The role of flavonoids in root-rhizosphere signalling: Opportunities and challenges for improving plant-microbe interactions

Journal of Experimental Botany

Volumn 63, Issue 9, 2012, Pages 3429-3444

  Hassan, Samira ^a   Mathesius, Ulrike ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Flavonoids; Mycorrhizae; Nodulation; Rhizosphere

Indexed keywords

FLAVONOID;

BACTERIUM; METABOLISM; MICROBIOLOGY; PLANT; PLANT ROOT; REVIEW; RHIZOSPHERE; SIGNAL TRANSDUCTION;

BACTERIA; FLAVONOIDS; PLANT ROOTS; PLANTS; RHIZOSPHERE; SIGNAL TRANSDUCTION;

EID: 84861905473     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err430     Document Type: Review

References (173)

1. Aguilar JMM, Ashby AM, Richards AJM, Loake GJ, Watson MD, Shaw CH. 1988. Chemotaxis of Rhizobium leguminosarum biovar phaseoli towards flavonoid inducers of the symbiotic nodulation genes. Journal of General Microbiology 134, 2741-2746.
2. Akiyama K, Matsuoka H, Hayashi H. 2002. Isolation and identification of a phosphate deficiency-induced C-glycosylflavonoid that stimulates arbuscular mycorrhiza formation in melon roots. Molecular Plant-Microbe Interactions 15, 334-340.
3. Akiyama K, Tanigawa F, Kashihara T, Hayashi H. 2010. Lupin pyranoisoflavones inhibiting hyphal development in arbuscular mycorrhizal fungi. Phytochemistry 71, 1865-1871.
4. Alford ER, Vivanco JM, Paschke MW. 2009. The effects of flavonoid allelochemicals from knapweeds on legume-rhizobia candidates for restoration. Restoration Ecology 17, 506-514.
5. Antunes PM, Rajcan I, Goss MJ. 2006. Specific flavonoids as interconnecting signals in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium japonicum (Kirchner) Jordan and soybean (Glycine max (L.) Merr.). Soil Biology and Biochemistry 38, 533-543.
6. Aoki T, Akashi T, Ayabe S. 2000. Flavonoids of leguminous plants: structure, biological activity, and biosynthesis. Journal of Plant Research 113, 475-488.
7. Armero J, Requejo R, Jorrin J, Lopez-Valbuena R, Tena M. 2001. Release of phytoalexins and related isoflavonoids from intact chickpea seedlings elicited with reduced glutathione at root level. Plant Physiology and Biochemistry 39, 785-795.
8. Badri DV, Loyola-Vargas VM, Broeckling CD, et al. 2008. Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiology 146, 762-771.
9. Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM. 2009. An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiology 151, 2006-2017.
10. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM. 2003. Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301, 1377-1380.
11. Becard G, Taylor LP, Douds DD, Pfeffer PE, Doner LW. 1995. Flavonoids are not necessary plant signal compounds in arbuscular mycorrhizal symbioses. Molecular Plant-Microbe Interactions 8, 252-258.
12. Begum AA, Leibovitch S, Migner P, Zhang F. 2001. Specific flavonoids induced nod gene expression and pre-activated nod genes of Rhizobium leguminosarum increased pea (Pisum sativum L.) and lentil (Lens culinaris L.) nodulation in controlled growth chamber environments. Journal of Experimental Botany 52, 1537-1543.
13. 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.
14. Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M. 2007. Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. The Plant Cell 19, 148-162.
15. Blair AC, Hanson BD, Brunk GR, Marrs RA, Westra P, Nissen SJ, Hufbauer RA. 2005. New techniques and findings in the study of a candidate allelochemical implicated in invasion success. Ecology Letters 8, 1039-1047.
16. Blount JW, Dixon RA, Paiva NL. 1992. Stress responses in alfalfa (Medicago sativa L). Antifungal activity of medicarpin and its biosynthetic precursors-implications for the genetic manipulation of stress metabolites. Physiological and Molecular Plant Pathology 41, 333-349.
17. Bodini SF, Manfredini S, Epp M, Valentini S, Santori F. 2009. Quorum sensing inhibition activity of garlic extract and p-coumaric acid. Letters in Applied Microbiology 49, 551-555.
