Bacterial lipopolysaccharides (LPSs) have multiple roles in plant—microbe interactions. LPS contributes to the low permeability of the outer membrane, which acts as a barrier to protect bacteria from plant-derived antimicrobial substances. Conversely, perception of LPS by plant cells can lead to the triggering of defence responses or to the priming of the plant to respond more rapidly and/or to a greater degree to subsequent pathogen challenge. LPS from symbiotic bacteria can have quite different effects on plants to those of pathogens. Some details are emerging of the structures within LPS that are responsible for induction of these different plant responses. The lipid A moiety is not solely responsible for all of the effects of LPS in plants; core oligosaccharide and O-antigen components can elicit specific responses. Here, we review the effects of LPS in induction of defence-related responses in plants, the structures within LPS responsible for eliciting these effects and discuss the possible nature of the (as yet unidentified) LPS receptors in plants.
Kao CC, Sequeira L.A gene cluster required for coordinated biosynthesis of lipopolysaccharide and extracellular polysaccharide also affects virulence of Pseudomonas solanacearum . J Bacteriol1991; 173: 7841—7847.
2.
Kingsley MT, Gabriel DW, Marlow GC, Roberts PDThe opsX locus of Xanthomonas campestris affects host range and biosynthesis of lipopolysaccharide and extracellular polysaccharide. J Bacteriol1993; 175: 5839—5850.
3.
Dow JM, Osbourn AE, Wilson TJ, Daniels MJA locus determining pathogenicity of Xanthomonas campestris is involved in lipopolysaccharide biosynthesis. Mol Plant Microbe Interact1995; 8: 768—777.
4.
Titarenko E. , Lopez-Solanilla E., Garcia-Olmedo F., Rodriguez-Palenzuela P.Mutants of Ralstonia (Pseudomonas) solanacearum sensitive to antimicrobial peptides are altered in their lipopolysaccharide structure and are avirulent in tobacco. J Bacteriol1997; 179: 6699—6704.
5.
Toth IK, Thorpe CJ, Bentley SD et al. Mutation in a gene required for lipopolysaccharide and enterobacterial common antigen biosynthesis affects virulence in the plant pathogen Erwinia carotovora subsp. atroseptica. Mol Plant Microbe Interact1999; 12: 499—507.
6.
Dow M., Newman MA, von Roepenack E.The induction and modulation of plant defence responses by bacterial lipopolysaccharides . Annu Rev Phytopathol 2000; 38: 241—261.
7.
Boher B., Nicole M., Potin M., Geiger JPExtracellular polysaccharides from Xanthomonas axonopodis pv. manihotis interact with cassava cell walls during pathogenesis. Mol Plant Microbe Interact1997; 10: 803—811.
8.
Dekkers LC, van der Bij AJ, Mulders IH et al. Role of the O-antigen of lipopolysaccharide, and possible roles of growth rate and of NADH:ubiquinone oxidoreductase (nuo) in competitive tomato root-tip colonization by Pseudomonas fluorescens WCS365. Mol Plant Microbe Interact1998; 11: 763—771.
9.
Lugtenberg BJ , Dekkers L., Bloemberg GVMolecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol2001; 39: 461—490.
10.
Nürnberger T., Brunner F.Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr OpinPlant Biol2002 ; 5: 318—324.
11.
Erbs G., Newman MAThe role of lipopolysaccharides in induction of plant defence responses. Mol Plant Pathol2003; 4: 421—425.
12.
Nürnberger T., Brunner F., Kemmerling B., Piater L.Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev2004; 198: 249—266.
13.
Shah J. Lipids , lipases, and lipid-modifying enzymes in plant disease resistance. Annu Rev Phytopathol 2005; 43: 229—260.
14.
Lamb CJPlant disease resistance genes in signal perception and transduction. Cell1994; 76: 419—422.
Lamb C., Dixon RAThe oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol1997; 48: 251—275.
17.
Greenberg JTProgrammed cell death in plant-pathogen interactions . Annu Rev Plant Physiol Plant Mol Biol1997 ; 48: 525—545.
18.
Gomez-Gomez L., Boller T.FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell2000; 5: 1003—1011.
