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Plant Flavonoids: Key Players in Signaling, Establishment, and Regulation of Rhizobial and Mycorrhizal Endosymbioses

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Mycorrhiza - Function, Diversity, State of the Art

Abstract

Plants belonging to family fabaceae play an imperative role in restoring soil fertility, with the remarkable ability to engage endosymbiotically with both rhizobia and arbuscular mycorrhiza (AM). Establishment of both symbioses is based on a finely regulated molecular dialogue between two partners. Plant roots secrete an assortment of flavonoids, competent to shape rhizosphere microflora by amplifying chemotactic surface motility of beneficial microorganisms while combating pathogenic ones. Flavonoids potentially regulate transcriptional activity of many microbial genes, e.g. nod genes, and fungal hyphal branching and initiate the production of microsymbiont signal molecules (Nod/Myc factor). The perception of these lipo-chito-oligosaccharides at epidermis stimulates partly analogous downstream signal transduction cascade to activate symbiosis-related genes and consequently enable successful penetration of both microsymbionts in the host. In response to host-specific microbe, selective accumulation of flavonoids drives suppression of plant innate immunity as well as cortical cell dedifferentiation into symbiosome. High degree of coordination between root cortical cell machinery and rhizobia/AM results in the formation of symbiotic interfaces—nodules/arbuscules respectively, where harboring bacteroids and arbuscules deliver macronutrients (nitrogen and phosphorus) to host in exchange for photosynthates. Flavonoids cross-link with plant proteins to form an O2− diffusion barrier in the symbiosome membrane and serve as a checkpoint for nitrogenase efficiency. Under nutrient-rich conditions, plants regulate flavonoid fluxes to prevent an excessive establishment of metabolically expensive symbioses. Therefore, understanding these selective forces that govern host selection of beneficial rhizomicrobiome, followed by underlying establishment and regulation of symbioses in legumes, is crucial for agrobiologists to achieve sustainable agriculture.

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References

  • Abd-Alla MH, El-enany A-WE, Bagy MK, Bashandy SR (2014) Alleviating the inhibitory effect of salinity stress on nod gene expression in Rhizobium tibeticum—fenugreek (Trigonella foenum graecum) symbiosis by isoflavonoids treatment. J Plant Interact 9:275–284

    Article  CAS  Google Scholar 

  • 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 Signal Behav 7:636–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agati G, Tattini M (2010) Multiple functional roles of flavonoids in photoprotection. New Phytol 186:786–793

    Article  CAS  PubMed  Google Scholar 

  • Aggarwal A, Kadian N, Tanwar A, Yadav A, Gupta KK (2011) Role of arbuscular mycorrhizal fungi (AMF) in global sustainable development. J Appl Nat Sci 3:340–351

    Google Scholar 

  • Akiyama K, Matsuoka H, Hayashi H (2002) Isolation and identification of a phosphate deficiency-induced C-glycosyl-flavonoid that stimulates arbuscular mycorrhiza formation in melon roots. Mol Plant Microbe Interact 15:334–340

    Article  CAS  PubMed  Google Scholar 

  • Akiyama K, Tanigawa F, Kashihara T, Hayashi H (2010) Lupin pyranoisoflavones inhibiting hyphal development in arbuscular mycorrhizal fungi. Phytochemistry 71:1865–1871

    Article  CAS  PubMed  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen OM, Markham KR (2006) Flavonoids: chemistry, biochemistry and applications. CRC Press, Boca Raton

    Google Scholar 

  • Antunes PM, Goss MJ (2005) Communication in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Rhizobia and legume plants: a review. Am Soc Agron 48:199–221

    CAS  Google Scholar 

  • Antunes PM, de Variennes A, Rajcan I, Goss MJ (2006) Accumulation of specific flavonoids in soybean as a function of the early tripartite symbiosis with arbuscular mycorrhizal fungi and Bradyrhizobium japonicum. Soil Biol Biochem 38:1234–1242

    Article  CAS  Google Scholar 

  • Ardourel M, Lortet G, Maillet F, Roche P, Truchet G, Promé JC, Rosenberg C (1995) In Rhizobium meliloti, the operon associated with the nod box n5 comprises nodL, noeA and noeB, three host-range genes specifically required for the nodulation of particular Medicago species. Mol Microbiol 17:687–699

    Article  CAS  PubMed  Google Scholar 

  • 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 Physiol 151:2006–2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32