18. Bolanos-Vasquez MC, Warner D. 1997. Effects of Rhizobium tropici, R. etli, and R. leguminosarum bv phaseoli on nod geneinducing flavonoids in root exudates of Phaseolus vulgaris. Molecular Plant-Microbe Interactions 10, 339-346.
19. Boot KJM, van Brussel AAN, Tak T, Spaink HP, Kijne JW. 1999. Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp nigra roots. Molecular Plant-Microbe Interactions 12, 839-844.
20. Borowicz VA. 2001. Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82, 3057-3068.
21. 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.
22. Buer CS, Djordjevic MA. 2009. Architectural phenotypes in the transparent testa mutants of Arabidopsis thaliana. Journal of Experimental Botany 60, 751-763.
23. Buer CS, Muday GK. 2004. The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. The Plant Cell 16, 1191-1205.
24. Buer CS, Muday GK, Djordjevic MA. 2007. Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiology 145, 478-490.
25. Butelli E, Titta L, Giorgio M, et al. 2008. Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nature Biotechnology 26, 1301-1308.
26. Carlsen SCK, Understrup A, Fomsgaard IS, Mortensen AG, Ravnskov S. 2008. Flavonoids in roots of white clover: interaction of arbuscular mycorrhizal fungi and a pathogenic fungus. Plant and Soil 302, 33-43.
27. Catford JG, Staehelin C, Larose G, Piche Y, Vierheilig H. 2006. Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant and Soil 285, 257-266.
28. Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L. 2010. Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant and Soil 329, 1-25.
29. Cooper JE. 2004. Multiple responses of rhizobia to flavonoids during legume root infection. Advances in Botanical Research 41, 1-62.
30. Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V. 1998. Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Molecular Plant-Microbe Interactions 11, 1017-1028.
31. Coronado C, Zuanazzi JAS, Sallaud C, Quirion JC, Esnault R, Husson HP, Kondorosi A, Ratet P. 1995. Medicago sativa root flavonoid production is nitrogen regulated. Plant Physiology 108, 533-542.
32. Curir P, Dolci M, Galeotti F. 2005. A phytoalexin-like flavonol involved in the carnation (Dianthus caryophyllus)-Fusarium oxysporum f. sp dianthi pathosystem. Journal of Phytopathology 153, 65-67.
33. Cushnie TPT, Lamb AJ. 2011. Recent advances in understanding the antibacterial properties of flavonoids. International Journal of Antimicrobial Agents 38, 99-107.
34. Dakora FD. 1995. Plant flavonoids-biological molecules for useful exploitation. Australian Journal of Plant Physiology 22, 87-99.
35. Dakora FD, Joseph CM, Phillips DA. 1993. Common bean root exudates contain elevated levels of daidzein and coumestrol in response to Rhizobium inoculation. Molecular Plant-Microbe Interactions 6, 665-668.
36. Dehne HW, Schonbeck F. 1979. Influence of endotrophic mycorrhiza on plant-diseases. 2. Phenol metabolism and lignification. Phytopathologische Zeitschrift-Journal of Phytopathology 95, 210-216.
37. Denny TP, Vanetten HD. 1981. Tolerance by Nectria haematococca MP-VI of the chickpea (Cicer arietinum) phytoalexins medicarpin and maackiain. Physiological Plant Pathology 19, 419-437.
38. Denny TP, Vanetten HD. 1982. Metabolism of the phytoalexins medicarpin and maackiain by Fusarium solani. Phytochemistry 21, 1023-1028.
39. Dharmatilake AJ, Bauer WD. 1992. Chemotaxis of Rhizobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Applied and Environmental Microbiology 58, 1153-1158.
40. Dixon RA, Paiva NL. 1995. Stress-induced phenylpropanoid metabolism. The Plant Cell 7, 1085-1097.
41. Dixon RA, Steele CL. 1999. Flavonoids and isoflavonoids-a gold mine for metabolic engineering. Trends in Plant Science 4, 394-400.
42. Du H, Huang YB, Tang YX. 2010. Genetic and metabolic engineering of isoflavonoid biosynthesis. Applied Microbiology and Biotechnology 86, 1293-1312.
43. Duke SO, Blair AC, Dayan FE, Johnson RD, Meepagala KM, Cook D, Bajsa J. 2009. Is (-)-catechin a novel weapon of spotted knapweed (Centaurea stoebe)? Journal of Chemical Ecology 35, 141-153.
