Strain specificity in the Myricaceae–Frankia symbiosis is correlated to plant root phenolics
Jean Popovici A C , Vincent Walker A , Cédric Bertrand A B , Floriant Bellvert A , Maria P. Fernandez A and Gilles Comte A
+ Author Affiliations
- Author Affiliations
A Université de Lyon, F-69622, Lyon, France, Université Lyon1, Villeurbanne, CNRS, UMR5557, Ecologie Microbienne, 43, Boulevard du 11 novembre 1918, F-69622 Villeurbanne Cedex, France.
B Present address: Université de Perpignan, Laboratoire de Chimie des Biomolécules et de l’Environnement, F-66860, Perpignan, France.
C Corresponding author. Email: popojean@hotmail.com
This paper originates from a presentation at the 16th International Meeting on Frankia and Actinorhizal Plants, Oporto, Portugal, 5–8 September 2010.
Functional Plant Biology 38(9) 682-689 https://doi.org/10.1071/FP11144
Submitted: 24 June 2011 Accepted: 2 July 2011 Published: 16 August 2011
Abstract
Plant secondary metabolites play an important role in the interaction between plants and their environment. For example, mutualistic nitrogen-fixing symbioses typically involve phenolic-based recognition between host plants and bacteria. Although these mechanisms are well studied in the rhizobia–legume symbiosis, little is known about the role of plant phenolics in the symbiosis between actinorhizal plants and the actinobacterium Frankia. In this study, the responsiveness of two Myricaceae plant species, Myrica gale L. and Morella cerifera L., to Frankia inoculation was correlated with the plant–bacteria compatibility status. Two Frankia strains were inoculated: ACN14a, compatible with both M. gale and M. cerifera and Ea112, compatible only with M. cerifera. The effect of inoculation on root phenolic metabolism was evaluated by metabolic profiling based on high-performance liquid chromatography (HPLC) and principal component analysis (PCA). Our results revealed that: (i) both Frankia strains induced major modifications in root phenolic content of the two Myricaceae species and (ii) strain-dependant modifications of the phenolic contents were detected. The main plant compounds differentially affected by Frankia inoculation are phenols, flavonoids and hydroxycinnamic acids. This work provides evidence that during the initial phases of symbiotic interactions, Myricaceae plants adapt their secondary metabolism in accordance with the compatibility status of Frankia bacterial strains.
Additional keywords: metabolic profiling, phenolic metabolism, plant–bacteria interactions, symbiotic specificity.
References
Bennett N, Wallsgrove R (1994) Secondary metabolism in plant defense mechanisms. New Phytologist 127, 617–633.| Secondary metabolism in plant defense mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvFOisrg%3D&md5=c6428f875f62ac23965f3de97e880a45CAS |
Benoit L, Berry A (1997) Flavonoid like compounds from seeds of red alder (Alnus rubra) influence host nodulation by Frankia (Actinomycetales). Physiologia Plantarum 99, 588–593.
| Flavonoid like compounds from seeds of red alder (Alnus rubra) influence host nodulation by Frankia (Actinomycetales).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVahtrs%3D&md5=2431c4fdd9a54135f2db8d4c5cc8e6dbCAS |
Bolaños-Vásquez M, Werner D (1997) Effects of Rhizobium tropici, R. etli, and R. leguminosarum bv. phaseoli on nod gene-inducing flavonoids in root exudates of Phaseolus vulgaris. Molecular Plant-Microbe Interactions 10, 339–346.
| Effects of Rhizobium tropici, R. etli, and R. leguminosarum bv. phaseoli on nod gene-inducing flavonoids in root exudates of Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar |
Brechenmacher L, Lei Z, Libault M, Findley S, Sugawara M, Sadowsky MJ, Sumner LW, Stacey G (2010) Soybean metabolites regulated in root hairs in response to the symbiotic bacterium Bradyrhizobium japonicum. Plant Physiology 153, 1808–1822.
| Soybean metabolites regulated in root hairs in response to the symbiotic bacterium Bradyrhizobium japonicum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVCrsrzL&md5=eaf1fe0a076f62c22760f92c22f108deCAS |
Cooper J (2004) Multiple responses of rhizobia to flavonoids during legume root infection. Advances in Botanical Research 41, 1–62.
| Multiple responses of rhizobia to flavonoids during legume root infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVClsrs%3D&md5=2ecb3ea85de5ccc0cfc6f20fdb119418CAS |
Dakora F, Joseph C, Phillips D (1993) Alfalfa (Medicago sativa L.) root exudates contain isoflavonoids in the presence of Rhizobium meliloti. Plant Physiology 101, 819–824.
