Molecular insights into bacteroid development during Rhizobium-legume symbiosis

FEMS Microbiology Reviews

Volumn 37, Issue 3, 2013, Pages 364-383

  Haag, Andreas F ^a   Arnold, Markus F F ^a   Myka, Kamila K ^a   Kerscher, Bernhard ^a   Dall'Angelo, Sergio ^a   Zanda, Matteo ^a,b   Mergaert, Peter ^c   Ferguson, Gail P ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b CNR   (Italy)

^c CNRS   (France)

Author keywords

Antimicrobial peptides; BacA; Bacteroid differentiation; Cysteine rich peptides; Lipopolysaccharide; Nodule specific; Rhizobium legume symbiosis

Indexed keywords

BACA PROTEIN; BACTERIAL PROTEIN; FATTY ACID; NITROGEN; UNCLASSIFIED DRUG;

BACTERIAL GROWTH; BRUCELLA ABORTUS; BRUCELLOSIS; ENVIRONMENTAL STRESS; FATTY ACID SYNTHESIS; LEGUME; MYCOBACTERIUM TUBERCULOSIS; NITROGEN FIXATION; NONHUMAN; PATHOGENESIS; PROTEIN FUNCTION; REVIEW; RHIZOBIUM; SINORHIZOBIUM MELILOTI; SYMBIOSIS; TUBERCULOSIS;

EID: 85027945183     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/1574-6976.12003     Document Type: Review

References (146)

1. Alunni B, Kevei Z, Redondo-Nieto M, Kondorosi A, Mergaert P & Kondorosi E (2007) Genomic organization and evolutionary insights on GRP and NCR genes, two large nodule-specific gene families in Medicago truncatula. Mol Plant Microbe Interact 20: 1138-1148.
2. Anderson RJ (1943) The chemistry of the lipids of the tubercle bacillus. Yale J Biol Med 15: 311-345.
3. Ardissone S, Kobayashi H, Kambara K, Rummel C, Noel KD, Walker GC, Broughton WJ, Deakin WJ (2011) Role of BacA in lipopolysaccharide synthesis, peptide transport and nodulation by Rhizobium sp. NGR234. Journal of Bacteriology 193: 2218-2228.
4. Ardourel M, Demont N, Debelle FD et al. (1994) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair-cells and induction of plant symbiotic developmental responses. Plant Cell 6: 1357-1374.
5. Arrighi JF, Barre A, Ben Amor B et al. (2006) The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265-279.
6. Barnett MJ, Toman CJ, Fisher RF & Long SR (2004) A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote-host interaction. P Natl Acad Sci USA 101: 16636-16641.
7. Barry CE III, Boshoff HI, Dartois V et al. (2009) The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 7: 845-855.
8. Basu SS, Karbarz MJ & Raetz CR (2002) Expression cloning and characterization of the C28 acyltransferase of lipid A biosynthesis in Rhizobium leguminosarum. J Biol Chem 277: 28959-28971.
9. Becker A, Bergès H, Krol E et al. (2004) Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol Plant Microbe Interact 17: 292-303.
10. Benincasa M, Scocchi M, Podda E, Skerlavaj B, Dolzani L & Gennaro R (2004) Antimicrobial activity of Bac7 fragments against drug-resistant clinical isolates. Peptides 25: 2055-2061.
11. Benincasa M, Mattiuzzo M, Herasimenka Y, Cescutti P, Rizzo R & Gennaro R (2009) Activity of antimicrobial peptides in the presence of polysaccharides produced by pulmonary pathogens. J Pept Sci 15: 595-600.
12. Bhat UR, Carlson RW, Busch M & Mayer H (1991) Distribution and phylogenetic significance of 27-hydroxy-octacosanoic acid in lipopolysaccharides from bacteria belonging to the alpha-2 subgroup of Proteobacteria. Int J Syst Bacteriol 41: 213-217.
13. Bisseling T, Bos RCVD, Kammen AV, Ploeg MVD, Duijn PV & Houwers A (1977) Cytofluorometrical determination of the DNA contents of bacteroids and corresponding broth-cultured Rhizobium bacteria. J Gen Microbiol 101: 79-84.