    Article  CAS  PubMed  Google Scholar 

  • Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nutr 12:547–562

    Article  Google Scholar 

  • Baptista MJ, Siqueira JO (1994) Efeito de flavonoides na germinação de esporos e no crescimento assimbiótico do fungo micorrízico arbuscular Gigaspora gigantea. Rev Bras Fisiol Veg 6:127–134

    CAS  Google Scholar 

  • Bécard G, Douds DD, Pfeffer PE (1992) Extensive in vitro hyphal growth of vesicular arbuscular mycorrhizal fungi in the presence of CO2 and flavonols. Appl Environ Microbiol 58:821–825

    PubMed  PubMed Central  Google Scholar 

  • Begum AA, Leibovitch S, Migner P, Zhang F (2001a) 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. J Exp Bot 52:1537–1543

    Article  CAS  PubMed  Google Scholar 

  • Begum AA, Leibovitch S, Migner P, Zhang F (2001b) Inoculation of pea (Pisum sativum L.) by Rhizobium leguminosarum bv. viceae preincubated with naringenin and hesperetin or application of naringenin and hesperetin directly into soil increased pea nodulation under short season conditions. Plant Soil 237:71–80

    Article  CAS  Google Scholar 

  • Bek AS, Sauer J, Thygesen MB, Duus JO, Petersen BO, Thirup S, James E, Jensen KJ, Stougaard J, Radutoiu S (2010) Improved characterization of nod factors and genetically based variations in LysM receptors domain identify amino acids expendable for nod factor recognition in lotus spp. Mol Plant Microbe 23:58–66

    Article  CAS  Google Scholar 

  • Belkheir AM, Zhou X, Smith DL (2001) Variability in yield and yield component responses to genistein pre-incubated Bradyrhizobium japonicum by soybean [Glycine max (L.) Merr] cultivars. Plant Soil 229:41–46

    Article  CAS  Google Scholar 

  • Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legranda M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Birt DF, Jeffery E (2013) Flavonoids. American Society for Nutrition. Adv Nutr 4:576–577

    Article  PubMed  PubMed Central  Google Scholar 

  • Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13:492–498

    Article  CAS  PubMed  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48. doi:10.1038/ncomms1046

    Article  PubMed  CAS  Google 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 Physiol 153:1808–1822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, Maolanon N, Vinther M, Lorentzen A, Madsen EB, Jensen KJ, Roepstorff P, Thirup S, Ronson CW, Thygesen MB, Stougaard J (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci USA 109:13859–13864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broughton WJ, Jabbouri S, Perret X (2000) Keys to symbiotic harmony. J Bacteriol 182:5641–5652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broughton WJ, Zhang F, Perret X, Staehelin C (2003) Signals exchanged between legumes and Rhizobium: agricultural uses and perspectives. Plant Soil 252:129–137

    Article  CAS  Google Scholar 

  • Bucher M, Wegmuller S, Drissner D (2009) Chasing the structures of small molecules in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 12:500–507

    Article  CAS  PubMed  Google Scholar 

  • Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. In: Dhal NK, Sahu SC (eds) Plant science. Intech, Janeza Trdine, p 107

    Google Scholar 

  • Buee M, Rossignol M, Jauneau A, Ranjeva R, Becard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant Microbe Interact 13:693–698

    Article  CAS  PubMed  Google Scholar 

  • 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. Plant Cell 16:1191–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52:98–111

    Article  CAS  PubMed  Google Scholar 

  • Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M, Hirsch S, Miwa H, Downie JA, Morris RJ, Ane JM, Oldroyd GE (2011) Nuclear membranes control symbiotic calcium signaling of legumes. Proc Natl Acad Sci USA 108:14348–14353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Soil 302:33–43

    Article  CAS  Google Scholar 

  • Catford JG, Stehelin C, Larose G, Piché Y, Vierheilig H (2006) Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285:257–266

    Article  CAS  Google Scholar 

  • Cerri MR, Frances L, Laloum T, Auriac MC, Niebel A, Oldroyd GE, Barker DG, Fournier J, de Carvalho-Niebel F (2012) Medicago truncatula ERN transcription factors: regulatory interplay with NSP1/NSP2 GRAS factors and expression dynamics throughout rhizobial infection. Plant Physiol 160:2155–2172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Soil 329:1–25

    Article  CAS  Google Scholar 

  • Chabot S, Bel-Rhlid R, Chênevert R, Piché Y (1992) Hyphal growth promotion in vitro of the VA mycorrhizal fungus, Gigaspora margarita Becker et Hall, by the activity of structurally specific flavonoid compounds under CO2-enriched conditions. New Phytol 122:461–467

