 119-154
24. M Kinkema PT Scott PM Gresshoff 2006 Legume nodulation: successful symbiosis through short- and long-distance signalling Funct Plant Biol 33 707 721 10.1071/FP06056 1:CAS:528:DC%2BD28XnsFCrsLg%3D (Pubitemid 44162015)
25. E Kiss BL Reuhs JS Kim A Kereszt G Petrovics P Putnoky I Dusha RW Carlson A Kondorosi 1997 The rkpGHI and -J genes are involved in capsular polysaccharide production by Rhizobium meliloti J Bacteriol 179 2132 2140 9079896 1:CAS:528:DyaK2sXit1Clsr0%3D (Pubitemid 27146865)
26. E Kiss A Kereszt F Barta B Stephens BL Reuhs A Kondorosi P Putnoky 2001 The rkp-3 region of Sinorhizobium meliloti Rm41 contains strain-specific genes that determine K antigen structure Mol Plant Microbe Interact 14 1395 1403 11768534 10.1094/MPMI.2001.14.12.1395 1:CAS:528:DC%2BD3MXpt1SmsLk%3D (Pubitemid 34018327)
27. Y Lamrabet RA Bellogín T Cubo MR Espuny A Gil-Serrano HB Krishnan M Megías FJ Ollero SG Pueppke JE Ruiz-Sainz HP Spaink P Tejero-Mateo J Thomas-Oates JM Vinardell 1999 Mutation in GDP-fucose synthesis genes of Sinorhizobium fredii alters Nod factors and significantly decreases competitiveness to nodulate soybeans Mol Plant Microbe Interact 12 207 217 10065558 10.1094/MPMI.1999.12.3.207 1:CAS:528:DyaK1MXisVKjtbc%3D (Pubitemid 29103118)
28. N Madinabeitia RA Bellogín A Buendía-Clavería M Camacho T Cubo MR Espuny AM Gil-Serrano MCCP Lyra A Moussaid FJ Ollero ME Soria-Díaz JM Vinardell J Zeng JE Ruiz-Sainz 2002 Sinorhizobium fredii HH103 has a truncated nolO gene due to a -1 frameshift mutation that is conserved among other geographically distant S. fredii strains Mol Plant Microbe Interact 15 150 159 11878319 10.1094/MPMI.2002.15.2.150 1:CAS:528: DC%2BD38XhsFChurY%3D (Pubitemid 34186397)
29. LW Meinhardt HB Krishnan PA Balatti SG Pueppke 1993 Molecular cloning and characterization of a sym plasmid locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USDA257 Mol Microbiol 9 17 29 8412662 10.1111/j.1365-2958.1993.tb01665.x 1:CAS:528:DyaK3sXmtFyrsL0%3D (Pubitemid 23217734)
30. MG Müller LS Forsberg DH Keating 2009 The rkp-1 cluster is required for secretion of Kdo homopolymeric capsular polysaccharide in Sinorhizobium meliloti strain Rm1021 J Bacteriol 191 6988 7000 19734304 10.1128/JB.00466-09
31. M Parada JM Vinardell FJ Ollero A Hidalgo R Gutiérrez AM Buendía-Clavería W Lei I Margaret FJ López-Baena AM Gil-Serrano MA Rodríguez-Carvajal J Moreno JE Ruiz-Sainz 2006 Sinorhizobium fredii HH103 mutants affected in capsular polysaccharide (KPS) are impaired for nodulation with soybean and Cajanus cajans Mol Plant Microbe Interact 19 43 52 16404952 10.1094/MPMI-19-0043 1:CAS:528:DC%2BD28XisVWjsw%3D%3D (Pubitemid 43011197)
32. BJ Pellock HP Cheng GC Walker 2000 Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides J Bacteriol 182 4310 4318 10894742 10.1128/JB.182.15.4310-4318.2000 1:CAS:528: DC%2BD3cXlt1Sgs7Y%3D (Pubitemid 30463796)
33. G Petrovics P Putnoky B Reuhs J Kim TA Thorp KD Noel RW Carlson A Kondorosi 1993 The presence of a novel type of surface polysaccharide in Rhizobium meliloti requires a new fatty acid synthase-like genes cluster involved in symbiotic nodule development Mol Microbiol 8 1083 1094 8361353 10.1111/j.1365-2958.1993.tb01653.x 1:CAS:528:DyaK3sXlsFGqt7s%3D (Pubitemid 23187027)
34. P Prentki HM Krisch 1984 In vitro insertional mutagenesis with a selectable DNA fragment Gene 29 303 313 6237955 10.1016/0378-1119(84)90059-3 1:CAS:528:DyaL2cXmt1equ7c%3D (Pubitemid 14038235)
35. BL Reuhs SB Stephens JS Kim J Glenn J Pzrytycki T Ojanen-Reuhs 1999 Epitope identification for a panel of anti-Rhizobium meliloti monoclonal antibodies and application to the analysis of K antigens and lipopolysaccharides from bacteroids Appl Environ Microbiol 65 5186 5191 10543844 1:CAS:528:DyaK1MXnt1Wls7g%3D
