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A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia

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Frankia Symbiosis

Abstract

Phenylacetic hopanetetrol is a Frankia specific lipid present in vesicles. Phenylacetic acid (PAA) is known as an auxinomimetic, exhibiting the same effect on plant growth as indole acetic acid (IAA). We hypothesize that PAA, only bound by an ester link to the hopanetetrol basic unit, would be easily released and could thus play a role in nodule formation. HPLC and mass spectrometry analysis allowed us to show that 2 Alnus- (ACoN24d and ACN14a) and 2 Elaeagnus-infective strains (EaI1 and EaI3) released PAA into the culture medium, at concentrations of about 10−5 to 10−6 M, whereas IAA was not detected. Furthermore, exogenous PAA added to axenically-grown Alnus glutinosa roots at a concentration of 5 × 10−5 M, resulted in the formation of thick, short lateral roots which resembled actinorhizal nodules. phenylalanine ammonia lyase (PAL) and chalcone syntase (CHS) induction by incompatible and compatible Frankia strains in A. glutinosa roots and the different contents in salicylic acid precursors (cinnamic acid and benzoic acid) observed between nodules and roots support the idea that PAA would be produced in nodules to the detriment of salicylic acid production. These results provide evidence that in actinorhizal root nodules, phenylpropanoid metabolism may play a multiple role in symbiotic interactions including the limitation of the induction of the systematic acquired resistance (SAR) by the plant.

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References

  • Akao S, Nakata S and Yoneyama T 1991 Formation of nodules on non-nodulating soybean T201 after treatment with 2,4dichlorophenoxy-acetate. Plant Soil 138, 207–212.

    Article  CAS  Google Scholar 

  • Albrecht C, Geurts R, l.apeyrie F and Bisseling T 1998 Endomycorrhizae and rhizobial Nod factors both require pSYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD I2A. Plant J. 15, 605–614.

    CAS  Google Scholar 

  • Baron C and Zambriski P C 1995 The plant response in pathogcnis, symbiosis and wounding: variations in a common theme. Ann. Rev. Genet. 29, 107–129.

    Article  PubMed  CAS  Google Scholar 

  • Bennett R N and Wallsgrove R M 1994 Secondary metabolites in plant defence mechanisms. New Phytol. 127, 617–633.

    Article  CAS  Google Scholar 

  • Beringer J E 1974 R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84, 188–198.

    Article  PubMed  CAS  Google Scholar 

  • Berry A M, Harriott O T, Moreau R A. Osman S F, Benson D R and Jones A D 1993 Hopanoid lipids compose the Frankia vesicle envelope presumptive barrier of oxygen diffusion to nitrogenase. Proc. Natl. Acad. Sci. USA 90, 6091–6094.

    Google Scholar 

  • Berry A M, Kahn R K S, and Booth M C 1989 Identification of in-dole compounds secreted by Frankia HFPAr13 in defined culture medium. Plant Soil 118, 205–209.

    Article  CAS  Google Scholar 

  • Bertrand H, Pinochet X and Cleyet-Marrcl J C 1996 Induction de pseudonodosités sur les racines de colza par traitement hormonal et modifications morphologiques du système racinaire accompagnant leur formation. OCL 3. 213–219.

    Google Scholar 

  • Beyrle H 1995 The role of phytohormones in the function and biology of mycorrhizas. In Mycorrhiza: Structure, Molecular Biology and Function. Eds. Varma A K and Hocks B. pp. 365–390. Springer-Verlag, Berlin.

    Google Scholar 

  • Bhuvaneswari TV and Solheim B 1985 Root hair deformation in the white clover/ Rhizobium trifolii symbiosis. Physiol. Plant. 63, 25–34.

    Article  CAS  Google Scholar 

  • Christensen-Weninger C and Vanderleyden J 1994 Ammonium-excreting Azospirillmn sp. become intracellularly in maize (zea mays) para-nodules. Biol. Fertil. Soils 17, 1–8.

    Article  Google Scholar 

  • Cooper J B and Long S R 1994 Morphogenetic rescue of Rhizobium meliloti nodulation mutant by trans-Zeatin secretion. Plant Cell. 6, 215–225.