    Article  CAS  Google Scholar 

  • Chen D-S, Liu C-W, Roy S, Cousins D, Stacey N, Murray JD (2015) Identification of a core set of rhizobial infection genes using data from single cell-types. Front Plant Sci 6:575. doi:10.3389/fpls.2015.00575

    PubMed  PubMed Central  Google Scholar 

  • Cheng A-X, Han X-J, Wu Y-F, Lou H-X (2014) The function and catalysis of 2-oxoglutarate-dependent oxygenases involved in plant flavonoid biosynthesis. Int J Mol Sci 15:1080–1095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20

    Article  CAS  PubMed  Google Scholar 

  • Cohen MF, Sakihama Y, Yamasaki H (2001) Roles of plant flavonoids in interactions with microbes: from protection against pathogens to the mediation of mutualism. In: Pandalai SG (ed) Recent research developments in plant physiology 2. Research Signpost, Trivandrum, pp 157–173

    Google Scholar 

  • Cooke TJ, Poli D, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338

    Article  CAS  PubMed  Google Scholar 

  • Cooper JE (2004) Multiple responses of rhizobia to flavonoids during legume root infection. Adv Bot Res 41:1–62

    Article  CAS  Google Scholar 

  • Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365

    Article  CAS  PubMed  Google Scholar 

  • Cordeiro MAS, Ferreira DA, Paulino HB, Souza CRF, Siqueira JO, Carneiro MAC (2015) Mycorrhization stimulant based in formononetin associated to fungicide and doses of phosphorus in soybean in the Cerrado. Biosci J 31:1062–1070

    Article  Google Scholar 

  • Crutzen P, Mosier AR, Smith KA, Winiwarter W (2007) N2O release from agro-fuel production negates global warming reduction by replacing fossil fuels. Atmos Chem Phys Discuss 7:11191–11205

    Article  Google Scholar 

  • D’haeseleer K, Keyser AD, Goormachtig S, Holsters M (2010) Transcription factor MtATB2: about nodulation, sucrose, and senescence. Plant Cell Physiol 51:1416–1424

    Article  PubMed  CAS  Google Scholar 

  • Dalla Via V, Zanetti ME, Blanco F (2016) How legumes recognize rhizobia. Plant Signal Behav 11(2):e1120396. doi:10.1080/15592324.2015.1120396

    Article  CAS  Google Scholar 

  • de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant Microbe Interact 14:267–277

    Article  PubMed  Google Scholar 

  • De’narie J, Debelle F, Truchet G, Prome JC (1993) Rhizobium and legume nodulation: a molecular dialogue. In: Palacios R, Moira J, Newton WE (eds) New horizons in nitrogen fixation. Kluwer, Dordrecht, pp 19–30

    Chapter  Google Scholar 

  • Delaux P-M, Radhakrishnan G, Oldroyd G (2015) Tracing the evolutionary path to nitrogen-fixing crops. Curr Opin Plant Biol 26:95–99

    Article  CAS  PubMed  Google Scholar 

  • Demont N, Debellé F, Aurelle H, Dénarié J, Promé JC (1993) Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors. J Biol Chem 268:20134–20142

    CAS  PubMed  Google Scholar 

  • Denison RF, Kiers ET (2011) Life histories of symbiotic rhizobia and mycorrhizal fungi. Curr Biol 21:775–785

    Article  CAS  Google Scholar 

  • Dixon RA, Pasinetti GM (2010) Flavonoids and Isoflavonoids: from plant biology to agriculture and neuroscience. Plant Physiol 154:453–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170

    Article  CAS  PubMed  Google Scholar 

  • Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in the Rhizobium-legume symbiosis. FEMS Microbiol Lett 285:1–9

    Article  CAS  PubMed  Google Scholar 

  • Feddermann N, Finlaya R, Bollerb T, Elfstrand M (2010) Functional diversity in arbuscular mycorrhiza—the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecol 3:1–8

    Article  Google Scholar 

  • Ferguson BJ, Indrasumunar A, Hayashi S, Lin M-L, Lin Y-H, Reid DE, Gresshoff PM (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52:61–76

    Article  CAS  PubMed  Google Scholar 

  • Fokom R, Nana WL, Tchameni S, Nwaga D (2010) Arbuscular mycorrhizal fungi (AMF) colonisation and rhizobia nodulation of cowpea as affected by flavonoid application. Res J Agric Biol Sci 6:1015–1021