44. Dunn MF, Pueppke SG, Krishnan HB. 1992. The nod gene inducer genistein alters the composition and molecular mass-distribution of extracellular polysaccharides produced by Rhizobium fredii USDA 193. FEMS Microbiology Letters 97, 107-112.
45. Erlejman AG, Verstraeten SV, Fraga CG, Oteiza PI. 2004. The interaction of flavonoids with membranes: potential determinant of flavonoid antioxidant effects. Free Radical Research 38, 1311-1320.
46. Ferrer JL, Austin MB, Stewart C, Noe JP. 2008. Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant Physiology and Biochemistry 46, 356-370.
47. Fowler ZL, Koffas MAG. 2009. Biosynthesis and biotechnological production of flavanones: current state and perspectives. Applied Micriobiology and Biotechnology 83, 799-808.
48. Friederich S, Rueffer M, Asakawa Y, Zenk MH. 1999. Cytochromes P-450 catalyze the formation of marchantins A and C in Marchantia polymorpha. Phytochemistry 52, 1195-1202.
49. Fuqua C, Parsek MR, Greenberg EP. 2001. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annual Review of Genetics 35, 439-468.
50. Fuqua WC, Winans SC, Greenberg EP. 1994. Quorum sensing in bacteria-the luxR-LuxI family of cell density-responsive transcriptional regulators. Journal of Bacteriology 176, 269-275.
51. Gao MS, Teplitski M, Robinson JB, Bauer WD. 2003. Production of substances by Medicago truncatula that affect bacterial quorum sensing. Molecular Plant-Microbe Interactions 16, 827-834.
52. Gheysen G, Mitchum MG. 2011. How nematodes manipulate plant development pathways for infection. Current Opinion in Plant Biology 14, 415-421.
53. Gonzalez JE, Marketon MM. 2003. Quorum sensing in nitrogenfixing rhizobia. Microbiology and Molecular Biology Reviews 67, 574-592.
54. Goodman CD, Casati P, Walbot V. 2004. A multidrug resistanceassociated protein involved in anthocyanin transport in Zea maiys. The Plant Cell 16, 1812-1826.
55. Goverse A, Engler JD, Verhees J, van der Krol S, Helder J, Gheysen G. 2000. Cell cycle activation by plant parasitic nematodes. Plant Molecular Biology 43, 747-761.
56. Graham TL. 1991. Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiology 95, 594-603.
57. Graham TL, Graham MY, Subramanian S, Yu O. 2007. RNAi silencing of genes for elicitation or biosynthesis of 5-deoxyisoflavonoids suppresses race-specific resistance and hypersensitive cell death in Pytophthora sojae infected tissues. Plant Physiology 144, 728-740.
58. Gressel J, Hanafi A, Head G, Marasas W, Obilana B, Ochanda J, Souissi T, Tzotzos G. 2004. Major heretofore intractable biotic constraints to African food security that may be amenable to novel biotechnological solutions. Crop Protection 23, 661-689.
59. Grotewold E. 2008. Transcription factors for predictive plant metabolic engineering: are we there yet? Current Opinion in Biotechnology 19, 138-144.
60. Grunewald W, van Noorden G, van Isterdael G, Beeckman T, Gheysen G, Mathesius U. 2009. Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. The Plant Cell 21, 2553-2562.
61. Guerreiro N, Redmond JW, Rolfe BG, Djordjevic MA. 1997. New Rhizobium leguminosarum flavonoid-induced proteins revealed by proteome analysis of differentially displayed proteins. Molecular Plant-Microbe Interactions 4, 506-516.
62. Hain R, Reif HJ, Krause E, et al. 1993. Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361, 153-156.
63. Harrison MJ. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology 59, 19-42.
64. Harrison MJ, Dixon RA. 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.
65. Harrison MJ, Dixon RA. 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.
66. Hartwig UA, Phillips DA. 1991. Release and modification of nod gene-inducing flavonoids from alfalfa seeds. Plant Physiology 95, 804-807.
67. Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Z. 1998. Function of root border cells in plant health: pioneers in the rhizosphere. Annual Review of Phytopathology 36, 311-327.
68. Heath MC. 2000. Hypersensitive response-related death. Plant Molecular Biology 44, 321-334.
69. Herná ndez I, Alegre L, Van Breusegem F, Munné-Bosch S, 2009, How relevant are flavonoids as antioxidants in plants? Trends in Plant Science, 14, 125-132.