14. Bisseling T, Limpens E, Franken C, Smit P, Willemse J & Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302: 630-633.
15. Bolaños L, Redondo-Nieto M, Rivilla R, Brewin NJ & Bonilla I (2004) Cell surface interactions of Rhizobium bacteroids and other bacterial strains with symbiosomal and peribacteroid membrane components from pea nodules. Mol Plant Microbe Interact 17: 216-223.
16. Bonaldi K, Gargani D, Prin Y et al. (2011) Nodulation of Aeschynomene afraspera and A. indica by photosynthetic Bradyrhizobium sp. strain ORS285: the nod-dependent versus the nod-independent symbiotic interaction. Mol Plant Microbe Interact 24: 1359-1371.
17. Brewin NJ (2004) Plant cell wall remodelling in the Rhizobium-legume symbiosis. Crit Rev Plant Sci 23: 293-316.
18. Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3: 238-250.
19. Brown DB, Huang YC, Kannenberg EL, Sherrier DJ & Carlson RW (2011) An acpXL mutant of Rhizobium leguminosarum bv. phaseoli lacks 27-hydroxyoctacosanoic acid in its lipid A and is developmentally delayed during symbiotic infection of the determinate nodulating host plant Phaseolus vulgaris. J Bacteriol 193: 4766-4778.
20. Brozek KA, Carlson RW & Raetz CRH (1996) A special acyl carrier protein for transferring long hydroxylated fatty acids to lipid A in Rhizobium. J Biol Chem 271: 32126-32136.
21. Campbell GR, Reuhs BL & Walker GC (2002) Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. P Natl Acad Sci USA 99: 3938-3943.
22. Campbell GR, Sharypova LA, Scheidle H, Jones KM, Niehaus K, Becker A & Walker GC (2003) Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants. J Bacteriol 185: 3853-3862.
23. Capela D, Filipe C, Bobik C, Batut J & Bruand C (2006) Sinorhizobium meliloti differentiation during symbiosis with alfalfa: a transcriptomic dissection. Mol Plant Microbe Interact 19: 363-372.
24. Cheng HP & Walker GC (1998) Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 180: 5183-5191.
25. Cho MJ & Harper JE (1991) Effect of inoculation and nitrogen on isoflavonoid concentration in wild-type and nodulation-mutant soybean roots. Plant Physiol 95: 435-442.
26. Chou MX, Wei XY, Chen DS & Zhou JC (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.
27. Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103: 1355-1365.
28. Crockard A, Bjourson J, Dazzo B & Cooper JE (2002) A white clover nodulin gene, dd23b, encoding a cysteine cluster protein, is expressed in roots during the very early stages of interaction with Rhizobium leguminosarum biovar trifolii and after treatment with chitolipooligosaccharide Nod factors. J Plant Res 115: 439-447.
29. Cronan JE & Thomas J (2009) Bacterial fatty acid synthesis and its relationships with polyketide synthetic pathways. Methods Enzymol, 459: 395-433.
30. Davidson AL & Chen J (2004) ATP-binding cassette transporters in bacteria. Annu Rev Biochem 73: 241-268.
31. Davila-Martinez Y, Ramos-Vega AL, Contreras-Martinez S, Encarnacion S, Geiger O & Lopez-Lara IM (2010) SMc01553 is the sixth acyl carrier protein in Sinorhizobium meliloti 1021. Microbiology 156: 230-239.
32. De Castro C, Molinaro A, Lanzetta R, Silipo A & Parrilli M (2008) Lipopolysaccharide structures from Agrobacterium and Rhizobiaceae species. Carbohydr Res 343: 1924-1933.
33. D'Haeze W, Leoff C, Freshour G, Noel KD & Carlson RW (2007) Rhizobium etli CE3 bacteroid lipopolysaccharides are structurally similar but not identical to those produced by cultured CE3 bacteria. J Biol Chem 282: 17101-17113.