    CAS  Google Scholar 

  • Fournier J, Timmers AC, Sieberer BJ, Jauneau A, Chabaud M, Barker DG (2008) Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol 148:1985–1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gachomo E, Allen JW, Pfeffer PE, Govindarajulu M, Douds DD, Jin HR, Nagahashi G, Lammers PJ, Shachar-Hill Y, Bücking H (2009) Germinating spores of Glomus intraradices can use internal and exogenous nitrogen sources for de novo biosynthesis of amino acids. New Phytol 184:399–411

    Article  CAS  PubMed  Google Scholar 

  • Gage DJ (2002) Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J Bacteriol 184:7042–7046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gagnon H, Ibrahim RK (1998) Aldonic acids: a novel family of nod gene inducers of Mesorhizobium loti, Rhizobium lupini, and Sinorhizobium meliloti. Mol Plant Microbe Interact 11:988–998

    Article  CAS  Google Scholar 

  • Geneva M, Zehirov G, Djonova E, Kaloyanova N, Georgiev G, Stancheva I (2006) The effect of inoculation of pea plants with mycorrhizal fungi and Rhizobium on nitrogen and phosphorus assimilation. Plant Soil Environ 52:435–440

    CAS  Google Scholar 

  • Genre A, Bonfante P (2010) The making of symbiotic cells in arbuscular mycorrhizal roots. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, New York, pp 57–71. doi:10.1007/978-90-481-9489-6_3

    Chapter  Google Scholar 

  • Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gholami A, Geyter ND, Pollier J, Goormachtig S, Goossens A (2014) Natural product biosynthesis in Medicago species. Nat Prod Rep 31:356–380

    Article  CAS  PubMed  Google Scholar 

  • Gianinazzi S, Gianinazzi-Pearson V (1988) Mycorrhizae: a plant’s health insurance. Chim Oggi 10:56–68

    Google Scholar 

  • Gianinazzi-Pearson V, Branzanti B, Gianinazzi S (1989) In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7:243–255

    CAS  Google Scholar 

  • Gibson KE, Kobayashi H, Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42:413–441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giovannetti M, Avio L, Sbrana C (2010) Fungal spore germination and presymbiotic mycelial growth—physiological and genetic aspects. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, New York, pp 3–32

    Chapter  Google Scholar 

  • Gobbato E (2015) Recent developments in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 26:1–7

    Article  PubMed  Google Scholar 

  • Gough C (2003) Rhizobium symbiosis: insight into Nod factor receptors. Curr Biol 13:973–975

    Article  CAS  Google Scholar 

  • Gould KS, Lister C (2005) Flavonoid functions in plants. In: Anderson OM, Markham KR (eds) Flavonoids: chemistry, biochemistry, and applications. CRC, Boca Raton, pp 397–441

    Chapter  Google Scholar 

  • Gourion B, Berrabah F, Ratet P, Stacey G (2015) Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20:186–194

    Article  CAS  PubMed  Google Scholar 

  • Graham TL (1991) Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol 95:594–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant C, Bittman S, Montreal M, Plenchette C, Morel C (2005) Soil and fertilizer phosphorus: effects on plant P supply and mycorrhizal development. Can J Plant Sci 85:3–14

    Article  Google Scholar 

  • Guenoune D, Galili S, Phillips DA, Volpin H, Chet I, Okon Y, Kapulnik Y (2001) The defense response elicited by the pathogen Rhizoctonia solani is suppressed by colonization of the AM-fungus Glomus intraradices. Plant Sci 160:925–932

    Article  CAS  PubMed  Google Scholar 

  • Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617

    Article  CAS  PubMed  Google Scholar 

  • Haag AF, Arnold MFF, Myka KK, Kerscher B, Dall’Angelo S, Zanda M, Mergaert P, Ferguson GP (2013) Molecular insights into bacteroid development during Rhizobium-legume symbiosis. FEMS Microbiol Rev 37:364–383

    Article  CAS  PubMed  Google Scholar 

  • Halbwirth H (2010) The creation and physiological relevance of divergent hydroxylation patterns in the flavonoid pathway. Int J Mol Sci 11:595–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamel LP, Beaudoin N (2010) Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant-microbe interactions. Planta 232:787–806

    Article  CAS  PubMed  Google Scholar 

  • Haney CH, Riely BK, Tricoli DM, Cook DR, Ehrhardt DW, Long SR (2011) Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell 23:2774–2787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison M, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant Microbe Interact 6:643–654

    Article  CAS  Google Scholar 

  • Hartwig UA, Maxwell CA, Joseph CM, Phillips DA (1990) Chrysoeriol and luteolin released from alfalfa seeds induce nod genes in Rhizobium meliloti. Plant Physiol 92:116–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hassan S, Mathesius U (2012) The role of flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant-microbe interactions. J Exp Bot 63:3429–3444

