Abstract
In addition to the flavonoids exuded by many legumes as signals to their rhizobial symbionts, alfalfa (Medicago sativa L.) releases two betaines, trigonelline and stachydrine, that induce nodulation (nod) genes in Rhizobium meliloti. Experiments with 14C-phenylalanine in the presence and absence of phenylalanine ammonia-lyase inhibitors show that exudation of flavonoid nod-gene inducers from alfalfa roots is linked closely to their concurrent synthesis. In contrast, flavonoid and betaine nod-gene inducers are already present on mature seeds before they are released during germination. Alfalfa seeds and roots release structurally different nod-gene-inducing signals in the absence of rhizobia. When R. meliloti is added to roots, medicarpin, a classical isoflavonoid phytoalexin normally elicited by pathogens, and a nod-gene-inducing compound, formononetin-7-O-(6″-O-malonylglycoside), are exuded. Carbon flow through the phenylpropanoid pathway and into the flavonoid pathway via chalcone synthase is controlled by complex cis-acting sequences and trans-acting factors which are not completely understood. Even less information is available on molecular regulation of the two other biosynthetic pathways that produce trigonelline and stachydrine. Presumably the three separate pathways for producing nod-gene inducers in some way protect the plant against fluctuations in the production or transmission of the two classes of signals. Factors influencing transmission of alfalfa nod-gene inducers through soil are poorly defined, but solubility differences between hydrophobic flavonoids and hydrophilic betaines suggest that the diffusional traits of these molecules are not similar. Knowledge derived from studies of how legumes regulate rhizobial symbionts with natural plant products offers a basis for defining new fundamental concepts of rhizosphere ecology.
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References
Amblès A, Jacquesy J C, Jambu P, Joffre J and Maggi-Churin R 1991 Polar lipid fraction in soil: a kerogen-like matter. Organic Geochem. 17,341–349.
Amrhein N and Gödeke K-H 1977 α-Aminooxy-β-phenylpropionic acid -a potent inhibitor of L-phenylalanine ammonia-lyase in vitro and in vivo. Plant Sci. Lett. 8, 313–317.
Ayabe S-I, Udagawa A and Furuya T 1988 NAD(P)H-dependent 6’-deoxychalcone synthase activity in Glycyrrhiza cells induced by yeast extract. Arch. Biochem. Biophys. 261, 458–462.
Barz W 1970 Isolation of rhizosphere bacterium capable of degrading flavonoids. Phytochemistry 9, 1745–1749.
Beilstein Handbook of Organic Chemistry. 1991. 4th edition. Springer-Verlag, Berlin.
Bernard T, Pocard J-A, Perroud B and Le Rudulier D 1986 Variations in the response of salt-stressed Rhizobium strains to betaines. Arch. Microbiol. 143, 359–364.
Boivin C, Barran L R, Malpica C A and Rosenberg C 1991 Genetic analysis of a region of the Rhizobium meliloti pSym plasmid specifying catabolism of trigonelline, a secondary metabolite present in legumes. J. Bacteriol. 173,2809–2817.
Caetano-Anollés G, Crist-Estes D K and Bauer W D 1988 Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J. Bacteriol. 170,3164–3169.
Cooper J E and Rao J R 1992 Localized changes in flavonoid biosynthesis in roots of Lotus pedunculatus after infection by Rhizobium loti. Plant Physiol. 100, 444–450.
Dakora F D, Joseph C M and Phillips D A 1993 Alfalfa root exudates contain isoflavonoids in the presence of Rhizobium meliloti. Plant Physiol. 101, 819–824.
Dalkin K, Edwards R, Edington B and Dixon R A 1990 Stress responses in alfalfa (Medicago sativa L.) I. Induction of phenylpropanoid biosynthesis and hydrolytic enzymes in elicitor-treated cell suspensions cultures. Plant Physiol. 92, 440–446.
D’ Arcy-Lameta A 1986 Study of soybean and lentil root exudates II. Identification of some polyphenolic compounds, relation with plantlet physiology. Plant and Soil 92, 113–123.
Dénarié J, Debellé F and Rosenberg C 1992 Signaling and host range variation in nodulation. Annu. Rev. Microbiol. 46,497–531.
Dharmatilake A J and Bauer W D 1992 Chemotaxis of Rhi zobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Appl. Environ. Microbiol. 58, 1153–1158.
Dixon R A and Lamb C J 1990 Regulation of secondary metabolism at the biochemical and genetic levels. In Secondary Products from Plant Tissue Culture. Ed. B V Charl-wood and M J C Rhodes. pp 103–118. Clarendon Press, Oxford.
Dornbos D L, Spencer G F and Miller R W 1990 Medicarpin delays alfalfa seed germination and seedling growth. Crop Sci. 30, 162–166.