34. Dixon R & Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2: 621-631.
35. Domenech P & Reed MB (2009) Rapid and spontaneous loss of phthiocerol dimycocerosate (PDIM) from Mycobacterium tuberculosis grown in vitro: implications for virulence studies. Microbiology 155: 3532-3543.
36. Domenech P, Kobayashi H, Levier K, Walker GC & Barry CE III (2009) BacA, an ABC transporter involved in maintenance of chronic murine infections with Mycobacterium tuberculosis. J Bacteriol 191: 477-485.
37. 2+] is indispensable for the transduction of the nod factor signal in alfalfa. Plant Physiol 121: 273-279.
38. Ferguson GP, Roop RM II & Walker GC (2002) Deficiency of a Sinorhizobium meliloti bacA mutant in alfalfa symbiosis correlates with alteration of the cell envelope. J Bacteriol 184: 5625-5632.
39. Ferguson GP, Datta A, Baumgartner J, Roop RM II, Carlson RW & Walker GC (2004) Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. P Natl Acad Sci USA 101: 5012-5017.
40. Ferguson GP, Datta A, Carlson RW & Walker GC (2005) Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis. Mol Microbiol 56: 68-80.
41. Ferguson GP, Jansen A, Marlow VL & Walker GC (2006) BacA-mediated bleomycin sensitivity in Sinorhizobium meliloti is independent of the unusual lipid A modification. J Bacteriol 188: 3143-3148.
42. 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.
43. Frühling M, Albus U, Hohnjec N, Geise G, Pühler A & Perlick AM (2000) A small gene family of broad bean codes for late nodulins containing conserved cysteine clusters. Plant Sci 152: 67-77.
44. Fugier E, Pappas G & Gorvel JP (2007) Virulence factors in brucellosis: implications for aetiopathogenesis and treatment. Expert Rev Mol Med 9: 1-10.
45. Gage DJ (2002) Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J Bacteriol 184: 7042-7046.
46. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68: 280-300.
47. Gage DJ, Bobo T & Long SR (1996) Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J Bacteriol 178: 7159-7166.
48. Geiger O & López-Lara IM (2002) Rhizobial acyl carrier proteins and their roles in the formation of bacterial cell-surface components that are required for the development of nitrogen-fixing root nodules on legume hosts. FEMS Microbiol Lett 208: 153-162.
49. Gibson KE, Kobayashi H & Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42: 413-441.
50. Glazebrook J, Ichige A & Walker GC (1993) A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev 7: 1485-1497.
51. Gong ZY, He ZS, Zhu JB, Yu GQ & Zou HS (2006) Sinorhizobium meliloti nifA mutant induces different gene expression profile from wild type in Alfalfa nodules. Cell Res 16: 818-829.
52. Graham MA, Silverstein KA, Cannon SB & VandenBosch KA (2004) Computational identification and characterization of novel genes from legumes. Plant Physiol 135: 1179-1197.
53. Guillemin J (2006) Scientists and the history of biological weapons: a brief historical overview of the development of biological weapons in the twentieth century. EMBO Rep 7: S45-S49.
54. Haag AF, Wehmeier S, Beck S, Marlow VL, Fletcher V, James EK & Ferguson GP (2009) The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa. J Bacteriol 191: 4681-4686.
55. Haag AF, Myka KK, Arnold MF, Caro-Hernandez P & Ferguson GP (2010) Importance of lipopolysaccharide and cyclic β-1, 2-glucans in Brucella-mammalian infections. Int J Microbiol 2010: 124509.
56. Haag AF, Wehmeier S, Muszynski A et al. (2011a) Biochemical characterization of Sinorhizobium meliloti mutants reveals gene products involved in the biosynthesis of the unusual lipid A very long-chain fatty acid. J Biol Chem 286: 17455-17466.
57. Haag AF, Baloban M, Sani M et al. (2011b) Protection of Sinorhizobium against host cysteine-rich antimicrobial peptides is critical for symbiosis. PLoS Biol 9: e1001169.
58. Haag AF, Kerscher B, Dall'angelo S et al. (2012) Role of cysteine residues and disulfide bonds on the activity of a legume root nodule-specific, cysteine-rich peptide. J Biol Chem, 287: 10791-10798.
