Silencing of the chalcone synthase gene in Casuarina glauca highlights the important role of flavonoids during nodulation

New Phytologist

Volumn 199, Issue 4, 2013, Pages 1012-1021

  Abdel Lateif, Khalid ^a   Vaissayre, Virginie ^a   Gherbi, Hassen ^a   Verries, Clotilde ^b   Meudec, Emmanuelle ^b   Perrine Walker, Francine ^a   Cheynier, Véronique ^b   Svistoonoff, Sergio ^a   Franche, Claudine ^a   Bogusz, Didier ^a   Hocher, Valérie ^a  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b SPO   (France)

Author keywords

Actinorhizal symbiosis; Casuarina glauca; Chalcone synthase; Endosymbiosis; Flavonoids; Frankia; RNA interference; Signaling

Indexed keywords

ACTINORHIZA; BACTERIUM; BIOACCUMULATION; ENDOSYMBIONT; ENZYME ACTIVITY; EVERGREEN TREE; FUNCTIONAL ROLE; GENE EXPRESSION; NODULATION; PHYTOCHEMISTRY; SECONDARY METABOLITE; SIGNALING;

BACTERIA (MICROORGANISMS); CASUARINA GLAUCA; FABACEAE; FRANKIA; PARASPONIA; RHIZOBIACEAE;

ACYLTRANSFERASE; CHALCONE SYNTHASE; FLAVANONE DERIVATIVE; FLAVONOID; NARINGENIN;

ACTINORHIZAL SYMBIOSIS; ARTICLE; CASUARINA GLAUCA; CYTOLOGY; ENDOSYMBIOSIS; ENZYMOLOGY; FAGACEAE; FRANKIA; GENE SILENCING; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; NODULATION; PHENOTYPE; PLANT GENE; PLANT ROOT; RNA INTERFERENCE; SIGNALING; TANDEM MASS SPECTROMETRY; TIME; TRANSGENIC PLANT;

ACTINORHIZAL SYMBIOSIS; CASUARINA GLAUCA; CHALCONE SYNTHASE; ENDOSYMBIOSIS; FLAVONOIDS; FRANKIA; RNA INTERFERENCE; SIGNALING;

ACYLTRANSFERASES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FAGACEAE; FLAVANONES; FLAVONOIDS; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GENES, PLANT; PHENOTYPE; PLANT ROOT NODULATION; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; TANDEM MASS SPECTROMETRY; TIME FACTORS;

EID: 84881240654     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12326     Document Type: Article

References (55)