70. Higgins VJ. 1978. The effect of some pterocarpanoid phytoalexins on germ tube elongation of Stemphylium botryosum. Phytopathology 68, 339-345.
71. Hooper AM, Hassanali A, Chamberlain K, Khan Z, Pickett JA. 2009. New genetic opportunities from legume intercrops for controlling Striga spp. parasitic weeds. Pest Management Science 65, 546-552.
72. Hooper AM, Tsanuo MK, Chamberlain K, Tittcomb K, Scholes J, Hassanali A, Khan ZR, Pickett JA. 2010. Isoschaftoside, a C-glycosylflavonoid from Desmodium uncinatum root exudate, is an allelochemical against the development of Striga. Phytochemistry 71, 904-908.
73. Hutangura P, Mathesius U, Jones MGK, Rolfe BG. 1999. Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway. Australian Journal of Plant Physiology 26, 221-231.
74. Hutzler P, Fischbach R, Heller W, Jungblut TP, Reuber S, Schmitz R, Veit M, Weissenboeck G, Schnitzler JP. 1998. Tissue localisation of phenolic compounds in plants by confocal laser scanning microscopy. Journal of Experimental Botany 49, 953-965.
75. Jez JM, Bowman ME, Noel JP. 2002. Expanding the biosynthetic repertoire of plant type III polyketide synthases by altering starter molecule specificity. Proceedings of the National Academy of Sciences, USA 99, 5319-5324.
76. Jia ZH, Zou BH, Wang XM, Qiu JA, Ma H, Gou ZH, Song SS, Dong HS. 2010. Quercetin-induced H2O2 mediates the pathogen resistance against Pseudomonas syringae pv. Tomato DC3000 in Arabidopsis thaliana. Biochemical and Biophysical Research Communications 396, 522-527.
77. Jimenez-Gonzalez L, Alvarez-Corral M, M. M-D, Rodriguez-Garcia I. 2008. Pterocarpans: interesting natural products with antifungal activity and other biological properties. Phytochemical Reviews 7, 125-154.
78. Jones JT, Furlanetto C, Phillips MS. 2007. The role of flavonoids produced in response to cyst nematode infection of Arabidopsis thaliana. Nematology 9, 671-677.
79. Jorgensen K, Rasmussen AV, Morant M, Nielsen AH, Bjarnholt N, Zagrobelny M, Bak S, Moller BL. 2005. Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Current Opinion in Plant Biology 8, 280-291.
80. Juszczuk IM, Wiktorowska A, Malusa E, Rychter AM. 2004. Changes in the concentration of phenolic compounds and exudation induced by phosphate deficiency in bean plants (Phaseolus vulgaris L.). Plant and Soil 267, 41-49.
81. Kapulnik Y, Guenoune D, Galili S, Phillips DA, Volpin H, Chet I, Okon Y. 2001. The defense response elicited by the pathogen Rhizoctonia solani is suppressed by colonization of the AM-fungus Glomus intraradices. Plant Science 160, 925-932.
82. Khan ZR, Midega CAO, Bruce TJA, Hooper AM, Pickett JA. 2010. Exploiting phytochemicals for developing a 'push-pull' crop protection strategy for cereal farmers in Africa. Journal of Experimental Botany 61, 4185-4196.
83. Khan ZR, Pickett JA, Wadhams LJ, Hassanali A, Midega CAO. 2006. Combined control of Striga hermonthica and stemborers by maize-Desmodium spp. intercrops. Crop Protection 25, 989-995.
84. Kikuchi K, Matsushita N, Suzuki K, Hogetsu T. 2007. Flavonoids induce germination of basidiospores of the ectomycorrhizal fungus Suillus bovinus. Mycorrhiza 17, 563-570.
85. Koes R, Verweij W, Quattrocchio F. 2005. Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends in Plant Science 10, 236-242.
86. Kosslak RM, Bookland R, Barkei J, Paaren HE, Appelbaum ER. 1987. Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proceedings of the National Academy of Sciences, USA 84, 7428-7432.
87. Krishnan HB, Lorio J, Kim WS, Jiang GQ, Kim KY, DeBoer M, Pueppke SG. 2003. Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like surface appendages and exported by a type III protein secretion system in Sinorhizobium fredii USDA257. Molecular Plant-Microbe Interactions 16, 617-625.