59. Halverson LJ & Stacey G (1986) Signal exchange in plant-microbe interactions. Microbiol Rev 50: 193-225.
60. Harries AD & Dye C (2006) Tuberculosis. Ann Trop Med Parasitol 100: 415-431.
61. Ichige A & Walker GC (1997) Genetic analysis of the Rhizobium meliloti bacA gene: functional interchangeability with the Escherichia coli sbmA gene and phenotypes of mutants. J Bacteriol 179: 209-216.
62. Izadpanah A & Gallo RL (2005) Antimicrobial peptides. J Am Acad Dermatol 52: 381-390; quiz 391-382.
63. Jensen E, Peoples M, Boddey R, Gresshoff P, Hauggaard-Nielsen H, Alves B & Morrison M (2012) Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries. A review. Agron Sustain Dev 32: 329-364.
64. Jimenez-Zurdo JI, Frugier F, Crespi MD & Kondorosi A (2000) Expression profiles of 22 novel molecular markers for organogenetic pathways acting in alfalfa nodule development. Mol Plant Microbe Interact 13: 96-106.
65. Jones KM, Kobayashi H, Davies BW, Taga ME & Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5: 619-633.
66. Kaijalainen S, Schroda M & Lindstrom K (2002) Cloning of nodule-specific cDNAs of Galega orientalis. Physiol Plant 114: 588-593.
67. Karakousis PC, Bishai WR & Dorman SE (2004) Mycobacterium tuberculosis cell envelope lipids and the host immune response. Cell Microbiol 6: 105-116.
68. Karunakaran R, Ramachandran VK, Seaman JC et al. (2009) Transcriptomic analysis of Rhizobium leguminosarum biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol 191: 4002-4014.
69. Karunakaran R, Haag AF, East AK et al. (2010) BacA is essential for bacteroid development in nodules of galegoid, but not phaseoloid, legumes. J Bacteriol 192: 2920-2928.
70. Kato T, Kawashima K, Miwa M, Mimura Y, Tamaoki M, Kouchi H & Suganuma N (2002) Expression of genes encoding late nodulins characterized by a putative signal peptide and conserved cysteine residues is reduced in ineffective pea nodules. Mol Plant Microbe Interact 15: 129-137.
71. Kobayashi H, Sunako M, Hayashi M & Murooka Y (2001) DNA synthesis and fragmentation in bacteroids during Astragalus sinicus root nodule development. Biosci Biotechnol Biochem 65: 510-515.
72. Kuppusamy KT, Endre G, Prabhu R et al. (2004) LIN, a Medicago truncatula gene required for nodule differentiation and persistence of rhizobial infections. Plant Physiol 136: 3682-3691.
73. Lavina M, Pugsley AP & Moreno F (1986) Identification, mapping, cloning and characterization of a gene (sbmA) required for microcin B17 action on Escherichia coli K12. J Gen Microbiol 132: 1685-1693.
74. LeVier K & Walker GC (2001) Genetic analysis of the Sinorhizobium meliloti BacA protein: differential effects of mutations on phenotypes. J Bacteriol 183: 6444-6453.
75. LeVier K, Phillips RW, Grippe VK, Roop RM II & Walker GC (2000) Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287: 2492-2493.
76. 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.
77. Lodwig EM, Hosie AH, Bourdes A et al. (2003) Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature 422: 722-726.
78. Login FH, Balmand S, Vallier A et al. (2011) Antimicrobial peptides keep insect endosymbionts under control. Science 334: 362-365.
79. Long S, McCune S & Walker GC (1988) Symbiotic loci of Rhizobium meliloti identified by random TnphoA mutagenesis. J Bacteriol 170: 4257-4265.
80. Maria-Pilar JDB, Dudal S, Dornand J & Gross A (2005) Cellular bioterrorism: how Brucella corrupts macrophage physiology to promote invasion and proliferation. Clin Immunol 114: 227-238.
81. Marlow VL, Haag AF, Kobayashi H, Fletcher V, Scocchi M, Walker GC & Ferguson GP (2009) Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J Bacteriol 191: 1519-1527.
