Abstract
Lipochitinoligosaccharides (LCOs) are made up of an N-acetylglucosamine backbone of four to five monosaccharide units bearing at it nonreducing end an N-linked fatty acyl chain. They are partly secreted as signaling molecules and are playing key roles in plant-root symbioses. However, these molecules are synthesized at the inner membrane and accumulated there. Therefore, they can be considered as membrane-associated lipids. We summarize in this chapter the outstanding contributions performed in the 1990s to the biosynthesis of these compounds in the rhizobium background, where the LCOs are named Nod factors. Recent work provided a new perspective to the time course of this complex biosynthetic pathway, and we will particularly elaborate it here. Finally, since Nod factor-like molecules were attested to be synthesized by the mycorrhiza, the actual trend is to understand their synthesis in fungi and to extend their inventory within this reign. Even if significant efforts are deployed nowadays, only little has been published on this topic. We aim to summarize these contributions to open up new avenues of investigation enabled by rapid genomic analysis.
References
Aoyama K, Haase A, Reeves PR (1994) Evidence for effect of the random genetic drift on G+C content after lateral transfer of fucose pathway genes to Escherichia coli K-12. Mol Biol Evol 11:829–838
Ardoundel M, Lortet G, Maillet F, Roche P, Truchet G, Promé JC, Rosenberg C (1995) In Rhizobium meliloti, the operon associated with the nod box n5 comprises nodL, noeA and noeB, three host-range genes specifically required for the nodulation of particular Medicago species. Mol Microbiol 17:687–699
Atkinson EM, Palcic MM, Hindsgaul O, Long SR (1994) Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acyltransferase activity. Proc Natl Acad Sci U S A 91:8418–8422
Barny MA, Downie JA (1993) Identification of NodC protein in the inner but not in the outer membrane of Rhizobium leguminosarum. Mol Plant-Microbe Interact 6:669–672
Bellato CM, Balatti PA, Pueppke SG, Krishnan H (1996) Proteins from cells of Rhizobium fredii bind to DNA sequences preceding nolX, a flavonoid inducible nod gene that is not associated with a nod box. Mol Plant-Microbe Interact 9:457–463
Berk S, Perret X, Quesada-Vincens D, Promé JC, Broughton WJ, Jabbouri S (1999) nolL of strain Rhizobium sp. NGR234 is required for O-acetyl-transferase activity. J Bacteriol 181:957–964
Bloemberg GV, Thomas-Oates JE, Lugtenberg BJJ, Spaink HP (1994) Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetyl glucosamine in vitro. Mol Microbiol 11:793–804
Bloemberg GV, Lagas R, van Leeuwen S, van der Marel G, van Boom JH, Lugtenberg BJJ, Spaink HP (1995) Substrate specificity and kinetic studies of nodulation protein NodL of Rhizobium leguminosarum. Biochemistry 34:12712–12720
Bulawa CE, Wasco W (1991) Chitin and nodulation. Nature 353:710
Byers DM, Gong H (2007) Acyl carrier protein: structure-function relationships in a conserved multifunctional protein family. Biochem Cell Biol 85:649–662
Cardenas L, Dominguez J, Quinto C, Lopez-Lara IM, Lugtemberg BJJ, Spaink HP, Rademaker GJ, Haverkamp J, Thomas-Oates JE (1995) Isolation, chemical structures and biological activities of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol Biol 29:453–464
D’Haeze W, Holsters M (2002) Nod factor structure, response and perception during initiation of nodule development. Glycobiology 12:79R–105R
Debellé F, Roche P, Plazanet C, Maillet F, Pujol C, Ardourel M, Demont N, Rosenberg C, Truchet G, Promé JC, Dénarié J (1995) The genetics of Rhizobium host-range control: allelic and non-allelic variation. In: Tikhonovich IA (ed) Nitrogen fixation: fundamentals and applications. Kluwer, Dordrecht, pp 275–280