88. 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.
89. Laplaze L, Gherbi H, Frutz T, Pawlowski K, Franche C, Macheix JJ, Auguy F, Bogusz D, Duhoux E. 1999. Flavancontaining cells delimit Frankia-infected compartments in Casuarina glauca nodules. Plant Physiology 121, 113-122.
90. Larose G, Chenevert R, Moutoglis P, Gagne S, Piche Y, Vierheilig H. 2002. Flavonoid levels in roots of Medicago sativa are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. Journal of Plant Physiology 159, 1329-1339.
91. Lattanzio V, Lattanzio VMT, Cardinali A. 2006. Role of phenolics in the resistance mechanism of plants against fungal pathogens and insects. In: Imperato F, ed. Phytochemistry: advances in research. Trivandrum, Kerala, India: Research Signpost, 23-67.
92. Li FQ, Hou BH, Chen L, Yao ZJ, Hong GF. 2008. In vitro observation of the molecular interaction between NodD and its inducer naringenin as monitored by fluorescence resonance energy transfer. Acta Biochimica et Biophysica Sinica 40, 783-789.
93. Li X, Bonawitz ND, Weng J-K, Chapple C. 2010. The growth reduction associated with repressed lignin biosynthesis in Arabidopsis thaliana is independent of flavonoids. The Plant Cell 22, 1620-1632.
94. Liu CJ, Blount JW, Steele CL, Dixon RA. 2002. Bottlenecks for metabolic engineering of isoflavone glycoconjugates in Arabidopsis. Proceedings of the National Academy of Sciences, USA 99, 14578-14583.
95. Liu CJ, Deavours BE, Richard SB, Ferrer JL, Blount JW, Huhman D, Dixon RA, Noel JP. 2006. Structural basis for dual functionality of isoflavonoid O-methyltransferases in the evolution of plant defense responses. The Plant Cell 18, 3656-3669.
96. Makoi JHJR, Ndakidemi PA. 2007. Biological, ecological and agronomic significance of plant phenolic compounds in rhizosphere of the symbiotic legumes. African Journal of Biotechnology 6, 1358-1368.
97. Manefield M, de Nys R, Kumar N, Read R, Givskov M, Steinberg P, Kjelleberg SA. 1999. Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145, 283-291.
98. Marrs KA, Alfenito MR, Lloyd AM, Walbot V. 1995. A glutathione-S- transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375, 397-400.
99. Masaoka Y, Kojima M, Sugihara S, Yoshihara T, Koshino M, Ichihara A. 1993. Dissolution of ferric phosphates by alfalfa (Medicago sativa L.) root exudates. Plant and Soil 155, 75-78.
100. Mathesius U. 2001. Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. Journal of Experimental Botany 52, 419-426.
101. Mathesius U, Bayliss C, Weinman JJ, Schlaman HRM, Spaink HP, Rolfe BG, McCully ME, Djordjevic MA. 1998a. Flavonoids synthesized in cortical cells during nodule initiation are early developmental markers in white clover. Molecular Plant-Microbe Interactions 11, 1223-1232.
102. Mathesius U, Mulders S, Gao MS, Teplitski M, Caetano-Anolles G, Rolfe BG, Bauer WD. 2003. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proceedings of the National Academy of Sciences, USA 100, 1444-1449.
103. Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA. 1998b. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. The Plant Journal 14, 23-34.
104. Mohney BK, Matz T, LaMoreaux J, Wilcox DS, Gimsing AL, Mayer P, Weidenhamer JD. 2009. In situ silicone tube microextraction: a new method for undisturbed sampling of root-exuded thiophenes from marigold (Tagetes erecta L.) in soil. Journal of Chemical Ecology 35, 1279-1287.
105. Morandi D. 1996. Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant and Soil 185, 241-251.
106. Morandi D, Bailey JA, Gianinazzipearson V. 1984. Isoflavonoid accumulation in soybean roots infected with vesicular arbuscular mycorrhizal fungi. Physiological Plant Pathology 24, 357-364.
107. Morandi D, le Signor C, Gianinazzi-Pearson V, Duc G. 2009. A Medicago truncatula mutant hyper-responsive to mycorrhiza and defective for nodulation. Mycorrhiza 19, 435-441.