    PubMed  CAS  Google Scholar 

  • Coquoz J L, Buchala A and Metraux J P 1998 The biosynthesis of salicylic acid in potato plant. Plant. Physiol. 117, 1095–1101.

    Google Scholar 

  • Costacurta A and Vanderleyden J 1995 Synthesis of phytohormones by plant-associated bacteria. Crit. Rev. Microbiol. 21, 1–18.

    Article  PubMed  Google Scholar 

  • De Billy F, Grosjean C, May S, Bennett M and Cullimore J V 2001 Expression studies on AUXI -like genes in Medicago trunratula suggest that auxin is required at two steps in early nodule development. Mol. Plant Microb. Interact. 14,267–277

    Google Scholar 

  • Déparié J. Debellé F and Promé J C 1996 Rhizobium lipochitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Ann. Rev. Biochem. 65,503–535.

    Google Scholar 

  • Eastbrook E M and Sengupta-Gopalan C 1991 Differential expression of phenylalaine ammonia -lyasc and chalcone synthase during soybean nodule development. Plant Cell 3, 299–308.

    Google Scholar 

  • Ernsten A, Sandberg G, Crozier A and Wheeler C T 1987 Endogenous indoles and the biosynthesis and metabolism of indole3–acetic acid in cultures of Rhizobieun phaseoli. Planta 171, 422–-428.

    Google Scholar 

  • Fahraeus G 1957 The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16. 374–381.

    Article  PubMed  CAS  Google Scholar 

  • Franche C, Laplaze L, Duhoux E and Bogusz D 1998 Actinorhizal symbioses: recent advances in plant molecular and genetic transformation studies. Critical Reviews in Plant Sciences 17, 1–28.

    Article  CAS  Google Scholar 

  • Fries L 1977 Growth regulating effects of phenylacetic acid and phydroxy-phcnylacetic acid on Fucus spiralis L. (Phaccophyccac, Fucales) in axenic culture. Phycol. 16, 451–455.

    Article  CAS  Google Scholar 

  • Gaffney T, Friedrich L Vernooij B, Negrotto D and Nye G 1993 Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754–756.

    Article  PubMed  CAS  Google Scholar 

  • Gamas P, de Billy F and Truchet G 1998 Symbiosis-specific expression of two Medicago truncatula nodulin genes, MINI and MtNI3, encoding products homologous to plant defense proteins. Mol. Plant Microb. Interact. 11, 393–403.

    CAS  Google Scholar 

  • Gogala N 1991 Regulation of mycorrhizal infection by hormonal factors produced by hosts and fungi. Experientia 47, 331–340.

    Article  CAS  Google Scholar 

  • Gramatica P, Ranzi B M and Manitto P 1981 Decarboxylation of cinnamic acids by Saccharomyces cerevi.siae. Bioorganic Chem. 10, 14–21.

    Article  CAS  Google Scholar 

  • Hammad Y, Maréchal J, Cournoyer B, Normand P and Domenach A M 2001 Modification of the protein expression pattern induced in the nitrogen-fixing actinomycete Frankia sp. strain ACN14atsr by root exudates of its symbiotic host A/mms glutinosa and cloning of the sodF gene. Can. J. Microbiol. 47, 541–547.

    Google Scholar 

  • Harley S E 1999 Are gall insects large rhizobia? Oikos 84, 333–342.

    Article  Google Scholar 

  • Hwang B K, Lim S W, Kim B S, Lcc J Y and Moon S S 2001 Isolation and in vivo and in vitro antifungal activity of phenylacetic acid and sodium phenylacetate from Streptomyces humides. Appt. Environ. Microbiol. 67, 3739–3745.

    Google Scholar 

  • Isogai Y, Okamoto T and Koizumi T 1967 Isolation of indole3–acetamide, 2–phenylacetamide and indole-3–carboxaldehyde from etiolated seedlings of Phaseolus. Chem. Pharm. Bull. Tokyo 15, 151–158.

    Google Scholar 

  • Kleeman G, Alskog G and Berry A 1994 Lipid composition and nitrogenase activity of symbiotic Frankia (Ahrus incana) in response to different oxygen concentration. Protoplasma 183, 107–115.