82. Maróti G, Kereszt A, Kondorosi E & Mergaert P (2011) Natural roles of antimicrobial peptides in microbes, plants and animals. Res Microbiol 162: 363-374.
83. Marshall E, Costa LM & Gutierrez-Marcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J Exp Bot 62: 1677-1686.
84. Maruya J & Saeki K (2010) The bacA gene homolog, mlr7400, in Mesorhizobium loti MAFF303099 is dispensable for symbiosis with Lotus japonicus but partially capable of supporting the symbiotic function of bacA in Sinorhizobium meliloti. Plant Cell Physiol 51: 1443-1452.
85. Mateos PF, Baker DL, Petersen M et al. (2001) Erosion of root epidermal cell walls by Rhizobium polysaccharide-degrading enzymes as related to primary host infection in the Rhizobium-legume symbiosis. Can J Microbiol 47: 475-487.
86. Mattiuzzo M, Bandiera A, Gennaro R, Benincasa M, Pacor S, Antcheva N & Scocchi M (2007) Role of the Escherichia coli SbmA in the antimicrobial activity of proline-rich peptides. Mol Microbiol 66: 151-163.
87. Maunoury N, Redondo-Nieto M, Bourcy M et al. (2010) Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches. PLoS ONE 5: e9519.
88. 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.
89. Mergaert P, Uchiumi T, Alunni B et al. (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. P Natl Acad Sci USA 103: 5230-5235.
90. Miller KJ, Kennedy EP & Reinhold VN (1986) Osmotic adaptation by gram-negative bacteria: possible role for periplasmic oligosaccharides. Science 231: 48-51.
91. O'Brian MR (1996) Heme synthesis in the Rhizobium-legume symbiosis: a palette for bacterial and eukaryotic pigments. J Bacteriol 178: 2471-2478.
92. Oldroyd GE & Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59: 519-546.
93. Oono R & Denison RF (2010) Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids. Plant Physiol 154: 1541-1548.
94. Oono R, Schmitt I, Sprent JI & Denison RF (2010) Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation. New Phytol 187: 508-520.
95. Ott T, van Dongen JT, Gunther C et al. (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15: 531-535.
96. Paau AS, Oro J & Cowles JR (1979) DNA content of free living rhizobia and bacteroids of various Rhizobium-legume associations. Plant Physiol 63: 402-405.
97. Pappas G, Papadimitriou P, Akritidis N, Christou L & Tsianos EV (2006) The new global map of human brucellosis. Lancet Infect Dis 6: 91-99.
98. Perret X, Staehelin C & Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201.
99. Pessi G, Ahrens CH, Rehrauer H, Lindemann A, Hauser F, Fischer HM & Hennecke H (2007) Genome-wide transcript analysis of Bradyrhizobium japonicum bacteroids in soybean root nodules. Mol Plant Microbe Interact 20: 1353-1363.
100. Podda E, Benincasa M, Pacor S, Micali F, Mattiuzzo M, Gennaro R & Scocchi M (2006) Dual mode of action of Bac7, a proline-rich antibacterial peptide. Biochim Biophys Acta 1760: 1732-1740.
101. Poole PS, Schofield NA, Reid CJ, Drew EM & Walshaw DL (1994) Identification of chromosomal genes located downstream of dctD that affect the requirement for calcium and the lipopolysaccharide layer of Rhizobium leguminosarum. Microbiology 140: 2797-2809.
102. Prell J, White JP, Bourdes A, Bunnewell S, Bongaerts RJ & Poole PS (2009) Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. P Natl Acad Sci USA 106: 12477-12482.
103. Que NL, Ribeiro AA & Raetz CR (2000a) Two-dimensional NMR spectroscopy and structures of six lipid A species from Rhizobium etli CE3. Detection of an acyloxyacyl residue in each component and origin of the aminogluconate moiety. J Biol Chem 275: 28017-28027.
104. Que NL, Lin S, Cotter RJ & Raetz CR (2000b) Purification and mass spectrometry of six lipid A species from the bacterial endosymbiont Rhizobium etli. Demonstration of a conserved distal unit and a variable proximal portion. J Biol Chem 275: 28006-28016.