108. Morris PF, Bone E, Tyler BM. 1998. Chemotropic and contact responses of Phytophthora sojae hyphae to soybean isoflavonoids and artificial substrates. Plant Physiology 117, 1171-1178.
109. Moscatiello R, Squartini A, Mariani P, Navazio L. 2010. Flavonoid-induced calcium signalling in Rhizobium leguminosarum bv. viciae. New Phytologist 188, 814-823.
110. Mueller LA, Goodman CD, Silady RA, Walbot V. 2000. AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid binding protein. Plant Physiology 123, 1561-1570.
111. Naoumkina M, Dixon RA. 2008. Subcellular localization of flavonoid natural products: a signalling function? Plant Signaling and Behaviour 3, 573-575.
112. Naoumkina MA, Zhao QA, Gallego-Giraldo L, Dai XB, Zhao PX, Dixon RA. 2010. Genome-wide analysis of phenylpropanoid defence pathways. Molecular Plant Pathology 11, 829-846.
113. Normand P, Lapierre P, Tisa LS, et al. 2007. Genome characteristics of facultatively symbiotic Frankia sp strains reflect host range and host plant biogeography. Genome Research 17, 7-15.
114. Novak K, Chovanec P, Skrdleta V, Kropacova M, Lisa L, Nemcova M. 2002. Effect of exogenous flavonoids on nodulation of pea (Pisum sativum L.). Journal of Experimental Botany 53, 1735-1745.
115. Padmavati M, Sakthivel N, Thara KV, Reddy AR. 1997. Differential sensitivity of rice pathogens to growth inhibition by flavonoids. Phytochemistry 46, 499-502.
116. Pankhurst CE, Biggs DR. 1980. Sensitivity of Rhizobium to selected isoflavonoids. Canadian Journal of Microbiology 26, 542-545.
117. Parniske M, Ahlborn B, Werner D. 1991. Isoflavonoid-inducible resistance to the phytoalexin glyceollin in soybean rhizobia. Journal of Bacteriology 173, 3432-3439.
118. Parvez MM, Tomita-Yokotani K, Fujii Y, Konishi T, Iwashina T. 2004. Effects of quercetin and its seven derivatives on the growth of Arabidopsis thaliana and Neurospora crassa. Biochemical Systematics and Ecology 32, 631-635.
119. Peck MC, Fisher RF, Long SR. 2006. Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. Journal of Bacteriology 188, 5417-5427.
120. Pedras MSC, Ahiahonu PWK. 2005. Metabolism and detoxification of phytoalexins and analogs by phytopathogenic fungi. Phytochemistry 66, 391-411.
121. Perez-Montano F, Guasch-Vidal B, Gonzalez-Barroso S, Lopez-Baena FJ, Cubo T, Ollero FJ, Gil-Serrano AM, Rodriguez-Carvajal MA, Bellogin RA, Espuny MR. 2011. Nodulation-geneinducing flavonoids increase overall production of autoinducers and expression of N-acyl homoserine lactone synthesis genes in rhizobia. Research in Microbiology 162, 715-723.
122. Peters NK, Frost JW, Long SR. 1986. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233, 977-980.
123. Plaper A, Golob M, Hafner I, Oblak M, Solmajer T, Jerala R. 2003. Characterization of quercetin binding site on DNA gyrase. Biochemical and Biophysical Research Communications 306, 530-536.
124. 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.
125. Pueppke SG, Vanetten HD. 1974. Pisatin accumulation and lesion development in peas infected with Aphanomyces euteiches, Fusarium solani f. sp. pisi, or Rhizoctonia solani. Phytopathology 64, 1433-1440.
126. Quattrocchio F, Baudry A, Lepiniec L, Gotewold E. 2006. The regulation of flavonoid biosynthesis. In: Grotewold E, ed. The science of flavonoids. Columbus, OH: The Ohio State University, 97-122.
127. Rajamani S, Bauer WD, Robinson JB, Farrow JM, Pesci EC, Teplitski M, Gao MS, Sayre RT, Phillips DA. 2008. The vitamin riboflavin and its derivative lumichrome activate the LasR bacterial quorum-sensing receptor. Molecular Plant-Microbe Interactions 21, 1184-1192.