Nürnberger T., Kemmerling B.Receptor protein kinases — pattern recognition receptors in plant immunity. Trends PlantSci2006; 11: 519—522.
21.
Ausubel F.Are innate immune signalling pathways in plants and animals conserved?Nat Immunol2005; 6: 973—979.
22.
Zipfel C., Kunze G., Chinchilla D. et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell2006; 125: 749—760.
23.
Davis KR, Lyon GD, Darvill AG, Albersheim P.Host—pathogen interactions: XXV. Endopolygalacturonic acid lyase from Erwinia carotovora elicits phytoalexin accumulation by releasing plant cell wall fragments. Plant Physiol1984; 74: 52—60.
24.
Abramovitch RB, Anderson JC, Martin GBBacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol2006 ; 7: 601—611.
Pieterse CM, VanLoon LC. NPR1: the spider in the web of induced resistance signaling pathways. Curr OpinPlant Biol2004; 7: 456—464.
27.
Raetz CR, Whitfield C.Lipopolysaccharide endotoxins. Annu Rev Biochem2002; 71: 635—700.
28.
Zähringer U. , Lindner B., Rietschel ETMolecular structure of lipid A, the endotoxic center of bacterial lipopolysaccharides. Adv Carbohydr Chem Biochem1994; 50: 211—276.
29.
Zähringer U., Lindner B., Rietschel ETChemical structure of lipid A: recent advances in structural analysis of biologically active molecules. In: Brade H, Morrison DC, Opal S, Vogel S. (eds) Endotoxin in Health and DiseaseNew York: Marcel Dekker, 1999; 93—114.
30.
Holst O.Chemical structure of the core region of lipopolysaccharides. In: Brade H, Morrison DC, Opal S, Vogel S. (eds) Endotoxin in Health and Disease. New York : Marcel Dekker, 1999; 115—154.
31.
Holst O.Chemical structure of the core region of lipopolysaccharides — an update . Trends Glycosci Glycotechnol2002; 14: 87—103.
32.
Duus JO, Gotfredsen CH, Bock K.Carbohydrate structural determination by NMR spectroscopy: modern methods and limitations. Chem Rev2000; 100: 4589—4614.
Corsaro MM, De Castro C, Molinaro A., Parrilli M.Structure of lipopolysaccharides from phytopathogenic bacteria. Recent Res DevelopPhytochem2001; 5: 119—138.
35.
Silipo A., Molinaro A., Sturiale L. et al. The elicitation of plant innate immunity by lipooligosaccharide of Xanthomonas campestris. J Biol Chem2005 ; 280: 33660—33668.
36.
Zdorovenko EL, Vinogradov E., Zdorovenko GM et al. Structure of the core oligosaccharide of a rough-type lipopolysaccharide of Pseudomonas syringae pv. phaseolicola . Eur J Biochem2004; 271: 4968—4977.
37.
Mahenthiralingam E., Urban TA, Goldberg JBThe multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol2005; 3: 144—156.
38.
Silipo A., De Castro C., Lanzetta R., Molinaro A., Parrilli M.Complete structural characterization of the lipid A fraction of a clinical strain of B. cepacia genomovar I lipopolysaccharide. Glycobiology2005; 15: 561—570.
39.
Kannenberg EL, Carlson RWLipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol Microbiol2001; 39: 379—391.
40.
Fischer SE, Miguel MJ, Mori GBEffect of root exudates on the exopolysaccharide composition and the lipopolysaccharide profile of Azospirillum brasilense Cd under saline stress. FEMS Microbiol Lett2003; 219: 53—62.
41.
Bishop REThe lipid A palmitoyltransferase PagP: molecular mechanisms and role in bacterial pathogenesis. Mol Microbiol2005; 57: 900—912.
42.
Bishop RE, Kim SH, El Zoeiby A.Role of lipid A palmitoylation in bacterial pathogenesis. J Endotoxin Res2005; 11: 174—180.
43.
Gudlavalleti SK, Forsberg LSStructural characterization of the lipid A component of Sinorhizobium sp. NGR234 rough and smooth form lipopolysaccharide. Demonstration that the distal amide-linked acyloxyacyl residue containing the long chain fatty acid is conserved in Rhizobium and Sinorhizobium spp . J Biol Chem2003; 278: 3957—3968.