    Article  Google Scholar 

  • Laplaze L, Gherbi H, Frutz T, Pawlowski K. Franche C. Macheix J J, Auguy F, Bogusz D and Duhoux E. Flavan-containing cells delimit Frankia-infected compartments in Casuarina gle,uco nodules. Plant Physiol. 121, 113–22.

    Google Scholar 

  • Lawton M A and Lamb C J 1987 Transcriptional activation of plant defense genes by fungal elicitor, wounding and infection. Mol. Cell. Biol. 7, 335–341.

    PubMed  CAS  Google Scholar 

  • Loper J E and Schroth M N 1986 Influence of bacterial sources of indole-3 acetic acid on root elongation of sugar beet. Phytopathol. 76, 386–389.

    Article  CAS  Google Scholar 

  • Luckner M 1972 Secondary Metabolism in Plants and Animals. Chapman and Hall, London. 344–365.

    Google Scholar 

  • Martinez-Abarca F, Herrera-Cernera J A, Bueno P, Sanjuan J, Bisseling T and Olivares J 1998 Involvement of salicylic acid in the establishment of the Rhizobium /nett/oh-Alfalfa symbiosis. Mol. Plant Microb. Interact. 11, 153–155.

    Google Scholar 

  • Mathesius U. Schlaman H R M, Spaink H P, Sautter C, Rolfe B G and Djordjevic M A 1998 Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin ologosaccharides. Plant J. 14, 23–34.

    Article  PubMed  Google Scholar 

  • Milborrow B V, Purse.1 G and Wightman F 1975 On the auxin activity of phenylacetic acid. Ann. Bot. 39, 1 143–1 146.

    Google Scholar 

  • Murry M, Fontaine M S and Torrey J G 1984 Growth kinetics and nitrogenase induction in Frankia sp. HFPAr13 grown in batch culture. Plant Soil 78, 61–78.

    Google Scholar 

  • Nalin R, Normand P and Domenach A M 1997. Distribution and N2–fixing activity of Frankia strains in relation to soil depth. Physiol. Plant. 99, 732–738.

    Google Scholar 

  • Nalin R, Putra S R, Domenach A M, Rohmer M, Gourbiere F and Berry A M 2000 High hopanoid/total lipid ratio in Frankia cells is not related to the nitrogen status. Microbiology 146, 30133019.

    Google Scholar 

  • Normand P and Lalonde M 1982 Evaluation of Frankia strains isolated from provenances of two Abuts species. Can. J. Microbiol. 28. 1133–1142.

    Article  Google Scholar 

  • Parniske M 2000 Intracellular accomodation of microbes by plants: a common developmental progam for symbiosis and disease ? Curr. Opin. Plant Biol. 3, 320–328.

    Article  PubMed  CAS  Google Scholar 

  • Patten C L and Glick B R 1996 Bacterial biosynthesis of indole-3acetic -acid. Can. J. Microbiol. 42, 207–220.

    Article  PubMed  CAS  Google Scholar 

  • Pawlowski K and Bissling T 1996 Rhizohial and actinorhizal symbioses: what are the shared features? The Plant Cell 8, 1899–1913.

    PubMed  CAS  Google Scholar 

  • Pawlowski K, Twigg P, Dobritsa S, Guan C and Mullin B C 1997 A nodule-specific gene family from Abuts glutinosa encodes glycine and histidine-rich proteins expressed in the early stages of actinorhizal nodule development. Mol. Plant Microb. Interact. 10, 656–664.

    Google Scholar 

  • Pepin R and Boumendil J 1982 Préservation de l’ultrastructure de Selerotinia tuberose, (Hedw.) Fuckel (champignon Discomycète), un modèle pour la préparation des échantillons imperméables et hétérogènes. Cytologica 47, 359–377.

    Article  Google Scholar 

  • Phillips D A and Torrey C T 1972 Studies on cytokinin production by’ Rhizobium. Plant Physiol. 49, 11–15.

