Activation of the isoflavonoid pathway in actinorhizal symbioses
Florence Auguy A , Khalid Abdel-Lateif A , Patrick Doumas A B , Pablo Badin A , Vanessa Guerin A , Didier Bogusz A and Valérie Hocher A C
+ Author Affiliations
- Author Affiliations
A Equipe Rhizogenèse, UMR DIADE (IRD, UM2), Institut de Recherche pour le Développement, 911 Avenue Agropolis, BP64501, 34 394 Montpellier Cedex 5, France.
B INRA, Département de Biologie Végétale, Centre de Recherche de Montpellier, 2 place Pierre Viala - Bât. 7, 34060 Montpellier, France.
C Corresponding author. Email: valerie.hocher@ird.fr
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) 690-696 https://doi.org/10.1071/FP11014
Submitted: 14 January 2011 Accepted: 11 April 2011 Published: 16 August 2011
Abstract
We investigated the involvement of flavonoids in the actinorhizal nodulation process resulting from the interaction between the tropical tree Casuarina glauca Sieb. ex Spreng. and the actinomycete Frankia. Eight C. glauca genes involved in flavonoid biosynthesis: chalcone synthase (CHS), chalcone isomerase (CHI), isoflavone reductase (IFR), flavonoid-3-hydroxylase (F3H), flavonoid 3′-hydroxylase (F3′H), flavonoid 3′,5′ hydroxylase (F3′5′H), dihydroflavonol 4-reductase (DFR) and flavonol synthase (FLS), were identified from a unigene database and gene expression patterns were monitored by quantitative real-time PCR (qRT–PCR) during the nodulation time course. Results showed that FLS and F3′5′H transcripts accumulated in mature nodules whereas CHI and IFR transcripts accumulated preferentially early after inoculation with Frankia. Comparison of IFR and CHI expression in inoculated plants and in control plants cultivated with or without nitrogen confirmed that early expression of IFR is specifically linked to symbiosis. Taken together, these data suggest for the first time that isoflavonoids are implicated in actinorhizal nodulation.
Additional keywords: actinorhiza, flavonoid, gene expression, isoflavonoid, nitrogen-fixing symbiosis.
References
Aoki T, Akashi T, Ayabe SI (2000) Flavonoids of leguminous plants: structure, biological activity and biosynthesis. Journal of Plant Research 113, 475–488.| Flavonoids of leguminous plants: structure, biological activity and biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Benoit LF, Berry AM (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 |
Buer SB, Imin N, Djordjevic A (2010) Flavonoids: new roles for old molecules. Journal of Integrative Plant Biology 52, 98–111.
| Flavonoids: new roles for old molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVOhsLc%3D&md5=899d2b6e144a46268364fa2872b2f9f1CAS |
Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294–5299.
| Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXisl2i&md5=82d80967cbf2f92a0fba46bae3da8714CAS |
Coronado C, Silviera Zuanazzi JA, Sallaud C, Quirion JC, Esnault R, Husson HP, Kondorosi A, Ratet P (1995) Alfalfa root flavonoid production is nitrogen regulated. Plant Physiology 108, 533–542.
Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. The Plant Cell 7, 1085–1097.
Franche C, Diouf D, Le QV, N’Diaye A, Gherbi H, Bogusz D, Gobé C, Duhoux E (1997) Genetic transformation of the actinorhizal tree Allocasuarina verticillata by Agrobacterium tumefaciens. The Plant Journal 11, 897–904.
| Genetic transformation of the actinorhizal tree Allocasuarina verticillata by Agrobacterium tumefaciens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1Cksr4%3D&md5=2b2ddd4972ebca5701b02d7826d8b102CAS |
Fritz C, Palacios-Rojas N, Feil R, Stitt M (2006) Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. The Plant Journal 46, 533–548.
| Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVGktrs%3D&md5=83ed3ceb1592eba94f249df4cb02c6a4CAS |
Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008a) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proceedings of the National Academy of Sciences of the United States of America 105, 4928–4932.
| SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktlSjsbo%3D&md5=3de9c59f7472f502b25ec523a87e7187CAS |
Gherbi H, Nambiar-Veetil M, Zhong C, Félix J, Autran D, Girardin R, Vaissayre V, Auguy F, Bogusz D, Franche C (2008b) Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata. Molecular Plant-Microbe Interactions 21, 518–524.
| Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltFSqs7c%3D&md5=787d53fbf6baab0d3ef5b2262ab9ea4cCAS |
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 |
Hocher V, Auguy F, Argout X, Laplaze L, Franche C, Bogusz D (2006) Expressed sequence tag analysis in Casuarina glauca actinorhizal nodule and root. New Phytologist 169, 681–688.
| Expressed sequence tag analysis in Casuarina glauca actinorhizal nodule and root.Crossref | GoogleScholarGoogle Scholar |
Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P, Normand P, Bogusz D (2011) Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiology
| Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade.Crossref | GoogleScholarGoogle Scholar |
Hughes M, Donnelly C, Crozier A, Wheeler CT (1999) Effect of the exposure of roots of Alnus glutinosa to light on flavonoïds and nodulation. American Journal of Botany 77, 1311–1315.