    Article  CAS  PubMed  Google Scholar 

  • Herder GD, Parniske M (2009) The unbearable naivety of legumes in symbiosis. Curr Opin Plant Biol 12:491–499

    Article  CAS  Google Scholar 

  • Hernández I, Alegre L, Van Breusegem F, Munné-Bosch S (2009) How relevant are flavonoids as antioxidants in plants? Trends Plant Sci 14:125–132

    Article  PubMed  CAS  Google Scholar 

  • Hichri I, Meilhoc E, Boscari A, Bruand C, Frendo P, Brouquisse R (2016) Nitric oxide: jack-of-all-trades of the nitrogen-fixing symbiosis? Adv Bot Res 77. doi:10.1016/bs.abr.2015.10.014

  • Hijri M, Sanders IR (2005) Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433:160–163

    Article  CAS  PubMed  Google Scholar 

  • Hiltner L (1904) Uber neure erfahrungen und probleme auf dem gebeit der bodenbackteriologie und unter besonderer berucksichtigung der grundungung und brache. Arb Deut Landwirsch Ges 98:59–78

    Google Scholar 

  • Hofferek V, Mendrinna A, Gaude N, Krajinski F, Devers EA (2014) MiR171h restricts root symbioses and shows like its target NSP2a complex transcriptional regulation in Medicago truncatula. BMC Plant Biol 14:199. doi:10.1186/s12870-014-0199-1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hsieh K, Huang AH (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19:582–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes JK, Hodge A, Fitter AH, Atkin OK (2008) Mycorrhizal respiration: implications for global scaling relationships. Trends Plant Sci 13:583–588

    Article  CAS  PubMed  Google Scholar 

  • Hungria M, Joseph CM, Phillips DA (1991) Rhizobium nod-gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris L.). Plant Physiol 97:759–764

    Google Scholar 

  • Indrasumunar A, Kereszt A, Searle I, Miyagi M, Li D, Nguyen CD, Men A, Carroll BJ, Gresshoff PM (2010) Inactivation of duplicated nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.) Plant Cell Physiol 51:201–214

    Article  CAS  PubMed  Google Scholar 

  • Indrasumunar A, Wilde J, Hayashi S, Li D, Gresshoff PM (2015) Functional analysis of duplicated symbiosis receptor kinase (SymRK) genes during nodulation and mycorrhizal infection in soybean (Glycine max). J Plant Physiol 176:157–168

    Article  CAS  PubMed  Google Scholar 

  • Irving HR, Boukli NM, Kelly MN, Broughton WJ (2000) Nod-factors in symbiotic development of root hairs. In: Ridge RW, Emons AMC (eds) Root hairs: cell and molecular biology. Springer, Tokyo, pp 241–265

    Chapter  Google Scholar 

  • Ivanova KA, Tsyganova AV, Brewin NJ, Tikhonovich IA, Tsyganov VE (2015) Induction of host defences by Rhizobium during ineffective nodulation of pea (Pisum sativum L.) carrying symbiotically defective mutations sym40 (PsEFD), sym33 (PsIPD3/PsCYCLOPS) and sym42. Protoplasma 252:1505–1517

    Article  CAS  PubMed  Google Scholar 

  • Jain V, Nainawatee HS (1999) Flavonoids influence growth and saccharide metabolism of Rhizobium meliloti. Folia Microbiol 44:311–316

    Article  CAS  Google Scholar 

  • Janczarek M, Skorupska A (2011) Modulation of rosR expression and exopolysaccharide production in Rhizobium leguminosarum bv. trifolii by phosphate and clover root exudates. Int J Mol Sci 12:4132–4155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janczarek M, Rachwał K, Cieśla J, Ginalska G, Bieganowski A (2015) Production of exopolysaccharide by Rhizobium leguminosarum bv. trifolii and its role in bacterial attachment and surface properties. Plant Soil 388:211–227

    Article  CAS  Google Scholar 

  • Jensen ES, Peoples MB, Boddey RM, Gresshoff PM, Hauggaard-Nielsen H, Alves BJR, Morrison MJ (2012) Legumes for mitigation of climate change and feedstock in a bio-based economy—a review. Agron Sustain Dev 32:329–364

    Article  CAS  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    Article  CAS  PubMed  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapulnik Y, Joseph CM, Phillips DA (1987) Flavone limitation to root nodulation and symbiotic nitrogen fixation in alfalfa. Plant Physiol 84:1193–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly SJ, Muszynski A, Kawaharada Y, Hubber AM, Sullivan JT, Sandal N, Carlson RW, Stougaard J, Ronson CW (2012) Conditional requirement for exopolysaccharide in the Mesorhizobium–Lotus symbiosis. Mol Plant Microbe Interact 26:319–329