Demont N, Debellé F, Aurelle H, Dénarié J, Promé JC (1993) Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors. J Biol Chem 268:20134–20142
Demont N, Ardourel M, Maillet F, Promé D, Ferro M, Promé JC, Dénarié J (1994) The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (omega-1)-hydroxylated fatty acids. EMBO J 13:2139–2149
Dénarié J, Debellé F, Rosenberg C (1992) Signaling and host range variation in nodulation. Annu Rev Microbiol 46:497–531
van der Drift KMGM, Spaink HP, Bloemberg BJJ, Haverkamp J, Thomas-Oates JE (1996) Rhizobium leguminosarum bv. trifolii produces Lipo-chitin oligosaccharides with nodE-dependent highly unsaturated fatty acyl moieties : an electrospray ionization and collision-induced dissociation tandem mass spectrometric study. J Biol Chem 271:22563–22569
Dutka-Malen S, Mazodier P, Badet B (1988) Molecular cloning and overexpression of the glucosamine synthase gene from Escherichia coli. Biochimie 70:287–290
Ehrhardt DW, Atkinson EM, Faull KF, Freedberg DI, Sutherlin DP, Amstrong R, Long SR (1995) In vitro sulfotransferase activity of NodH, a nodulation protein of Rhizobium meliloti required for host-specific nodulation. J Bacteriol 177:6237–6245
Fellay R, Hanin M, Montorzi G, Frey J, Freiberg C, Golinowski W, Staehelin C, Broughton WJ, Jabbouri S (1998) nodD2 of Rhizobium sp. NGR234 is involved in the repression of the nodABC operon. Mol Microbiol 27:1039–1050
Fernandez-Lopez M, D’Haeze W, Mergeart P, Verplancke C, Promé JC, van Montagu M, Holster M (1996) Role of NodI and NodJ in lipo chitooligosaccharide secretion in Azorhizobium caulinodans. Mol Microbiol 20:993–1000
Firmin JL, Wilson KE, Carlson RW, Davies AE, Dowie JA (1993) Resistance to nodulation of cv Afghanistan peas is overcome by nodX which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol Microbiol 10:351–360
Fisher RF, Egelhoff TT, Long SR (1988) Specific binding proteins from Rhizobium meliloti cell-free extracts containing nod to DNA sequences upstream of inducible nod genes. Genes Dev 2:282–293
Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharides involvement in establishing the Rhizobium-legume symbiosis. Revue Eur J Biochem 270:1365–1380
Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosentahl A, Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401
Garcia K, Delaux PM, Cope KR, Ané JM (2015) Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses. New Phytol 208:79–87
Geelen D, Leyman B, Mergaert P, Klarskov K, van Montagu M, Geremia R, Holsters M (1995) NodS is an S-adenosyl-L-methionine-dependent methyl transferase that methylates chitooligosaccharides deacetylated at the non-reducing end. Mol Microbiol 17:387–397
Geiger O, Spaink HP, Kennedy EP (1991) Isolation of the rhizobium leguminosarum NodF nodulation protein: NodF carries a 4′-phosphopantetheine prosthetic group. J Bacteriol 173:2872–2878
Geiger O, Thomas-Oates JE, Glushka J, Spaink HP, Lugtenberg BJJ (1994) Phospholipids of Rhizobium contain nodE-determined highly unsaturated fatty acid moieties. J Biol Chem 269:11090–11097
Geiger O, Glushka J, Lugtenberg BJJ, Spaink HP, Thomas-Oates JE (1998) NodFE-dependent fatty acids that lack an alpha-beta unsaturation are subject to differential transfer, leading to novel phospholipids. Mol Plant-Microbe Interact 11:33–44
Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, Rey T, Fournier J, Rochange S, Bécard G, Bonfante P, Barker DG (2013) Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198:190–202
Gianinazzi-Pearson V, Dénarié J (1997) Red carpet genetic programmes for root endosymbiosis. Trends in Plant Sci 2:371–372