Estabrook, E M and Sengupta-Gopalan C 1991 Differential expression of phenylalanine ammonia-lyase and chalcone synthase during soybean nodule development. Plant Cell 3, 299–308.
Firmin J L, Wilson K E, Rossen L and Johnston A W B 1986 Flavonoid activation of nodulation genes in Rhizobium reversed by other compounds present in plants. Nature 324, 90–92.
Fisher R F and Long S R 1992 Rhizobium-plmí signal exchange. Nature 357, 655–660.
Fougère F and Le Rudulier D 1990 Uptake of glycine betaine and its analogues by bacteroids of Rhizobium meliloti. J. Gen. Microbiol. 136, 157–163.
Gajendiran N and Mahadevan A 1990 Utilization of phenolic substances by Rhizobium sp. Ind. J. Exp. Biol. 28, 1136–1140.
Geissman T A and Clinton R O 1946 Flavanones and related compounds. I. The preparation of polyhydroxyçhalcones and flavanones. J. Am. Chem. Soc. 68, 697–700..
Gloux K and Le Rudulier D 1989 Transport and catabolism of proline betaine in salt stressed Rhizobium meliloti. Arch. Microbiol. 151, 143–148.
Goldmann A, Boivin C, Fleury V, Message B, Lecoeur L, Maille M and Tepfer D 1991 Betaine use by rhizosphere bacteria: genes essential for trigonelline, stachydrine, and carnitine catabolism in Rhizobium meliloti are located on pSym in the symbiotic region. Mol. Plant-Microbe Inter.4, 571–578.
Göttfert M, Horvath B, Kondorosi E, Putnoky P, Rodriguez-Quinones F and Kondorosi A 1986 At least two different nodD genes are necessary for efficient nodulation on alfaifa by Rhizobium meliloti. J. Mol. Biol. 191, 411–420.
Gustine D L, Sherwood R T and Vance C P 1978 Regulation of phytoalexin synthesis in jackbean callus cultures. Plant Physiol. 61, 226–230.
Hans N and Grover S K 1993 An efficient conversion of 2’-hydroxychalcones to flavones. Synthetic Comm. 23, 1021–1023.
Harborne J B (Ed.) 1988 The Flavonoids, Advances in Research Since 1980. Chapman and Hall, London. 621P.
Harrison M J, Choudhary A D, Dubery I, Lamb C J and Dixon R A 1991a Stress responses in alfalfa (Medicago sativa L.). 8. Cis-elements and trans-acting factors for the quantitative expression of a bean chalcone synthase gene promoter in electroporated alfalfa protoplasts. Plant Molec. Biol. 16, 877–890.
Harrison M J, Lawton M A, Lamb C J and Dixon R A 1991b Characterization of a nuclear protein that binds to three elements within the silencer region of a bean chalcone synthase gene promoter. Proc. Natl. Acad., Sci. USA 88, 2515–2519.
Hartwig U A, Joseph C M and Phillips D A 1991 Flavonoids released naturally from alfalfa seeds enhance growth rate of Rhizobium meliloti. Plant Physiol. 95, 797–803.
Hartwig U A, Maxwell C A, Joseph C M and Phillips D A 1990a Chrysoeriol and luteolin released from alfalfa seeds induce nod genes in Rhizobium meliloti. Plant Physiol. 92, 116–122.
Hartwig U A, Maxwell C A, Joseph C M and Phillips D A 1990b Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes. J. Bacteriol. 172,2769–2773.
Hartwig U A and Phillips D A 1991 Release and modification of nod-gene-inducing flavonoids from alfalfa seeds. Plant Physiol. 95, 804–807.
Harwood L M, Loftus G C, Oxford A and Thomson C 1990 An improved procedure for cyclisation of chalcones to flavanones using celite supported potassium fluoride in methanol: total synthesis of bavachinin. Syn. Comm. 20, 649–657.
Honma M A and Ausubel F M 1987 Rhizobium meliloti has three functional copies of the nodD symbiotic regulatory gene. Proc. Natl. Acad. Sci., USA 84, 8558–8562.
Hungria M, Joseph C M and Phillips D A 1991 Anthocyanidins and flavonols, major nod-gene inducers from seeds of a black-seeded common bean (Phaseolus vulgaris L.). Plant Physiol. 97, 751–758.
Ingham J L 1983 Naturally occurring isoflavonoids (1855-1981). Fortschritte d. Chem. org. Naturst. 43, 1–266.
Jones G P, Naidu B P, Starr R K and Paleg L G 1986 Estimates of solutes accumulating in plants by 1H nuclear magnetic resonance spectroscopy. Aust. J. Plant Physiol. 13, 649–658.
Kosslak R M, Bookland R, Barkei J, Paaren H E and Appelbaum E R 1987 Induction of Bradyrhizobium japonicum common nod gene by isoflavones isolated from Glycine max. Proc. Natl. Acad. Sci., USA 84, 7428–7432.