105. Raetz CRH & Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635-700.
106. Raetz CR, Reynolds CM, Trent MS & Bishop RE (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76: 295-329.
107. Ramos-Vega AL, Davila-Martinez Y, Sohlenkamp C, Contreras-Martinez S, Encarnacion S, Geiger O & Lopez-Lara IM (2009) SMb20651 is another acyl carrier protein from Sinorhizobium meliloti. Microbiology 155: 257-267.
108. Rivas-Santiago B, Schwander SK, Sarabia C et al. (2005) Human b-defensin 2 is expressed and associated with Mycobacterium tuberculosis during infection of human alveolar epithelial cells. Infect Immun 73: 4505-4511.
109. Rivas-Santiago B, Sada E, Tsutsumi V, Aguilar-Leon D, Contreras JL & Hernandez-Pando R (2006) beta-Defensin gene expression during the course of experimental tuberculosis infection. J Infect Dis 194: 697-701.
110. Robertson JG & Lyttleton P (1984) Division of peribacteroid membranes in root nodules of white clover. J Cell Sci 69: 147-157.
111. Robledo M, Jimenez-Zurdo JI, Velazquez E et al. (2008) Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. P Natl Acad Sci USA 105: 7064-7069.
112. Robledo M, Jimenez-Zurdo JI, Soto MJ, Velazquez E, Dazzo F, Martinez-Molina E & Mateos PF (2011) Development of functional symbiotic white clover root hairs and nodules requires tightly regulated production of rhizobial cellulase CelC2. Mol Plant Microbe Interact 24: 798-807.
113. Roop RM II, Robertson GT, Ferguson GP, Milford LE, Winkler ME & Walker GC (2002) Seeking a niche: putative contributions of the hfq and bacA gene products to the successful adaptation of the brucellae to their intracellular home. Vet Microbiol 90: 349-363.
114. Roop RM II, Gaines JM, Anderson ES, Caswell CC & Martin DW (2009) Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host. Med Microbiol Immunol 198: 221-238.
115. Salomon RA & Farias RN (1995) The peptide antibiotic microcin 25 is imported through the tonB pathway and the SbmA protein. J Bacteriol 177: 3323-3325.
116. Scheres B, van Engelen F, van der Knaap E, van de Wiel C, van Kammen A & Bisseling T (1990) Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 2: 687-700.
117. Schroeder BO, Wu Z, Nuding S et al. (2011) Reduction of disulphide bonds unmasks potent antimicrobial activity of human beta-defensin 1. Nature 469: 419-423.
118. Scocchi M, Romeo D & Zanetti M (1994) Molecular cloning of Bac7, a proline- and arginine-rich antimicrobial peptide from bovine neutrophils. FEBS Lett 352: 197-200.
119. Scocchi M, Mattiuzzo M, Benincasa M, Antcheva N, Tossi A & Gennaro R (2008) Investigating the mode of action of proline-rich antimicrobial peptides using a genetic approach: a tool to identify new bacterial targets amenable to the design of novel antibiotics. Methods Mol Biol 494: 161-176.
120. Sen D & Weaver R (1981) A comparison of nitrogen-fixing ability of peanut, cowpea and siratro plants nodulated by different strains of Rhizobium. Plant Soil 60: 317-319.
121. Sen D & Weaver RW (1984) A basis for different rates of N2-fixation by the same strains of Rhizobium in peanut and cowpea root nodules. Plant Science Letters 34: 239-246.
122. Sharypova LA, Niehaus K, Scheidle H, Holst O & Becker A (2003) Sinorhizobium meliloti acpXL mutant lacks the C28 hydroxylated fatty acid moiety of lipid A and does not express a slow migrating form of lipopolysaccharide. J Biol Chem 278: 12946-12954.
123. Sieberer B & Emons AMC (2000) Cytoarchitecture and pattern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors. Protoplasma 214: 118-127.
124. Sieberer BJ, Timmers ACJ, Lhuissier FGP & Emons AMC (2002) Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs. Plant Physiol 130: 977-988.