Kim HB, Bae JH, Lim JD, Yu CY, An CS (2007) Expression of a functional type-I chalcone isomerase gene is localized to the infected cells of root nodules of Elaeagnus umbellata. Molecules and Cells 23, 405–409.
Koes RE, Quattrocchio F, Mol JNM (1994) The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays 16, 123–132.
| The flavonoid biosynthetic pathway in plants: function and evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVGjsLs%3D&md5=279dea2142491e319e13e562ba986e6aCAS |
Laffont C, Blanchet S, Lapierre C, Brocard L, Ratet P, Crespi M, Mathesius U, Frugier F (2010) The Compact Root Architecture1 gene regulates lignification, flavonoid production and polar auxin transport in Medicago truncatula. Plant Physiology 153, 1597–1607.
| The Compact Root Architecture1 gene regulates lignification, flavonoid production and polar auxin transport in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVCrsr%2FN&md5=3c020f7e6b11e9d97b083e58bfdddfa9CAS |
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 |
Laplaze L, Duhoux E, Franche C, Frutz T, Svistoonoff S, Bisseling T, Bogusz D, Pawlowski K (2000) Casuarina glauca prenodule cells display the same differentiation as the corresponding nodule cells. Molecular Plant-Microbe Interactions 13, 107–112.
| Casuarina glauca prenodule cells display the same differentiation as the corresponding nodule cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislSgtA%3D%3D&md5=fb05afd0b423bc46f754eb439490e2c7CAS |
Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BE, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Research 17, 7–15.
| Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography.Crossref | GoogleScholarGoogle Scholar |
Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology 59, 519–546.
| Coordinating nodule morphogenesis with rhizobial infection in legumes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsbk%3D&md5=f7fe61ce411fe5f965ed6c1a4a292632CAS |
Pawlowski K (2009) Induction of actinorhizal nodules by Frankia. In ‘Microbiology monographs. Vol. 8’. (Ed. K Pawlowski) pp. 127–154. (Spinger-Verlag: Berlin)
Perrine-Walker F, Gherbi H, Imanishi L, Hocher V, Ghodhbane-Gtari F, Lavenus J, Nambiar-Veetil M, Svistoonoff S, Laplaze L (2011) Symbiotic signalling in actinorhizal symbioses. Current Protein & Peptide Science
| Symbiotic signalling in actinorhizal symbioses.Crossref | GoogleScholarGoogle Scholar |
Popovici J, Comte G, Bagnarol E, Alloisio N, Fournier P, Bellvert F, Bertrand C, Fernandez MP (2010) Rare specific flavonoids affect differentially compatible and incompatible strains in the Myrica gale–Frankia actinorhizal symbiosis. Applied and Environmental Microbiology 76, 2451–2460.
| Rare specific flavonoids affect differentially compatible and incompatible strains in the Myrica gale–Frankia actinorhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVSlsrw%3D&md5=407116670fa676072818646a38937a37CAS |
Schijlen EGWM, Ric de Vos CH, van Tunen AJ, Bovy AG (2004) Modification of flavonoid biosynthesis in crop plants. Phytochemistry 65, 2631–2648.
| Modification of flavonoid biosynthesis in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotF2hsro%3D&md5=d42f37c22fcdb687d02b38545523a9d2CAS |
Subramanian S, Graham MY, Yu O, Graham TL (2005) RNA interference of soybean isoflavone synthase genes leads to silencing in tissues distal to the transformation site and to enhanced susceptibility to Phytophthora sojae. Plant Physiology 137, 1345–1353.
| RNA interference of soybean isoflavone synthase genes leads to silencing in tissues distal to the transformation site and to enhanced susceptibility to Phytophthora sojae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslaqurc%3D&md5=a90b6a60d8970d9486734237a0fbe39aCAS |
Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium. The Plant Journal 48, 261–273.
| Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFGhsr3N&md5=e69a03d474ffdafb5b0a70121552f379CAS |
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 |
Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Current Opinion in Plant Biology 8, 317–323.
| Flavonoids as developmental regulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslKntrs%3D&md5=8753328786255bf5eac3e0e0aae87f88CAS |
Ververidis F, Trantas E, Douglas C, Vollmer G, Kretzschma G, Panopoulos N (2007) Biotechnology of flavonoids and other phenylpropanoid-derived natural products. Part I: Chemical diversity, impacts on plant biology and human health. Biotechnology Journal 2, 1214–1234.
| Biotechnology of flavonoids and other phenylpropanoid-derived natural products. Part I: Chemical diversity, impacts on plant biology and human health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSlu7rJ&md5=8241fbc975b58c38e7ad5c955e9abc92CAS |
Vessey JK, Pawlowski K, Bergman B (2005) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads. Plant and Soil 266, 205–230.
| Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads.Crossref | GoogleScholarGoogle Scholar |
Wasson AP, Pellerone AI, Mathesius U (2006) Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation in rhizobia. The Plant Cell 18, 1617–1629.
| Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation in rhizobia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvV2qt7s%3D&md5=6af33179481501833b81c221fa9e57adCAS |
Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126, 485–493.
| Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXks1Gnu74%3D&md5=bb0a62109c5bb07de8a3d586f46c637fCAS |
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 |