1. Abdel-Lateif K, Bogusz D, Hocher V. 2012. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and frankia bacteria. Plant Signaling and Behavior 7: 636-641.
2. Auguy F, Abdel-Lateif K, Doumas P, Badin P, Guerin P, Bogusz D, Hocher V. 2011. Activation of the isoflavonoid pathway in actinorhizal symbioses. Functional Plant Biology 38: 690-696.
3. Beauchemin NJ, Furnholm T, Lavenus J, Svistoonoff S, Doumas P, Bogusz D, Laplaze L, Tisa LS. 2012. Casuarina root exudates alter the physiology, surface properties, and plant infectivity of Frankia sp. Strain CcI3. Applied and Environmental Microbiology 78: 575-580.
4. Bell CD, Soltis DE, Soltis PS. 2010. The age and diversification of the angiosperms re-revisited. American Journal of Botany 97: 1296-1303.
5. 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.
6. Boisson-Dernier A, Chabaud M, Garcia F, Becard G, Rosenberg C, Barker DG. 2001. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Molecular Plant-Microbe Interactions 14: 695-700.
7. Boot KJM, van Brussel AAN, Tak T, Spaink HP, Kijne JW. 1999. Lipo-chitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp. nigra roots. Molecular Plant-Microbe Interactions 12: 839-844.
8. Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK. 2001. Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiology 126: 524-535.
9. Cérémonie H, Debelle F, Fernandez MP. 1999. Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Canadian Journal of Botany 77: 1293-1301.
10. Dénarié J, Débellé F, Promé JC. 1996. Rhizobium lipochitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annual Review of Biochemistry 65: 503-535.
11. Doyle JJ. 1998. Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends in Plant Science 3: 473-478.
12. Doyle JJ. 2011. Phylogenetic perspectives on the origins of nodulation. Molecular Plant-Microbe Interaction 24: 1289-1295.
13. 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. Plant Journal 11: 897-904.
14. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C et al. 2008b. SymRK defines a common genetic basis for plant root endosymbioses with AM fungi, rhizobia and Frankia bacteria. Proceedings of the National Academy of Sciences, USA 105: 4928-4932.
15. Gherbi H, Nambiar-Veetil M, Zhong C, Félix J, Autran D, Girardin R, Vaissayre V, Auguy F, Bogusz D, Franche C. 2008a. Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata. Molecular Plant-Microbe Interaction 21: 518-524.
16. Gibson AH. 1963. Physical environment and symbiotic nitrogen fixation. I. The effect of root temperature on recently nodulated Trifolium subterraneum L. plants. Australian Journal of Biological Sciences 16: 28-42.
17. Gough C, Cullimore J. 2011. Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Molecular Plant-Microbe Interaction 24: 867-878.
18. Hassan S, Mathesius U. 2012. The role of flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant-microbe interactions. Journal of Experimental Botany 63: 3429-3444.
19. Helliwell C, Waterhouse P. 2003. Constructs and methods for high-throughput gene silencing in plants. Methods 30: 289-295.
20. Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P et al. 2011. Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiology 156: 700-711.
21. Hocher V, Auguy F, Argout X, Laplaze LT, Franche C, Bogusz D. 2006. Expressed sequence-tag analysis in Casuarina glauca actinorhizal nodule and root. New Phytologist 169: 681-688.
22. Hughes M, Donnelly C, Crozier A, Wheeler CT. 1999. Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation. Canadian Journal of Botany 77: 1311-1315.
23. 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 umbellatae. Molecules and Cells 23: 405-409.
24. Kim HB, Oh CJ, Lee H, An CS. 2003. A Type-A chalcone isomerase mRNA is highly expressed in the root nodules of Elaeagnus umbellatae. Journal of Plant Biology 46: 263-270.
25. Kumagai H, Kouchi H. 2003. Gene silencing by expression of hairpin RNA in Lotus japonicus roots and nodules. Molecular Plant-Microbe Interactions 16: 663-668.
26. Laplaze L, Gherbi H, Frutz T, Pawlowski K, Franche C, Macheix J-J, Auguy F, Bogusz D, Duhoux E. 1999. Flavan-containing cells delimit Frankia infected compartements in Casuarina glauca nodules. Plant Physiology 121: 113-122.
27. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J. 1990. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781-784.
28. Maillet F, Poinsot V, André O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A et al. 2011. Fungal lipochitooligo-saccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
29. Mané C, Souquet JM, Ollé D, Verriès C, Véran F, Mazerolles G, Cheynier V, Fulcrand H. 2007. Optimization of simultaneous flavanol, phenolic acid and anthocyanin extraction from grapes using an experimental design; application to the characterization of Champagne grape varieties. Journal of Agricultural and Food Chemistry 55: 7224-7233.