44.
Bhat UR, Forsberg LS, Carlson RWStructure of lipid A component of Rhizobium leguminosarum bv. phaseoli lipopolysaccharide. Unique nonphosphorylated lipid A containing 2-amino-2-deoxygluconate, galacturonate, and glucosamine. J Biol Chem1994; 269: 14402—14410.
45.
Silipo A., De Castro C., Lanzetta R., Molinaro A., Parrilli M.Full structural characterization of the lipid A components from the Agrobacterium tumefaciens strain C58 lipopolysaccharide fraction. Glycobiology2004; 14: 805—815.
46.
De Castro C. , Carannante A., Lanzetta R., Liparoti V., Molinaro A., Parrilli M.Core oligosaccharide structure from the highly phytopathogenic Agrobacterium tumefaciens TT111 and conformational analysis of the putative rhamnan epitope, Glycobiology2006; 16: 1272—1280.
47.
Zeidler D., Zähringer U., Gerber I. et al. Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defence genes. Proc Natl Acad Sci USA2004; 101: 15811—15816.
48.
Guo FQ, Okamoto M., Crawford NMIdentification of a plant nitric oxide synthase gene involved in hormonal signaling. Science2003; 302: 100—103.
49.
Zemojtel T. , Fröhlich A., Palmieri MC et al. Plant nitric oxide synthase: a never-ending story? Trends Plant Sci2006; 11: 524—525.
50.
Crawford NM , Galli M., Tischner R., Heimer YM, Okamoto M., Mack M.Response to Zemojtel et al.: Plant nitric oxide synthase: back to square one. Trends Plant Sci2006; 11: 526—527.
51.
Guo FQResponse to Zemojtel et al.: Plant nitric oxide synthase: AtNOS1 is just the beginning. Trends Plant Sci2006; 11: 527-528.
52.
Coventry HS , Dubery IALipopolysaccharides from Burkholderia cepacia contribute to an enhanced defensive capacity and the induction of pathogenesis-related proteins in Nicotiana tabacum. Physiol Mol Plant Pathol2001; 58: 149—158.
53.
Albus U., Baier R., Holst O., Pühler A., Niehaus K.Suppression of an elicitor-induced oxidative burst reaction in Medicago sativa cell cultures by Sinorhizobium meliloti lipopolysaccharides. New Phytol2001; 151: 597—606.
54.
Meyer A., Pühler A., Niehaus K.The lipopolysaccharides of the phytopathogen Xanthomonas campestris pv. campestris induce an oxidative burst reaction in cell cultures of Nicotiana tabacum. Planta2001; 213: 214—222.
55.
Sanabria NM , Dubery IADifferential display profiling of the Nicotiana response to LPS reveals elements of plant basal resistance. Biochem Biophys Res Commun2006; 344: 1001—1007.
56.
Braun SG, Meyer A., Holst O., Pühler A., Niehaus K.Characterization of the Xanthomonas campestris pv. campestris lipopolysaccharide substructures essential for elicitation of an oxidative burst in tobacco cells . Mol Plant Microbe Interact2005; 18: 674—681.
57.
Küpper FC, Gaquerel E., Boneberg EM, Morath S., Salaun JP, Potin P.Early events in the perception of lipopolysaccharides in the brown alga Laminaria digitata include an oxidative burst and activation of fatty acid oxidation cascades. J Exp Bot2006; 57: 1991—1999.
58.
Desaki Y., Miya A., Venkatesh B., Tsuyumu S., Yamane H., Kaku H., Minami E., Shibuya N.Bacterial lipopolysaccharides induce defence responses associated with programmed cell death in rice cells. Plant Cell Physiol2006; 47: 1530—1540.
59.
Desender S. , Klarzynski O., Potin P., Barzic MR, Andrivon D., Val F.Lipopolysaccharides of Pectobacterium atrosepticum and Pseudomonas corrugata induce different defence response patterns in tobacco, tomato, and potato. Plant Biol (Stuttg)2006; 8: 636—645.