Gough C, Jacquet C (2013) Nod factor perception protein carries weight in biotic interactions. Trends Plant Sci 18:566–574
Guasch-Vidal B, Estévez J, Dardanelli MS, Soria-Díaz ME, de Córdoba FF, Balog CI, Manyani H, Gil-Serrano A, Hensbergen PJ, Deelder AM, Megías M, van Brussel AA (2013) High NaCl concentrations induce the nod genes of Rhizobium tropici CIAT899 in the absence of flavonoid inducers. Mol Plant-Microbe Interact 26:451–460
Györgypàl Z, Kondorosi A (1991) Homology of the ligand-binding regions of Rhizobium symbiotic regulatory protein NodD and vertebrate nuclear receptors. Mol Gen Genet 226:337–340
Jabbouri S, Fellay R, Talmont F, Kamalaprija P, Burger U, Relic B, Promé JC, Broughton WJ (1995) Involvement of NodS in N-methylation and nod U in 6-carbamoylation of Rhizobium sp NGR234 nod factors. J Biol Chem 270:22968–22973
Jabbouri S, Relić B, Hanin M, Kamalaprija P, Burger U, Promé D, Promé JC, Broughton WJ (1998) nolO and noeI (HsnIII) of Rhizobium sp. NGR234 are involved in 3-O-carbamoylation and 2-O-methylation of Nod factors. J Biol Chem 273:12047–12055
John M, Röhrig H, Schmidt J, Wienecke U, Schell J (1993) Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc Natl Acad Sci U S A 90:625–629
Kafetzopoulos D, Thieros G, Vournakis JN, Bouriotis V (1993) The primary structure of a fungal chitin deacetylase reveals the function for two bacterial gene products. Proc Natl Acad Sci U S A 90:8005–8008
Kamst E, van der Drift KMGM, Thomas-Oates JE, Lugtenberg BJJ, Spaink HP (1995) Mass spectrometric analysis of chitin oligosaccharides produced by NodC protein in Escherichia coli. J Bacteriol 177:6282–6285
Kamst E, Bakkers J, Quaedvlieg NEM, Pilling J, Kijne JW, Lugtenberg BJJ, Spaink HP (1999) Chitin oligosaccharide synthesis by the bacterial NodC protein and zebrafish DG42 starts at the reducing terminal residue. Biochemistry 38:4045–4052
Kassaw T, Bridges W, Frugoli J (2015) Multiple Autoregulation of nodulation (AON) signals identified through split root analysis of Medicago truncatula sunn and rdn1 mutants. Plants 4:209–224
Kisner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518
Kiss E, Mergaert P, Olàh B, Kereszt A, Staehelin C, Davies AE, Downie JA, Kondorosi A, Kondorosi E (1998) Conservation of noIR in the Sinorhizobium and Rhizobium genera of the Rhizobiaceae Family. Mol Plant-Microbe Interact 12:1186–1195
Loh J, Stacey G (2003) Nodulation gene regulation in Bradyrhizobium japonicum: a unique integration of global regulatory circuits. Appl Environ Microbiol 69:10–17
López-Lara IM, Geiger O (2000) Expression and purification of four different rhizobial acyl carrier proteins. Microbiology 146:839–849
López-Lara IM, Geiger O (2001) The nodulation protein NodG shows the enzymatic activity of an 3-oxoacyl-acyl carrier protein reductase. Mol Plant-Microbe Interact 14:349–357
López-Lara IM, van den Berg JD, Thomas-Oates JE, Glushka J, Lugtenberg BJ, Spaink HP (1995) Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol Microbiol 15:627–638
López-Lara IM, Blog-Tip L, Quinto C, Garcia ML, Stacey G, Bloemberg GV, Lamers GEM, Lugtenberg BJJ, Thomas-Oates JE, Spaink HP (1996) NodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation signals. Mol Microbiol 21:397–408
Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63
Mergaert P, D’Haeze W, Geelen D, Promé D, van Montagu M, Geremia R, Promé JC, Holsters M (1995) Biosynthesis of Azorhizobium caulinodans nod factors: study of the activity of the NodABC proteins by expression of the genes in Escherichia coli. J Biol Chem 270:29217–29223