128. Rao JR, Cooper JE. 1994. Rhizobia catabolize nod gene-inducing flavonoids via C-ring fission mechanisms. Journal of Bacteriology 176, 5409-5413.
129. Rao JR, Cooper JE. 1995. Soybean nodulating rhizobia modify nod gene inducers daidzein and genistein to yield aromatic products that can influence gene-inducing activity. Molecular Plant-Microbe Interactions 8, 855-862.
130. Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG. 1986. Flavones induce expression of nodulation genes in Rhizobium. Nature 323, 632-635.
131. Ringli C, Bigler L, Kuhn BM, Leiber RM, Diet A, Santelia D, Frey B, Pollmann S, Klein M. 2008. The modified flavonol glycosylation profile in the Arabidopsis rol1 mutants results in alterations in plant growth and cell shape formation. The Plant Cell 20, 1470-1481.
132. Saslowsky DE, Warek U, Winkel BSJ. 2005. Nuclear localization of flavonoid enzymes in Arabidopsis. Journal of Biological Chemistry 280, 23735-23740.
133. Savouré A, Sallaud C, El-Turk J, Zuanazzi J, Ratet P, Schultze M, Kondorosi A, Esnault R, Kondorosi E. 1997. Distinct response of Medicago suspension cultures and roots to Nod factors and chitin oligomers in the elicitation of defense-related responses. The Plant Journal 11, 277-287.
134. Scervino JM, Ponce MA, Erra-Bassells R, Bornpadre J, Vierheilig H, Ocampo JA, Godeas A. 2007. The effect of flavones and flavonols on colonization of tomato plants by arbuscular mycorrhizal fungi of the genera Gigaspora and Glomus. Canadian Journal of Microbiology 53, 702-709.
135. Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A. 2005. Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycological Research 109, 789-794.
136. Schaefer AL, Greenberg EP, Oliver CM, et al. 2008. A new class of homoserine lactone quorum-sensing signals. Nature 454, 595-599.
137. Schmidt PE, Broughton WJ, Werner D. 1994. Nod-factors of Bradyrhizobium japonicum and Rhizobium sp. NGR234 induce flavonoid accumulation in soybean root exudate. Molecular Plant-Microbe Interactions 7, 384-390.
138. Shaw LJ, Hooker JE. 2008. The fate and toxicity of the flavonoids naringenin and formononetin in soil. Soil Biology and Biochemistry 40, 528-536.
139. Shaw LJ, Morris P, Hooker JE. 2006. Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environmental Microbiology 8, 1867-1880.
140. Siqueira JO, Safir GR, Nair MG. 1991. Stimulation of vesiculararbuscular mycorrhizae formation and growth of white clover by flavonoid compounds. New Phytologist 118, 87-93.
141. Spaink HP. 1995. The molecuar basis of infection and nodulation by Rhizobia: the ins and outs of sympathogenesis. Annual Review of Phytopathology 33, 345-368.
142. Stafford HA. 1990. Flavonoid metabolism. Boca Raton, FL: CRC Press.
143. 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.
144. Subramanian S, Hu X, Lu GH, Odell JT, Yu O. 2004. The promoters of two isoflavone synthase genes respond differentially to nodulation and defense signals in transgenic soybean roots. Plant Molecular Biology 54, 623-639.
145. Subramanian S, Stacey G, Yu O. 2006. Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. The Plant Journal 48, 261-273.
146. Sugiyama A, Shitan N, Yazaki K. 2007. Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-Rhizobium symbiosis. Plant Physiology 144, 2000-2008.
147. Suzuki H, Takahashi S, Watanabe R, Fukushima Y, Fujita N, Noguchi A, Yokoyama R, Nishitani K, Nishino T, Nakayama T. 2006. An isoflavone conjugate-hydrolyzing beta-glucosidase from the roots of soybean (Glycine max) seedlings. Purification, gene cloning, phylogenetics, and cellular localization. Journal of Biological Chemistry 281, 30251-30259.
148. Teplitski M, Robinson JB, Bauer WD. 2000. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Molecular Plant-Microbe Interactions 13, 637-648.
149. Tomasi N, Weisskopf L, Renella G, Landi L, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S. 2008. Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biology and Biochemistry 40, 1971-1974.
150. Tsai SM, Phillips DA. 1991. Flavonoids released naturally from alfalfa promote development of symbiotic Glomus spores in vitro. Applied and Environmental Microbiology 57, 1485-1488.