Köster J, Strack D and Barz W 1983 High performance liquid chromatographic separation of isoflavones and structural elucidation of isoflavone 7-O-glucoside 6“malonates from Cicer arietinum. J. Med. Planta Res. 48, 131–135.
Lam S T, Ellis D M and Ligon J M 1991 Genetic approaches for studying rhizosphere colonization. In The Rhizosphere and Plant Growth. Ed. D L Keister and P B Cregan. pp 43–50. Kluwer Academic Publ, Dordrecht.
León-Barrios M, Dakora F D, Joseph C M and Phillips D A 1993 Isolation of Rhizobium meliloti nod gene inducers from alfalfa rhizosphere soil. Appl. Environ. Microbiol. 59, 636–639.
Loake G J, Choudhary A D, Harrison M J, Mavandad M, Lamb C J and Dixon R A 1991 Phenylpropanoid pathway intermediates regulate transient expression of a chalcone synthase gene promoter. Plant Cell 3, 829–840.
Maxwell C A, Edward R and Dixon R A 1992 Identification, purification and characterization of S-adenosyl-L-methonine: isoliquiritigenin 2’-O-methyltransferase from alfalfa (Medicago sativa L.). Arch. Biochem. Biophys. 293, 158–166.
Maxwell C A, Harrison M J and Dixon R A 1993 Molecular characterization and expression of alfalfa isoliquiritigenin 2’-O-methyltransferase, an enzyme specifically involved in the biosynthesis of a transcriptional activator of Rhizo bium meliloti nodulation genes. Plant J. 4, 971–981.
Maxwell C A, Hartwig U A, Joseph C M and Phillips D A 1989 A chalcone and two related flavonoids released from alfalfa roots induce nod genes in Rhizobium meliloti. Plant Physiol. 91, 842–847.
Maxwell C A and Phillips D A 1990 Concurrent synthesis and release of nod-gene-inducing flavonoids from alfalfa roots. Plant Physiol. 93, 1552–1558.
Morgan A and Marion L 1956 The biogenesis of alkaloids XVII. Further study of the role of ornithine in the biogenesis of stachydrine. Can. J. Chem. 34, 1704–1708.
Musich J A and Rapoport H 1977 Reaction of O-methyl-N,N’-diisopropylisourea with amino acids and amines. J. Org. Chem. 42, 139–141.
Parniske M, Zimmermann C, Cregan P B and Werner D 1990 Hypersensitive reaction of nodule cells in the Glycine sp./Bradyrhizobium japonicum-symbiosis occurs at the genotype-specific level. Bot. Acta 103, 143–148.
Peters N K, Frost J W and Long S R 1986 plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233, 977–980.
Phillips D A 1992 Flavonoids: plant signals to soil microbes. In Phenolic Metabolism in Plants. Eds. H A Stafford and R K Ibrahim, Plenum Press, New York. Rec. Adv. Phytochem. 26, 201–231.
Phillips D A, Dakora F D, León-Barrios M, Sande E and Joseph C M 1993 Signals released from alfalfa regulate microbial activities in the rhizosphere. In New Horizons in Nitrogen Fixation. Ed. R Palacios, J Mora and W E Newton. pp 197–206. Nijhoff/Junk, Dordrecht.
Phillips D A, Joseph C M and Maxwell C A 1992 Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol. 99, 1526–1531.
Rao J R, Sharma N D, Hamilton J T G, Boyd D R and Cooper J E 1991 Biotransformation of the pentahydroxy flavone quercetin by Rhizobium loti and Bradyrhizobium strains (Lotus). Appl. Environ. Microbiol. 57, 1563–1565.
Recourt K, Schripsema J, Kijne J W, Van Brussel A A N and Lugtenberg B J J 1991 Inoculation of Vicia sativa subsp. nigra roots with Rhizobium leguminosarum biovar viciae results in release of nod gene activating flavanones and chalcones. Plant Mol. Biol. 16, 841–852.
Recourt K, van Tunen A J, Mur L A, van Brussel A A N, Lugtenberg B J J and Kijne J W 1992 Activation of flavonoid biosynthesis in roots of Vicia sativa subsp. nigra by inoculation with Rhizobium leguminosarum biovar viciae. Plant Molec. Biol. 19: 411–420.
Redmond J W, Batley M, Djordjevic M A, Innes R W, Kuempel P L and Rolfe B G 1986 Flavones induce expression of nodulation genes in Rhizobium. Nature 323, 632–635.
Robertson A V and Marion L 1960 The biogenesis of alkaloids XXV. The role of hygric acid in the biogenesis of stachydrine. Can. J. Chem. 38, 396–398.