    Article  CAS  Google Scholar 

  • Kereszt A, Mergaert P, Kondorosi E (2011) Bacteroid development in legume nodules: evolution of mutual benefit or of sacrificial victims? Mol Plant Microbe Interact 24:1300–1309

    Article  CAS  PubMed  Google Scholar 

  • Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ, Szczyglowski K, Parniske M (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17:2217–2229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209

    Article  CAS  PubMed  Google Scholar 

  • Kobae Y, Hata S (2010) Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 51:341–353

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi H, Naciri-Graven Y, Broughton WJ, Perret X (2004) Flavanoids induce temporal shifts in gene-expression of nod-box controlled loci in Rhizobium sp. NGR234. Mol Microbiol 51:335–347

    Article  CAS  PubMed  Google Scholar 

  • Kondorosi E, Kondorosi E (2004) Endoreduplication and activation of the anaphase-promoting complex during symbiotic cell development. FEBS Lett 567:152–157

    Article  CAS  PubMed  Google Scholar 

  • Kondorosi E, Mergaert P, Kereszt A (2013) A paradigm for endosymbiotic life: cell differentiation of rhizobium bacteria provoked by host plant factors. Annu Rev Microbiol 67:611–628

    Article  CAS  PubMed  Google Scholar 

  • Kosslak RM, Bookland R, Barkei J, Paaren EH, Appelbaum ER (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci USA 84:7428–7432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarie J, Barker DG, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:1–11

    Article  CAS  Google Scholar 

  • Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara Y, Suganuma N, Kawaguchi M (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 51:1381–1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laffont C, Rey T, André O, Novero M, Kazmierczak T, Debellé F, Bonfante P, Jacquet C, Frugier F (2015) The CRE1 cytokinin pathway is differentially recruited depending on Medicago truncatula root environments and negatively regulates resistance to a pathogen. PLoS One 10(1):e0116819. doi:10.1371/journal.pone.0116819

    Article  PubMed  PubMed Central  Google Scholar 

  • Laloum T, Baudin M, Frances L, Lepage A, Billault-Penneteau B, Cerri MR, Ariel F, Jardinaud M-F, Gamas P, de Carvalho-Niebel F, Niebel A (2014) Two CCAAT-box-binding transcription factors redundantly regulate early steps of the legume-rhizobia endosymbiosis. Plant J 79:757–768

    Article  CAS  PubMed  Google Scholar 

  • Laparre J, Malbreila M, Letissec F, Portaisc JC, Rouxa C, Bécarda G, Puech-Pagèsa V (2014) Combining metabolomics and gene expression analysis reveals that propionyl- and butyryl carnitines are involved in late stages of arbuscular mycorrhizal symbiosis. Mol Plant 7:554–566

    Article  CAS  PubMed  Google Scholar 

  • Laplaze L, Lucas M, Champion A (2015) Rhizobial root hair infection requires auxin signaling. Trends Plant Sci 20:332–334

    Article  CAS  PubMed  Google Scholar 

  • Lareen A, Burton F, Schäfer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 90:575–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larose G, Chênevert R, Moutoglis P, Gagné S, Piché 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. J Plant Physiol 159:1329–1339

    Article  CAS  Google Scholar 

  • Leibovitch S, Migner P, Zhang F, Smith DL (2001) Evaluation of the effect of Soyasignal technology on soybean yield [Glycine max (L.)] Merr under field conditions over 6 years in Eastern Canada and the Northern United States. J Agron Crop Sci 187:281–292

    Article  CAS  Google Scholar 

  • Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430

    Article  CAS  PubMed  Google Scholar 

  • Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    Article  PubMed  CAS  Google Scholar 

  • Li B, Li Y-Y, Wu H-M, Zhang F-F, Lia C-J, Li X-X, Lambers H, Li L (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. PNAS. doi:10.1073/pnas.1523580113

    Google Scholar 

  • Liang Y, Cao Y, Tanaka K, Wan J, Choi J, ho ho Kang C, Qui J, Stacey G (2013) Nonlegumes respond to rhizobial nod factors by suppressing the innate immune response. Science 34:1384-1387

    Google Scholar 

  • Limpens E, Bisseling T (2008) Nod factor signal transduction in the Rhizobium-legume symbiosis. In: AMC E, Ketelaar T (eds) Root hairs, Plant cell monographs, vol 12. Springer, Berlin, pp 249–276