60.
Keshavarzi M., Soylu S., Brown I. et al. Basal defences induced in pepper by lipopolysaccharides are suppressed by Xanthomonas campestris pv. vesicatoria . Mol Plant Microbe Interact2004; 17: 805—815.
Newman MA, von Roepenack-Lahaye E., Parr A., Daniels MJ, Dow JMPrior exposure to lipopolysaccharide potentiates expression of plant defences in response to bacteria. Plant J2002; 29: 487—495.
63.
Conrath U., Beckers GJ, Flors V. et al. Priming: getting ready for battle. Mol Plant Microbe Interact2006; 19: 1062—1071.
64.
Newman MA, von Roepenack-Lahaye E., Parr A., Daniels MJ, Dow JMInduction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris, a plant defence response activated by hrp gene-dependent and hrp gene-independent mechanisms. Mol Plant Microbe Interact2001; 14: 785—792.
65.
Newman MA, Daniels MJ, Dow JMThe activity of lipid A and core components of bacterial lipopolysaccharides in the prevention of the hypersensitive response in pepper. Mol Plant Microbe Interact1997; 10: 926—928.
66.
Kim MG, da Cunha L., McFall AJ et al. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defence in Arabidopsis. Cell2005; 121: 749—759.
67.
van Loon LC, Bakker PA, Pieterse CMSystemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol1998; 36: 453—483.
68.
Leeman M., Vanpelt JA, Denouden FM, Heinsbroek M., Bakker Pahm, Schippers B.Induction of systemic resistance against Fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology1995; 85: 1021—1027.
69.
Van Wees SC , Pieterse CM, Trijssenaar A., Van't Westende YA, Hartog F., Van Loon LCDifferential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol Plant Microbe Interact1997; 10: 716—724.
70.
Reitz M., Rudolph K., Schroder I., Hoffmann-Hergarten S., Hallmann J., Sikora RALipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl Environ Microbiol2000; 66: 3515—3518.
71.
Gerber IB, Laukens K., Witters E., Dubery IALipopolysaccharide-responsive phosphoproteins in Nicotiana tabacum cells. Plant Physiol Biochem2006; 44: 369—379.
72.
Piater LA, Nürnberger T., Dubery IAIdentification of a lipopolysaccharide responsive erk-like MAP kinase in tobacco leaf tissue. Mol Plant Pathol2004; 5: 331—338.
73.
Gerber IB, Dubery IAProtein phosphorylation in Nicotiana tabacum cells in response to perception of lipopolysaccharides from Burkholderia cepacia. Phytochemistry2004; 65: 2957—2966.
74.
Gross A., Kapp D., Nielsen T., Niehaus K.Endocytosis of Xanthomonas campestris pathovar campestris lipopolysaccharides in non-host plant cells of Nicotiana tabacum. New Phytol2005; 165: 215—226.
75.
Robatzek S. , Chinchilla D., Boller T.Ligand induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev2006; 20: 537—542.
Husebye H., Halaas O., Stenmark H. et al. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J2006; 25: 683—692.
78.
Latz E., Visintin A., Lien E. et al. Lipopolysaccharide rapidly trafficks to and from the Golgi apparatus with the Toll-like receptor 4—MD-2—CD14 complex in a process that is distinct from the initiation of signal transduction. J Biol Chem2002; 277: 47834—47843.
79.
Soto MJ, Sanjuan J., Olivares J.Rhizobia and plant-pathogenic bacteria: common infection weapons. Microbiology2006; 152: 3167—3174.
80.
Dazzo FB, Truchet GL, Hollingsworth RI et al. Rhizobium lipopolysaccharide modulates infection thread development in white clover root hairs. J Bacteriol1991 ; 173: 5371—5384.
81.
Mathis R., Van Gijsegem F, De Rycke R et al. Lipopolysaccharides as a communication signal for progression of legume endosymbiosis. Proc Natl Acad Sci USA2005; 102: 2655—2660.
82.
Scheidle H. , Gross A., Niehaus K.The lipid A substructure of the Sinorhizobium meliloti lipopolysaccharides is sufficient to suppress the oxidative burst in host plants. New Phytol2005; 165: 559—565.