30. Markmann K, Giczey G, Parniske M. 2008. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biology 6: e68.
31. Mathesius U, Schlaman HRM, Spaink H, Sautter C, Rolfe BG, Djordjevic MA. 1998. Auxin transport inhibition preceded root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant Journal 14: 23-34.
32. Meilhoc E, Cam Y, Skapski A, Bruand C. 2010. The response to nitric oxide of the nitrogen-fixing symbiont Sinorhizobium meliloti. Molecular Plant-Microbe Interaction 6: 748-759.
33. Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N et al. 2007a. Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Research 17: 7-15.
34. Normand P, Queiroux C, Tisa LS, Benson DR, Rouyd Z, Cruveiller S, Medigue C. 2007b. Exploring the genomes of Frankia. Physiologia Plantarum 130: 331-343.
35. Olle D, Guiraud JL, Souquet JM, Terrier N, Ageorges A, Cheynier V, Verries C. 2011. Effect of pre- and post-veraison water deficit on proanthocyanidin and anthocyanin accumulation during Shiraz berry development. Australian Journal of Grape and Wine Research 17: 90-100.
36. Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6: 763-775.
37. Pawlowski K, Bisseling T. 1996. Rhizobial and actinorhizal symbioses: what are the shared features? The Plant Cell 8: 1899-1913.
38. Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS. 2001. Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. Plant Physiology 126: 536-548.
39. Péret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, Franche C, Bogusz D et al. 2007. Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiology 144: 1852-1862.
40. 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. Applied and Environmental Microbiology 76: 2451-2460.
41. Prin Y, Rougier M. 1987. Preinfection events in the establishment of Alnus-Frankia symbiosis: study of the root hair deformation step. Plant Physiology 6: 99-106.
42. Saleh NAM, El-Lakany M. 1979. A quantitative variation in the flavonoids and phenolics of some Casuarina species. Biochemical Systematics and Ecology 7: 13-15.
43. Santi C, Svistoonoff S, Constans L, Auguy F, Duhoux E, Bogusz D, Franche C. 2003. Choosing a reporter for gene expression studies in transgenic actinorhizal plants of the Casuarinaceae family. Plant and Soil 254: 229-237.
44. Schüssler A, Schwarzott D, Walker C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105: 1413-1421.
45. Sheahan JJ, Rechnitz GA. 1992. Flavonoid-specific staining of Arabidopsis thaliana. BioTechniques 13: 880-883.
46. Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG. 1995. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences, USA 92: 2647-2651.
47. Souquet JM, Mazauric JP, Meudec E, Preys S, Morel-Salmi C, Cheynier V. 2004. Comparison of different methods of depolymerization for the characterization and quantification of proanthocyanidins in grape seed, grape skin and wine. In: Hiokkala A, Soidinsal O, Wahala K, eds. XXIInd International Conference on Polyphenols. Helsinki, Finland, 693-694.
48. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint J-P, Vierheilig H. 2007. Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12: 1290-1306.
49. Svistoonoff S, Gherbi H, Nambiar-Veetil M, Zhong C, Michalak Z, Laplaze L, Vaissayre V, Auguy F, Hocher V, Doumas P et al. 2010. Contribution of transgenic Casuarinaceae to our knowledge of the actinorhizal symbioses. Symbiosis 1: 3-11.
50. Svistoonoff S, Laplaze L, Auguy F, Runions J, Duponnois R, Haseloff J, Franche C, Bogusz D. 2003. Cg12 expression is specifically linked to infection of root hairs and cortical cells during Casuarina glauca and Allocasuarina verticillata actinorhizal nodule development. Molecular Plant-Microbe Interaction 16: 600-607.
51. Van Ghelue M, Lovaas E, Ringo E, Solheim B. 1997. Early interactions between Alnus glutinosa and Frankia strain Ari3: production and specificity of root hair deformation factor. Physiologia Plantarum 99: 579-587.
52. Verries C, Guiraud JL, Souquet JM, Vialet S, Terrier N, Ollé D. 2008. Validation of an extraction method on whole pericarp of grape berry (Vitis vinifera L. cv. Shiraz) to study biochemical and molecular aspects of flavan-3-ol synthesis during berry development. Journal of Agricultural and Food Chemistry 56: 5896-5904.
53. 2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads. Plant and Soil 274: 51-78.
54. Wasson P, Flavia I, Mathesius U. 2006. Silencing the flavonoids pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by Rhizobia. The Plant Cell 18: 1617-1629.
55. Zhang JH, Subramanian S, Stacey G, Yu O. 2009. Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant Journal 57: 171-183.