    Article  PubMed  CAS  Google Scholar 

  • Priesen E, Chauvaux N, Schmidt J, John M, Wieneck De Greef.1, Schell J and Van Onckclen H 1991 Stimulation of indole-acetic acid production in Rhicobia by flavonoids. FEBS Lett. 282, 5355.

    Google Scholar 

  • Ribeiro A, Akkermans A D, van Kammen A, Bisseling T and Pawlowski K 1995 A nodule-specific gene encoding a subtilisinlike protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7, 785–94.

    PubMed  CAS  Google Scholar 

  • Richardson K C, Jarret L and Finke E H 1960 Embedding in epoxy resins for ultratin sectionning for electron microscopy. Stain Technol 35 313–323.

    Google Scholar 

  • Rodriguez-Barrueco C and Bermudez de Castro F 1973 Cytokinininduced pseudonodules on Abuts glutinosa. Physiol. Plant. 29. 277–280.

    Article  CAS  Google Scholar 

  • Rosas S, Soria R, Correa N and Abdala G 1998 Jasmonic acid stimulates the expression of nod genes in Rhizobium. Plant Mol. Biol. 38, 1161–1168.

    Google Scholar 

  • Samar M. W T and Franckenberger J R 1995 Fate of t. phenylalanine in soil and its effect on plant growth. Soil Sei. Soc. Am. J. 59, 1625–1630.

    Google Scholar 

  • Schneider S. El-Said M and Fuchs G 1997 Anaerobic metabolism of L-phenylalaninc via benzoyl-CoA in the denitrifying bacterium Thanera aromatics. Arch Microbiol. 168, 310–320.

    Google Scholar 

  • Simonet P, Capetian() A, Navarro E, Bardin R and Moiroud A 1984 An improved method for lysis of Frankia with achromopeptidase allows detection of new plasmids. Can. J. Microbiol. 30, 12921295.

    Google Scholar 

  • Stafford H A and Lewis L L 1979 Conversion of L- and Dphenylalanine to phenylacetate via phenypyruvate in sorghum leaf extracts. Plant Physiol. 64, 176–181.

    Article  PubMed  CAS  Google Scholar 

  • Stevens G A J R and Berry A M 1988 Cytokinin secretion by Frankia sp. HFPAr13 in defined medium. Plant. Physiol. 87. 1516.

    Article  Google Scholar 

  • Swensen S M 1996 The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association. Am. J. Bot. 99, 565–573.

    Google Scholar 

  • Thompson J D, Gibson I. J, Plewniak F, Jeamnougin F and Higgins D G 1997 The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25, 4876–882.

    Google Scholar 

  • Vasse J, de Billy F and Truchet G 1993 Abortion of infection during the Rhizobium nreli/oti-alfalfa symbiotic interaction is accompagnicd by a hypersensitive reaction. Plant J. 4. 555–566.

    Article  Google Scholar 

  • Wheeler C T, Crozier A and Sandberg G 1984 The biosynthesis of indole-3–acetic acid by Frankia. Plant Soil. 78, 99–104.

    Article  CAS  Google Scholar 

  • Wightman F 1973 biosynthesis of auxins in tomato shoots. Biochem. Soc. Symp. 38, 247–275.

    Google Scholar 

  • Wightman F and Lighty DL 1982 Identification of phenylacetic acid as a natural auxin in the shoots of higher plants; Physiol. Plant. 55. 17–24.

    Article  CAS  Google Scholar 

  • Wisniewski J P, Rathbun E A, Knox J P and Brewin N J 2000 Involvement of Diamine Oxidase and peroxidase in insoluhilisation of the extracellular matrix: implications for pea nodule initiation by Rhizobium legrmrinosarum. Mol. Plant Microb. Interact. 13, 413–420.

    Google Scholar 

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Correspondence to Anne-Marie Domenach .

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P. Normand J. O. Dawson K. Pawlowski

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Hammad, Y. et al. (2003). A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia . In: Normand, P., Dawson, J.O., Pawlowski, K. (eds) Frankia Symbiosis. Developments in Plant and Soil Sciences, vol 100. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-1601-7_21

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  • DOI: https://doi.org/10.1007/978-94-017-1601-7_21

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