Estabrook E, Sengupta-Gopalan C (1991) Differential expression of phenylalanine ammonia-lyase and chalcone synthase during soybean nodule development. The Plant Cell Online 3, 299–308.
| Differential expression of phenylalanine ammonia-lyase and chalcone synthase during soybean nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1Grsbg%3D&md5=43abe68dc53467389a6aa02109750e6cCAS |
Fernandez M, Meugnier H, Grimont P, Bardin R (1989) Deoxyribonucleic acid relatedness among members of the genus Frankia. International Journal of Systematic and Evolutionary Microbiology 39, 424–429.
Gianinazzi-Pearson V, Sejalon-Delmas N, Genre A, Jeandroz S, Bonfante P (2007) Plants and arbuscular mycorrhizal fungi: cues and communication in the early steps of symbiotic interactions. Advances in Botanical Research 46, 181–219.
| Plants and arbuscular mycorrhizal fungi: cues and communication in the early steps of symbiotic interactions.Crossref | GoogleScholarGoogle Scholar |
Gould K, Lister C (2006) Flavonoid functions in plants. In ‘Flavonoids: chemistry, biochemistry and applications’. (Eds M Andersen, KR Markham) pp. 397–441. (Taylor and Francis Group: Boca Raton, FL, USA)
Hammad Y, Nalin R, Marechal J, Fiasson K, Pepin R, Berry AM, Normand P, Domenach AM (2003) A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia. Plant and Soil 254, 193–205.
| A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVKhur8%3D&md5=7595687247afe18add70ecc62f7d6683CAS |
Harrison M, Dixon R (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Molecular Plant-Microbe Interactions 6, 643–654.
| Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFalsbo%3D&md5=17a77a070d0b0beab6d929af5163fcd3CAS |
Harrison M, Dixon R (1994) Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. The Plant Journal 6, 9–20.
| Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsFWnsro%3D&md5=abb955bcef7079f05f8da4d47065439aCAS |
Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Molecular Biology 57, 155–171.
| Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtV2hu7Y%3D&md5=df9be3f6b4112aacc2be8ba1a40537ecCAS |
Hoagland D, Arnon D (1950) The water-culture method for growing plants without soil. Circular of the California Agricultural Experiment Station 347, 1–32.
Hughes M, Donnelly C, Crozier A, Wheeler C (1999) Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation. Botany 77, 1311–1315.
| Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFSgsrw%3D&md5=e5736c3bf02c9585e9323aec55cf9162CAS |
Huguet V, Gouy M, Normand P, Zimpfer J, Fernandez M (2005) Molecular phylogeny of Myricaceae: a reexamination of host–symbiont specificity. Molecular Phylogenetics and Evolution 34, 557–568.
| Molecular phylogeny of Myricaceae: a reexamination of host–symbiont specificity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXptlCiug%3D%3D&md5=5379a67dea1ea763c1d2902b085b3a55CAS |
Laplaze L, Gherbi H, Frutz T, Pawlowski K, Franche C, Macheix JJ, Auguy F, Bogusz D, Duhoux E (1999) Flavan-containing cells delimit Frankia-infected compartments in Casuarina glauca nodules. Plant Physiology 121, 113–122.
| Flavan-containing cells delimit Frankia-infected compartments in Casuarina glauca nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGlsLg%3D&md5=5b6afbbbeb32fef31bbdb3b676293ceeCAS |
Maggia L, Bousquet J (1994) Molecular phylogeny of the actinorhizal Hamamelidae and relationships with host promiscuity towards Frankia. Molecular Ecology 3, 459–467.
| Molecular phylogeny of the actinorhizal Hamamelidae and relationships with host promiscuity towards Frankia.Crossref | GoogleScholarGoogle Scholar |
Malterud KE (1992) C-methylated dihydrochalcones from Myrica gale fruit exudate. Acta Pharmaceutica Nordica 4, 65–68.
Metlen K, Aschehoug E, Callaway R (2009) Plant behavioural ecology: dynamic plasticity in secondary metabolites. Plant, Cell & Environment 32, 641–653.
| Plant behavioural ecology: dynamic plasticity in secondary metabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmslems7Y%3D&md5=c6bc9550d40e1d235bd5fd236f8d9f2bCAS |
Muller J (1981) Fossil pollen records of extant angiosperms. Botanical Review 47, 1–142.
| Fossil pollen records of extant angiosperms.Crossref | GoogleScholarGoogle Scholar |
Murry M, Fontaine M, Torrey J (1984) Growth kinetics and nitrogenase induction in Frankia sp. HFPArI 3 grown in batch culture. Plant and Soil 78, 61–78.
| Growth kinetics and nitrogenase induction in Frankia sp. HFPArI 3 grown in batch culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkt1Sgt7c%3D&md5=eb538079f008eb95a56b8465470e6f5bCAS |
Normand P, Lalonde M (1982) Evaluation of Frankia strains isolated from provenances of two Alnus species. Canadian Journal of Microbiology 28, 1133–1142.