    Chapter  Google Scholar 

  • Limpens E, van Zeijl A, Geurts R (2015) Lipochitooligosaccharides modulate plant host immunity to enable endosymbioses. Annu Rev Phytopathol 53:311–334

    Article  CAS  PubMed  Google Scholar 

  • Lira MA Jr, Nascimento LRS, Fracetto GGM (2015) Legume-rhizobia signal exchange: promiscuity and environmental effects. Front Microbiol 6:945. doi:10.3389/fmicb.2015.00945

    Article  PubMed  PubMed Central  Google Scholar 

  • López-Baena FJ, Ruiz-Sainz JE, Rodríguez-Carvajal MA, Vinardell JM (2016) Bacterial molecular signals in the Sinorhizobium fredii-soybean symbiosis. Int J Mol Sci 17:755. doi:10.3390/ijms17050755

    Article  PubMed Central  CAS  Google Scholar 

  • López-Lara IM, Geiger O (2001) The nodulation protein NodG shows the enzymatic activity of an 3-oxoacyl-acyl carrier protein reductase. Mol Plant Microbe Interact 14:349–357

    Article  PubMed  Google Scholar 

  • Madsen LH, Tirichine L, Jurkiwicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1:1–12

    Article  CAS  PubMed Central  Google Scholar 

  • Magori S, Kawaguchi M (2009) Long-distance control of nodulation: molecules and models. Mol Cells 27:129–134

    Article  CAS  PubMed  Google Scholar 

  • Maier W, Peipp H, Schmidt J, Wray V, Strack D (1995) Levels of a terpenoid glycoside (blumenin) and cell wallbound phenolics in some cereal mycorrhizas. Plant Physiol 109:465–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63

    Article  CAS  PubMed  Google Scholar 

  • Makarova LE, Dudareva LV, Petrova IG (2015) The content of phenolic compounds in the pea seedling root exudates depends on the size of their roots and inoculation of bacteria mutualistic and antagonistic type of interactions. J Stress Physiol Biochem 11:94–103

    Google Scholar 

  • Manchanda G, Garg N (2007) Endomycorrhizal and rhizobial symbiosis: how much do they share? J Plant Interact 2:79–88

    Article  CAS  Google Scholar 

  • Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandal SM, Chakraborty D, Dutta SR, Ghosh AK, Pati BR, Korpole S, Paul D (2016) Induction of nodD gene in a Betarhizobium isolate, Cupriavidus sp. of Mimosa pudica, by root nodule phenolic acids. Curr Microbiol 72:733–737

    Article  CAS  PubMed  Google Scholar 

  • Mapope N, Dakora FD (2013) Rrole of flavonoid and isoflavonoid molecules in symbiotic functioning and host-plant defence in the leguminosae. In: Gurib-Fakim A, Eloff JN (eds) Chemistry for sustainable development in Africa. Springer, Berlin, Heidelberg, pp 33–48

    Chapter  Google Scholar 

  • Marais JPJ, Deavours B, Dixon RA, Ferreira D (2006) The stereochemistry of flavonoids. In: Grotewold E (ed) The science of flavonoids. The Ohio State University, Columbus, OH, pp 1–46

    Chapter  Google Scholar 

  • Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptorkinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol 6:e68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martens S, Mithöfer A (2005) Flavones and flavone synthases. Phytochemistry 66:2399–2407

    Article  CAS  PubMed  Google Scholar 

  • Mathesius U (2001) Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J Exp Bot 52:419–426

    Article  CAS  PubMed  Google Scholar 

  • Mathesius U (2009) Comparative proteomic studies of root-microbe interactions. J Proteomics 72:353–366

    Article  CAS  PubMed  Google Scholar 

  • Mathesius U, Bayliss C, Weinman JJ, Schlaman HRM, Spaink HP, Rolfe BG, Mccully ME, Djordjevic MA (1998) Flavonoids synthesized in cortical cells during nodule initiation are early developmental markers in white clover. Mol Plant Microbe Interact 11:1223–1232

    Article  CAS  Google Scholar 

  • McNear DH Jr (2013) The rhizosphere—roots, soil and everything in between. Nat Educ Knowl 4:1

    Google Scholar 

  • Mechri B, Tekaya M, Cheheb H, Attia F, Hammami M (2015) Accumulation of flavonoids and phenolic compounds in olive tree roots in response to mycorrhizal colonization: a possible mechanism for regulation of defense molecules. J Plant Physiol 185:40–43