125. Soupene E, Foussard M, Boistard P, Truchet G & Batut J (1995) Oxygen as a key developmental regulator of Rhizobium meliloti N2-fixation gene expression within the alfalfa root nodule. P Natl Acad Sci USA 92: 3759-3763.
126. Tan BH, Meinken C, Bastian M et al. (2006) Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens. J Immunol 177: 1864-1871.
127. Tan XJ, Cheng Y, Li YX, Li YG & Zhou JC (2009) BacA is indispensable for successful Mesorhizobium-Astragalus symbiosis. Appl Microbiol Biotechnol 84: 519-526.
128. Tjepkema JD & Cartica RJ (1982) Diffusion limitation of oxygen uptake and nitrogenase activity in the root nodules of Parasponia rigida Merr. and Perry. Plant Physiol 69: 728-733.
129. Udvardi MK & Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Physiol Plant Mol Biol 48: 493-523.
130. Vallecillo AJ & Espitia C (2009) Expression of Mycobacterium tuberculosis pe_pgrs33 is repressed during stationary phase and stress conditions, and its transcription is mediated by sigma factor A. Microb Pathog 46: 119-127.
131. Van De Velde W, Zehirov G, Szatmari A et al. (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327: 1122-1126.
132. Vanderlinde EM, Muszynski A, Harrison JJ et al. (2009) Rhizobium leguminosarum biovar viciae 3841, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired in desiccation tolerance, biofilm formation and motility. Microbiology 155: 3055-3069.
133. Vasse J, de Billy F, Camut S & Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172: 4295-4306.
134. Vedam V, Kannenberg EL, Haynes JG, Sherrier DJ, Datta A & Carlson RW (2003) A Rhizobium leguminosarum AcpXL mutant produces lipopolysaccharide lacking 27-hydroxyoctacosanoic acid. J Bacteriol 185: 1841-1850.
135. Vedam V, Haynes JG, Kannenberg EL, Carlson RW & Sherrier DJ (2004) A Rhizobium leguminosarum lipopolysaccharide lipid-A mutant induces nitrogen-fixing nodules with delayed and defective bacteroid formation. Mol Plant Microbe Interact 17: 283-291.
136. Vedam V, Kannenberg E, Datta A, Brown D, Haynes-Gann JG, Sherrier DJ & Carlson RW (2006) The pea nodule environment restores the ability of a Rhizobium leguminosarum lipopolysaccharide acpXL mutant to add 27-hydroxyoctacosanoic acid to its lipid A. J Bacteriol 188: 2126-2133.
137. Wang D, Griffitts J, Starker C et al. (2010) A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327: 1126-1129.
138. Wehmeier S, Arnold MF, Marlow VL et al. (2010) Internalization of a thiazole-modified peptide in Sinorhizobium meliloti occurs by BacA-dependent and -independent mechanisms. Microbiology 156: 2702-2713.
139. Wei H & Layzell DB (2006) Adenylate-coupled ion movement. A mechanism for the control of nodule permeability to O2 diffusion. Plant Physiol 141: 280-287.
140. White J, Prell J, James EK & Poole P (2007) Nutrient sharing between symbionts. Plant Physiol 144: 604-614.
141. Whitehead LF & Day DA (1997) The peribacteroid membrane. Physiol Plant 100: 30-44.
142. Xie F, Murray JD, Kim J, Heckmann AB, Edwards A, Oldroyd GE & Downie JA (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci USA 109: 633-638.
143. Yorgey P, Lee J, Kordel J, Vivas E, Warner P, Jebaratnam D & Kolter R (1994) Posttranslational modifications in microcin B17 define an additional class of DNA gyrase inhibitor. P Natl Acad Sci USA 91: 4519-4523.
144. Young EJ (1995) An overview of human brucellosis. Clin Infect Dis 21: 283-289.
145. Young ND, Debelle F, Oldroyd GE et al. (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: 520-524.
146. Yurgel SN & Kahn ML (2008) A mutant GlnD nitrogen sensor protein leads to a nitrogen-fixing but ineffective Sinorhizobium meliloti symbiosis with alfalfa. P Natl Acad Sci USA 105: 18958-18963.