151. Uppalapati SR, Marek SM, Lee HK, Nakashima J, Tang Y, Sledge MK, Dixon RA, Mysore KS. 2009. Global gene expression profiling during Medicago truncatula-Phymatotrichopsis omnivora interaction reveals a role for jasmonic acid, ethylene, and the flavonoid pathway in disease development. Molecular Plant-Microbe Interactions 22, 7-17.
152. Vandeputte OM, Kiendrebeogo M, Rajaonson S, Diallo B, Mol A, El Jaziri M, Baucher M. 2010. Identification of catechin as one of the flavonoids from Combretum albiflorum bark extract that reduces the production of quorum-sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Applied and Environmental Microbiology 76, 243-253.
153. VanEtten HD, Wu QD. 2004. Introduction of plant and fungal genes into pea (Pisum sativum L.) hairy roots reduces their ability to produce pisatin and affects their response to a fungal pathogen. Molecular Plant-Microbe Interactions 17, 798-804.
154. Vikram A, Jayaprakasha GK, Jesudhasan PR, Pillai SD, Patil BS. 2010. Suppression of bacterial cell-cell signalling, biofilm formation and type III secretion system by citrus flavonoids. Journal of Applied Microbiology 109, 515-527.
155. Von Bodman SB, Bauer WD, Coplin DL. 2003. Quorum sensing in plant-pathogenic bacteria. Annual Review of Phytopathology 41, 455-482.
156. Walker TS, Bais HP, Grotewold E, Vivanco JM. 2003. Root exudation and rhizosphere biology. Plant Physiology 132, 44-51.
157. Wang Y, Chen S, Yu O. 2011. Metabolic engineering of flavonoids in plants and microorganisms. Applied Microbiology and Biotechnology 91, 949-956.
158. 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 18, 1617-1629.
159. Wasson AP, Ramsay K, Jones MGK, Mathesius U. 2009. Differing requirements for flavonoids during the formation of lateral roots, nodules and root knot nematode galls in Medicago truncatula. New Phytologist 183, 167-179.
160. Weidenhamer JD, Boes PD, Wilcox DS. 2009. Solid-phase root zone extraction (SPRE): a new methodology for measurement of allelochemical dynamics in soil. Plant and Soil 322, 177-186.
161. Weir TL, Bais HP, Vivanco JM. 2003. Intraspecific and interspecific interactions mediated by a phytotoxin, (-)-catechin, secreted by the roots of Centaurea maculosa (spotted knapweed). Journal of Chemical Ecology 29, 2397-2412.
162. Weisshaar B, Jenkins GI. 1998. Phenylpropanoid biosynthesis and its regulation. Current Opinion in Plant Biology 1, 251-257.
163. Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E. 2006. White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant, Cell and Environment 29, 919-927.
164. Whipps JM. 2004. Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Canadian Journal of Botany 82, 1198-1227.
165. Winkel-Shirley B. 2001. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126, 485-493.
166. Winkel BSJ. 2004. Metabolic channeling in plants. Annual Review of Plant Biology 55, 85-107.
167. Wuyts N, Lognay G, Swennen R, De Waele D. 2006a. Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. Journal of Experimental Botany 57, 2825-2835.
168. Wuyts N, Swennen R, De Waele D. 2006b. Effects of plant phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita. Nematology 8, 89-101.
169. Yu O, Shi J, Hession AO, Maxwell CA, McGonigle B, Odell JT. 2003. Metabolic engineering to increase isoflavone biosynthesis in soybean seed. Phytochemistry 63, 753-763.
170. 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.
171. Zhao J, Dixon RA. 2009. MATE transporters facilitate vacuolar uptake of epicatechin 3'-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. The Plant Cell 21, 2323-2340.
172. Zhao J, Huhman D, Shadle G, He XZ, Sumner LW, Tang YH, Dixon RA. 2011. MATE2 mediates vacuolar sequestration of flavonoid glycosides and glycoside malonates in Medicago truncatula. The Plant Cell 23, 1536-1555.
173. Zuanazzi JAS, Clergeot PH, Quirion JC, Husson HP, Kondorosi A, Ratet P. 1998. Production of Sinorhizobium meliloti nod gene activator and repressor flavonoids from Medicago sativa roots. Molecular Plant-Microbe Interactions 11, 784-794.