Mergeart P, D’Haeze W, Fernandez-Lopez M, Geelen D, Goethals K, Promé JC, von Montagu M, Holsters M (1996) Fucosylation and arabinosylation of nod factors in Azorhizobium caulinodans: involvements of nolK, nodZ as well as noeC and or downstream genes. Mol Microbiol 21:409–419
Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of beta-subclass of proteobacteria. Nature 411:948–950
Oldroyd GED (2013) Speak, friend and enter: signaling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263
Orgambide GG, Lee J, Hollingworth RI, Dazzo FB (1995) Structurally diverse chitooligosaccharide Nod factors accumulate primarily in membranes of wild type Rhizobium leguminosarum biovar trifolii. Biochemistry 34:3832–3840
Österman J, Marsh J, Laine PK, Zeng Z, Alatalo E, Sullivan JT, Young JPW, Thomas-Oates J, Paulin L, Lindström K (2014) Genome sequencing of two Neorhizobium galegae strains reveals a noeT gene responsible for the unusual acetylation of the nodulation factors. BMC Genomics 15:500
Perret X, Staehelin C, Broughton W (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201
Persson T, Battenberg K, Demin IV, Vigil-stenman T, Vanden Heuvel B, Puijic P et al (2015) Candidatus Frankia Datiscae Dg1, the Actinobacterial microsymbiont of Dastica glomerata, expresses the canonical nod genes nodABC in symbiosis with its host plant. PLoS ONE 10:e0127630. doi:10.1371/journal.pone.0127630
Pohl A, Devaux PF, Herrmann A (2005) Function of prokaryotic and eukaryotic ABC proteins in lipid transport. Biochim Biophys Acta 1733:29–52
Poinsot V, Crook MB, Erdn S, Maillet F, Bascaules A, Ané JM (2016) New insights into Nod factor biosynthesis: analyses of chitooligomers and lipo-chitooligomers of Rhizobium sp. IRBG mutants. Carbohydr Res 434:83–93
Price NPJ, Talmont F, Wieriszeski JM, Promé D, Promé JC (1996) Structural determination of symbiotic nodulation factors from the broad host-range Rhizobium species NGR234. Carbohydr Res 289:115–136
Pueppke SG (1996) The genetic and biochemical basis for nodulation of legumes by rhizobia. Crit Rev Biotechnol 16:1–51
Quesada-Vincens D, Hanin M, Fellay R, Broughton WJ, Jabbouri S (1998) In vitro sulfotransferase activity of noeE, a nodulation protein of rhizobium sp. NGR234. Mol Plant-Microbe Interact 11:592–600
Quinto C, Wijfjes AHM, Bloemberg GV, Blog-Tip L, Lopès-Lara IM, Lugtenberg BJJ, Thomas-Oates JE, Spaink HP (1997) Bacterial nodulation protein NolZ is a chitin oligosaccharide fucosyl transferase which can also recognize related substrates of animal origin. Proc Natl Acad Sci U S A 94:4336–4341
Rao JR, Cooper JE (1994) Rhizobia catabolize nod gene inducing flavonoids via C-ring fission mechanisms. J Bacteriol 176:5409–5413
van Rijn P, Feys B, Verreth C, Vanderleyden J (1993) Multiple copies of nodD in Rhizobium tropici CIAT899 and BR816. J Bacteriol 175:438–447
Ritsema T, Wijfjes AHM, Lugtenberg BJJ, Spaink HP (1996) Rhizobium nodulation protein NodA is a host-specific determinant of the transfer of fatty acids in nod factor biosynthesis. Mol Gen Genet 251:44–51
Rivilla R, Sutton JM, Downie JA (1995) Rhizobium leguminosarum nodT is related to a family of outer-membrane transport proteins that includes TolC, PrtF, CyaE and AprF. Gene 161:27–31
Sadowsky MJ, Cregan PB, Gottfert M, Sharma A, Gerhold D, Rodriguez-Quinones F, Keyser HH, Hennecke H, Stacey G (1991) The bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans. Proc Natl Acad Sci U S A 88:637–641
Schlaman HRM, Phillips DA (1998) Genetic organization and transcriptional regulation of Rhizobial nodulation genes. In Spaink HP, Kondorosi E, Hooykaas HH (eds) The Rhizobiaceae Springer, Dordrecht, 361–386
Schlaman HRM, Spaink HH, Okker RJK, Lugtenberg BJJ (1989) Subcellular localization of the nod gene product in Rhizobium leguminosarum. J Bacteriol 171:4686–4693