36. MA Rodríguez-Carvajal P Tejero-Mateo JL Espartero JE Ruiz-Sainz AM Buendía-Clavería FJ Ollero SS Yang AM Gil-Serrano 2001 Determination of the chemical structure of the capsular polysaccharide of strain B33, a fast-growing soya bean-nodulating bacterium isolated from an arid region of China Biochem J 357 505 511 11439101 10.1042/0264-6021:3570505 (Pubitemid 32701788)
37. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
38. A Schafer A Tauch W Jager J Kalinowski G Thierbach A Pühler 1994 Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum Gene 145 69 73 8045426 10.1016/0378-1119(94)90324-7 1:STN:280:DyaK2czitVOruw%3D%3D (Pubitemid 24224965)
39. R Simon 1984 High frequency mobilization of gram-negative bacterial replicons by the in vivo constructed Tn5-Mob transposon Mol Gen Genet 196 413 420 6094969 10.1007/BF00436188 1:CAS:528:DyaL2cXmt1ektrk%3D (Pubitemid 14010694)
40. S Simsek T Ojanen-Reuhs C Marie B Reuhs 2009 An apigenin-induced decrease in K-antigen production by Sinorhizobium sp. NGR234 is y4gM and nodD1-dependent Carbohydr Res 344 1947 1950 19679303 10.1016/j.carres.2009.07.006 1:CAS:528:DC%2BD1MXhtF2gsrnF
41. J Thomas-Oates J Bereszczak E Edwards A Gill S Noreen JC Zhou MZ Chen LH Miao FL Xie JK Yang Q Zhou SS Yang XH Li L Wang HP Spaink HRM Schlaman M Harteveld CL Díaz AAN van Brussel M Camacho DN Rodríguez-Navarro C Santamaría F Temprano JM Acebes RA Bellogín AM Buendía-Clavería MT Cubo MR Espuny AM Gil R Gutiérrez A Hidalgo FJ López-Baena N Madinabeitia C Medina FJ Ollero JM Vinardell JE Ruiz-Sainz 2003 A catalogue of molecular, physiological and symbiotic properties of soybean-nodulating rhizobial strains from different soybean cropping areas of China Syst Appl Microbiol 26 453 465 14529189 10.1078/072320203322497491 1:CAS:528:DC%2BD3sXovFCisL4%3D (Pubitemid 37139766)
42. EM Vanderlinde JJ Harrison A Muszynski RW Carlson RJ Turner CK Yost 2010 Identification of a novel ABC transporter required for desiccation tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841 FEMS Microbiol Ecol 71 327 340 20030718 10.1111/j.1574-6941.2009.00824.x 1:CAS:528: DC%2BC3cXitFCmu7c%3D
43. JM Vinardell FJ López-Baena A Hidalgo FJ Ollero R Bellogín MR Espuny F Temprano F Romero HB Krishnan SG Pueppke JE Ruiz-Sainz 2004 The effect of FITA mutations on the symbiotic properties of Sinorhizobium fredii varies in a chromosomal-background-dependent manner Arch Microbiol 181 144 154 14689165 10.1007/s00203-003-0635-3 1:CAS:528:DC%2BD2cXmvVGgsQ%3D%3D (Pubitemid 38221651)
44. JM Vinardell FJ Ollero A Hidalgo FJ López-Baena C Medina K Ivanov-Vangelov M Parada N Madinabeitia MR Espuny RA Bellogín M Camacho DN Rodríguez-Navarro ME Soria-Díaz AM Gil-Serrano JE Ruiz-Sainz 2004 NolR regulates diverse symbiotic signals of Sinorhizobium fredii HH103 Mol Plant Microbe Interact 17 676 685 15195950 10.1094/MPMI.2004.17.6.676 1:CAS:528:DC%2BD2cXktlOmurk%3D (Pubitemid 38642211)
45. Vincent JM (1970) Appendix III. The modified Fähraeus slide technique. In: Vincent JM (ed) A manual for the practical study of root nodule bacteria. Blackwell Scientific Publications, Oxford, pp 144-145
46. JG Wallis JL Watts J Browse 2002 Polyunsaturated fatty acid synthesis: what will they think of next? Trends Biochem Sci 27 467 473 12217522 10.1016/S0968-0004(02)02168-0 1:CAS:528:DC%2BD38Xms1Oltbo%3D (Pubitemid 35246256)
47. S Yang RA Bellogín AM Buendía-Clavería M Camacho M Chen T Cubo A Daza CL Díaz MR Espuny R Gutiérrez M Harteveld XH Li MCCP Lyra N Madinabeitia C Medina L Miao FJ Ollero MMA Olsthoorn DN Rodríguez C Santamaría HRM Schlaman HP Spaink F Temprano JE Thomas-Oates AAN van Brussel JM Vinardell F Xie J Yang HY Zhang J Zhen J Zhou JE Ruiz-Sainz 2001 Effect of pH and soybean cultivars on the quantitative analyses of soybean rhizobia populations J Biotechnol 91 243 255 11566395 10.1016/S0168-1656(01)00340-6 1:CAS:528:DC%2BD3MXmvVKltbo%3D (Pubitemid 32868786)