83.
Price NP, Jeyaretnam B., Carlson RW, Kadrmas JL, Raetz CR, Brozek KALipid A biosynthesis in Rhizobium leguminosarum: role of a 2-keto-3-deoxyoctulosonate-activated 4′ phosphatase. Proc Natl Acad Sci USA1995; 92: 7352—7356.
84.
Brozek KA, Kadrmas JL, Raetz CRLipopolysaccharide biosynthesis in Rhizobium leguminosarum. Novel enzymes that process precursors containing 3-deoxy-D-manno-octulosonic acid. J Biol Chem1996; 271: 32112—32118.
85.
Karbarz MJ, Kalb SR, Cotter RJ, Raetz CRExpression cloning and biochemical characterization of a Rhizobium leguminosarum lipid A 1-phosphatase. J Biol Chem2003; 278: 39269—39279.
86.
Holst O., Süsskind M., Grimmecke D., Brade L., Brade H.Core structures of enterobacterial lipopolysaccharides. Prog Clin Biol Res1998; 397: 23—35.
87.
Lerouge I., Vanderleyden J.O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol Rev2002; 26: 17—47.
88.
Bedini E., De Castro C, Erbs G. et al. Structure-dependent modulation of a pathogen response in plants by synthetic O-antigen polysaccharides. J Am Chem Soc2005; 127: 2414—2416.
89.
Bedini E., Carabellese A., Barone G., Parrilli M.First synthesis of the β-D-rhamnosylated trisaccharide repeating unit of the O-antigen from Xanthomonas campestris pv. campestris 8004. J Org Chem2005; 70: 8064—8070.
90.
Schromm AB, Brandenburg K., Loppnow H. et al. The charge of endotoxin molecules influences their conformation and IL-6-inducing capacity. J Immunol1998 ; 161: 5464—5471.
91.
Schromm AB, Brandenburg K., Loppnow H. et al. Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur J Biochem2000; 267: 2008—2013.
Inohara N., Nunez G.NODs: intracellular proteins involved in inflammation and apoptosis. Nat Rev Immunol2003; 3: 371—382.
94.
Miyake K.Roles for accessory molecules in microbial recognition by Toll-like receptors . J Endotoxin Res2006; 12: 195—204.
95.
Hayashi F., Smith KD, Ozinsky A. et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature2001; 410: 1099—1103.
96.
Song WY, Wang GL, Chen LL et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science1995; 270: 1804—1806.
97.
Dangl JL, Jones JDPlant pathogens and integrated defence responses to infection. Nature2001; 411: 826—833.
98.
Jones JD, Dangl JLThe plant immune system. Nature2006; 444: 323—329.
99.
Jebanathirajah JA, Peri S., Pandey A.Toll and interleukin-1 receptor (TIR) domain-containing proteins in plants: a genomic perspective. Trends Plant Sci2002; 7: 388—391.
100.
Baveye S., Elass E., Mazurier J., Legrand D.Lactoferrin inhibits the binding of lipopolysaccharides to L-selectin and subsequent production of reactive oxygen species by neutrophils. FEBS Lett2000; 469: 5—8.
101.
Triantafilou M., Triantafilou K.The dynamics of LPS recognition: complex orchestration of multiple receptors. J Endotoxin Res2005 ; 11: 5—11.
102.
Lu R., Malcuit I., Moffett P. et al. High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J2003; 22: 5690—5699.
103.
Weber AP, Oesterhelt C., Gross W. et al. EST-analysis of the thermoacidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol2004; 55: 17—32.
104.
Conrad ML, Pardy RL, Wainwright N., Child A., Armstrong PBResponse of the blood clotting system of the American horseshoe crab, Limulus polyphemus, to a novel form of lipopolysaccharide from a green alga. Comp Biochem Physiol A Mol IntegrPhysiol2006; 144: 423—428.
105.
Armstrong MT, Theg SM, Braun N., Wainwright N., Pardy RL, Armstrong PBHistochemical evidence for lipid A (endotoxin) in eukaryote chloroplasts. FASEB J2006; 20: 2145—2146.