Schmidt J, Wingender R, John M, Wieneke U, Schell J (1988) Rhizobium meliloti nodA and nodB genes are involved in generating compounds that stimulates mitosis of plant cells. Proc Natl Acad Sci U S A 83:9581–9585
Schmidt J, John M, Wieneke U, Stacey G, Röhring H, Schell J (1991) Studies of the function of Rhizobium meliloti nodulation genes. In: Hennecke H, Verma DPS (eds) Advances in molecular genetics of plant-microbe interactions. Kluwer, Dordrecht, pp 150–155
Schmidt PE, Broughton WJ, Werner D (1994) Nod factor of Bradyrhizobium japonicum and Rhizobium sp NGR234 induce flavonoid accumulation in soybean root exudate. Mol Plant-Microbe Interact 7:384–390
Schultze M, Staehlin C, Röhrig H, John M, Schmidt J, Kondorosi E, Schell J, Kondorosi A (1995) In vitro sulfotransferase activity or Rhizobium meliloti NodH protein: Lipochitooligosaccharide nodulation signal are sulfated after synthesis of the core structure. Proc Natl Acad Sci U S A 92:2706–2709
Schwedock JS, Long SR (1990) ATP sulphurylase activity of nodP and nodQ gene products of Rhizobium meliloti. Nature 348:644–647
Schwedock JS, Liu CX, Leyh TS, Long SR (1994) Rhizobium meliloti NodP and NodQ form a multifunctional sulfate-activating complex requiring GTP for activity. J Bacteriol 176:7055–7064
Slabas AR, Chase D, Nishida I, Murata N, Sidebottom C, Safford R, Sheldon PS, Kekwick RG, Hardie DG, Mackintosh RW (1992) Molecular cloning of higher-plant 3-oxoacyl-(acyl carrier protein) reductase. Sequence identities with the nodG-gene product of the nitrogen-fixing soil bacterium Rhizobium meliloti. Biochem J 283:321–326
Snoek C, Luyten E, Poinsot V, Savagnac A, Vanderleyden J, Promé JC (2001) Rhizobium sp. BR816 produces a complex mixture of known and novel lipooligosaccharide molecules. Mol Plant-Microbe Interact 14:678–684
Spaink HP, Aarts A, Stacey G, Bloemberg GV, Lugtenberg BJJ, Kennedy EP (1992) Detection and separation of Rhizobium and Bradyrhizobium Nod metabolites using thin layer chromatography. Mol Plant-Microbe Interact 5:72–80
Spaink HP, Wijfjes AHM, van der Drift KMGM, Haverkamp J, Thomas-Oates JE, Lugtenberg BJJ (1994) Structural identification of metabolites produced by the NodB and NodC proteins of Rhizobium leguminosarum. Mol Microbiol 13:821–831
Swanson JA, Mulligan JT, Long SR (1993) Regulation of syrM and nodD3 in Rhizobium meliloti. Genetics 134:435–444
Treilhou M, Ferro M, Monteiro C, Poinsot V, Jabbouri S, Kanony C, Promé D, Promé JC (2000) Differentiation of O-acetyl and O-Carbamoyl esters of N-acetyl-glucosamine by decomposition of their oxonium ions. Application to the structure of the nonreducing terminal residue of Nod factors. J Am Soc Mass Spectrom 11:301–311
Vazquez M, Santana O, Quinto C (1993) The NodI and NodJ proteins from Rhizobium and Bradyrhizobium strains are similar to capsular polysaccharide secretion proteins from gram negative bacteria. Mol Microbiol 5:71–75
Yang GP, Debellé F, Savagnac A, Ferro M, Schiltz O, Maillet F, Promé D, Treilhou M, Vialas C, Lindström K, Promé JC (1999) Structure of the Mesorhizobium huakii and Rhizobium galegea Nod factors: a cluster of phylogenetically related legumes are nodulated by rhizobia producing Nod factors with α,β-unsaturated N-acyl substitutions. Mol Microbiol 34:227–237
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Poinsot, V., Couderc, F. (2017). Formation of Lipochitin Oligosaccharide Signaling Molecules. In: Geiger, O. (eds) Biogenesis of Fatty Acids, Lipids and Membranes. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-43676-0_64-1
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