| Evaluation of Frankia strains isolated from provenances of two Alnus species.Crossref | GoogleScholarGoogle Scholar |
Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra A (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. International Journal of Systematic Bacteriology 46, 1–9.
| Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xhtl2ls7s%3D&md5=7aed30ea383af928e8fa1e10844ff2bdCAS |
Pontais I, Treutter D, Paulin JP, Brisset MN (2008) Erwinia amylovora modifies phenolic profiles of susceptible and resistant apple through its type III secretion system. Physiologia Plantarum 132, 262–271.
| Erwinia amylovora modifies phenolic profiles of susceptible and resistant apple through its type III secretion system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlKmurg%3D&md5=c3d4771ddccc04eb056deac66838bd24CAS |
Popovici J, Bertrand C, Bagnarol E, Fernandez MP, Comte G (2008) Chemical composition of essential oil and headspace-solid microextracts from fruits of Myrica gale L. and antifungal activity. Natural Product Research 22, 1024–1032.
Popovici J, Comte G, Bagnarol E, Alloisio N, Fournier P, Bellvert F, Bertrand C, Fernandez MP (2010) Differential effects of rare specific flavonoids on compatible and incompatible strains in the Myrica gale–Frankia actinorhizal symbiosis. Applied and Environmental Microbiology 76, 2451–2460.
| Differential effects of rare specific flavonoids on compatible and incompatible strains in the Myrica gale–Frankia actinorhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVSlsrw%3D&md5=407116670fa676072818646a38937a37CAS |
Schliemann W, Ammer C, Strack D (2008) Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 69, 112–146.
| Metabolite profiling of mycorrhizal roots of Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVOks7rN&md5=7f26dfd2c27da17184301aad65d956eeCAS |
Spitaler R, Schlorhaufer P, Ellmerer E, Merfort I, Bortenschlager S, Stuppner H, Zidorn C (2006) Altitudinal variation of secondary metabolite profiles in flowering heads of Arnica montana cv. ARBO. Phytochemistry 67, 409–417.
| Altitudinal variation of secondary metabolite profiles in flowering heads of Arnica montana cv. ARBO.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvVagsg%3D%3D&md5=da1b8e5f0a6827f3bb7eb60865597341CAS |
Subramanian S, Stacey G, Yu O (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends in Plant Science 12, 282–285.
| Distinct, crucial roles of flavonoids during legume nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslWlu70%3D&md5=fc33516d219b33c2583b67ef7db3ba39CAS |
Swensen SM (1996) The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association. American Journal of Botany 83, 1503–1512.
| The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association.Crossref | GoogleScholarGoogle Scholar |
Tirillini B, Ricci A, Pintore G, Chessa M, Sighinolfi S (2006) Induction of hypericins in Hypericum perforatum in response to chromium. Fitoterapia 77, 164–170.
| Induction of hypericins in Hypericum perforatum in response to chromium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFWntbo%3D&md5=691d881e755487ae19d971134b6a24a4CAS |
Vasse J, Billy F, Truchet G (1993) Abortion of infection during the Rhizobium melilotióalfalfa symbiotic interaction is accompanied by a hypersensitive reaction. The Plant Journal 4, 555–566.
| Abortion of infection during the Rhizobium melilotióalfalfa symbiotic interaction is accompanied by a hypersensitive reaction.Crossref | GoogleScholarGoogle Scholar |
Walker V, Bertrand C, Bellvert F, Moënne-Loccoz Y, Bally R, Comte G (2011) Host plant secondary metabolite profiling shows a complex, strain-dependent response of maize to plant growth-promoting rhizobacteria of the genus Azospirillum. New Phytologist 189, 494–506.
| Host plant secondary metabolite profiling shows a complex, strain-dependent response of maize to plant growth-promoting rhizobacteria of the genus Azospirillum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlChtb8%3D&md5=dc8fbe4f29c0934c5da885f438403a9eCAS |
Wasson AP, Pellerone FI, Mathesius U (2006) Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. The Plant Cell Online 18, 1617–1629.
| Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvV2qt7s%3D&md5=6af33179481501833b81c221fa9e57adCAS |
Zhang J, Subramanian S, Stacey G, Yu O (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. The Plant Journal 57, 171–183.
| Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOiu7s%3D&md5=a40c685551467bf9d14f8c177cd385e0CAS |
Zobayed S, Afreen F, Kozai T (2007) Phytochemical and physiological changes in the leaves of St John’s wort plants under a water stress condition. Environmental and Experimental Botany 59, 109–116.
| Phytochemical and physiological changes in the leaves of St John’s wort plants under a water stress condition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Cqtb%2FN&md5=26def67e39b3a881cc501450aadc380dCAS |