Rolfe B G, Batley M, Redmond J W, Richardson A E, Simpson R J, Bassam B J, Sargent C L, Weinman J J, Djordjevic M A, and Dazzo F B 1988 Phenolic compounds secreted by legumes. In Nitrogen Fixation: Hundred Years After. Ed. H Bothe, F J de Bruijn and W E Newton. pp 405–409. Gustav Fischer, Stuttgart.
Rovira A D and Harris J R 1961 Plant root excretions in relation to the rhizosphere effect V. The exudation of Bgroup vitamins. Plant and Soil 14, 199–214.
Ryder T B, Hedrick S A, Bell J N, Liang X, Clouse S D and Lamb C J 1987 Organization and differential activation of a gene family encoding the plant defense enzyme chalcone synthase. Molec. Gen. Genet. 210, 219–233.
Sanjuan J and Olivares J 1989 Implication of nifA in the regulation of genes located on a Rhizobium meliloti cryptic plasmid that affects nodulation efficiency. J. Bacteriol. 171,4154–4161.
Schmidt J, John M, Wieneke U, Krüssmann H-D and Schell J 1986 Expression of the nodulation gene nodA in Rhizo bium meliloti and localization of the gene product in the cytosol. Proc. Natl. Acad. Sci., USA 83, 9581–9585.
Seshadri TR 1962 Interconversions of flavonoid compounds. In The Chemistry of Flavonoid Compounds. Ed. T A Geissman. pp. 156–196. McMillan, NY.
Sethi J K and Carew D P 1974 Growth and betaine formation in Medicago sativa tissue cultures. Phytochemistry 13, 321–324.
Siqueira J O, Nair M G, Hammerschmidt R and Safir G R 1991 Significance of phenolic compounds in plant-soilmicrobial systems. Crit. Rev. Plant Sci. 10, 63–121.
Spaink H P 1992 Rhizobial lipo-oligosaccharides: answers and questions. Plant Molec. Biol. 20, 977–986.
Srivastava S D and Srivastava S K 1987 Synthesis of a new flavone Ind. J. Chem. 26B, 257–58.
Stafford H A 1990 Flavonoid Metabolism. CRC Press, Boca Raton, Florida. 298 p.
Steenbock H 1918 Isolation and identification of stachydrin from alfalfa hay. J. Biol. Chem. 35, 1–13.
Taguchi H, Nishitani H, Okumura K, Shimabayashi Y and lwai K 1989a Biosynthesis and metabolism-of NAD in Lemna paucicostata 151. Agric. Biol. Chem. 53, 1543–1549.
Taguchi H, Nishitani H, Okumura K, Shimabayashi Y and lwai K 1989b Biosynthesis and metabolism of trigonelline in Lemna paucicostata 151. Agric. Biol. Chem. 53, 2867–2871.
Taguchi H and Shimabayashi Y 1983 Findings of trigonelline demethylating enzyme activity in various organisms and some properties of the enzyme from hog liver. Biochem. Biophys. Res. Comm. 113, 569–574.
Tramontano W A, McGinley P A, Ciancaglini E F and Evans L S 1986 A survey of trigonelline concentrations in dry seeds of the Dicotyledoneae. Environ. Expt. Bot. 26, 197–205.
Upmeier B, Gross W, Köster S and Barz W 1988 Purification and properties of S-adenosyl-L-methionine: nicotinic acid-N-methyltransferase from cell suspension cultures of Glycine max L. Arch. Biochem. Biophys. 262, 445–454.
Welle R and Grisebach H 1989 Phytoalexin synthesis in soybean cells: elicitor induction of reductase involved in biosynthesis of 6’-deoxychalcone. Arch. Biochem. Biophy. 272, 97–102.
Wiehler G and Marion L 1958 The biogenesis of alkaloids XX. The induced biogenesis of stachydrine. J. Biol. Chem. 231,799–805.
Wolk C P, Cai Y and Panoff J M 1991 Use of a transposon with luciferase as a reporter to identify environmentally responsive genes in a cyanobacterium. Proc. Natl. Acad. Sci., USA 88, 5355–5359.
Wyn Jones R G and Storey R 1981 Betaines In Physiology and Biochemistry of Drought Resistance in Plants. Ed. L G Paleg and D Aspinall. pp 171–204. Academic Press, Sydney.
Zoń J and Amrhein N 1992 Inhibitors of phenylalanine ammmonia-lyase: 2-aminoindan-2-phophonic acid and related compounds. Liebigs Ann. Chem. 1992, 625–628.
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Phillips, D.A., Dakora, F.D., Sande, E., Joseph, C.M., Zoń, J. (1994). Synthesis, release, and transmission of alfalfa signals to rhizobial symbionts. In: Graham, P.H., Sadowsky, M.J., Vance, C.P. (eds) Symbiotic Nitrogen Fixation. Developments in Plant and Soil Sciences, vol 57. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-1088-4_7
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