    Article  CAS  PubMed  Google Scholar 

  • Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715

    Article  CAS  PubMed  Google Scholar 

  • Messinese E, Mun JH, Yeun LH, Jayaraman D, Rougé P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, Ané JM (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20:912–921

    Article  CAS  PubMed  Google Scholar 

  • Miransari M, Smith DL (2009) Alleviating salt stress on soybean (Glycine max (L.) Merr.)-Bradyrhizobium japonicum symbiosis, using signal molecule genistein. Eur J Soil Biol 45:146–152

    Article  CAS  Google Scholar 

  • Miri M, Janakirama P, Held M, Ross L, Szczyglowski K (2016) Into the root: how cytokinin controls rhizobial infection. Trends Plant Sci. doi:10.1016/j.tplants.2015.09.003

    PubMed  Google Scholar 

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GED, Long SR (2004a) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitra RM, Shaw SL, Long SR (2004b) Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume-rhizobia symbiosis. Proc Natl Acad Sci USA 101:10217–10222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact 19:914–923

    Article  CAS  PubMed  Google Scholar 

  • Mohammadi K, Khalesro S, Sohrabi Y, Heidari G (2011) A review: beneficial effects of the mycorrhizal fungi for plant growth. J Appl Environ Biol Sci 1:310–319

    Google Scholar 

  • Morandi D, Bailey JA, Gianinazzi-Pearson V (1984) Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol Plant Pathol 24:357–364

    Article  CAS  Google Scholar 

  • Morandi D, Branzanti B, Gianinazzi-Pearson V (1992) Effect of some plant flavonoid on in vitro behavior of an arbuscular mycorrhizal. Agronomie 12:811–816

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Morieri G, Martinez EA, Jarynowski A, Driguez H, Morris R, Oldroyd GED, Downie JA (2013) Host-specific nod-factors associated with Medicago truncatula nodule infection differentially induce calcium influx and calcium spiking in root hairs. New Phytol 200:656–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moscatiello R, Squartini A, Mariani P, Navazio L (2010) Flavonoid-induced calcium signalling in Rhizobium leguminosarum bv. viciae. New Phytol 188:814–823

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee A, Ané JM (2011) Germinating spore exudates from arbuscular mycorrhizal fungi: molecular and developmental responses in plants and their regulation by ethylene. Mol Plant Microbe Interact 24:260–270

    Article  CAS  PubMed  Google Scholar 

  • Mulder L, Hogg B, Bersoult A, Cullimore JV (2005) Integration of signalling pathways in the establishment of the legume-rhizobia symbiosis. Physiol Plant 123:207–218

    Article  CAS  Google Scholar 

  • Murphy A, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211:315–324

    Article  CAS  PubMed  Google Scholar 

  • Murray JD (2011) Invasion by invitation: rhizobial infection in legumes. Mol Plant Microbe Interact 24:631–639

    Article  CAS  PubMed  Google Scholar 

  • Nair MG, Safir GR, Siqueira JO (1991) Isolation and identification of vesicular-arbuscular mycorrhiza-stimulatory compounds from clover (Trifolium repens) roots. Appl Environ Microbiol 57:434–439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Naoumkina M, Dixon RA (2008) Subcellular localization of flavonid natural products: a signalling function? Plant Signal Behav 3:573–575

    Article  Google Scholar 

  • Naoumkina M, Farag MA, Sumner LW, Tang Y, Liu C-J, Dixon RA (2007) Different mechanisms for phytoalexin induction by pathogen and wound signals in Medicago truncatula. Proc Natl Acad Sci USA 104:17909–17915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 144:673–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson MS, Sadowsky MJ (2015) Secretion systems and signal exchange between nitrogen-fixing rhizobia and legumes. Front Plant Sci 6:491. doi:10.3389/fpls.2015.00491

    Article  PubMed  PubMed Central  Google Scholar 

  • Ng JLP, Perrine-Walker F, Wasson AP, Mathesius U (2015) Flavonoids and auxin transport inhibitors rescue symbiotic nodulation in the Medicago truncatula cytokinin perception mutant cre1. Plant Cell 27:2210–2226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nijjer S, Rogers WE, Siemann E (2010) The impacts of fertilization on mycorrhizal production and investment in western gulf coast grasslands. Am Midl Nat 163:124–133

    Article  Google Scholar 

  • Novák K, Chovanec P, Skrdleta V, Kropacova M, Lisa L, Nemcova M (2002) Effect of exogenous flavonoids on nodulation of pea (Pisum sativum L.) J Exp Bot 53:1735–1745

    Article  PubMed  CAS  Google Scholar 

  • O’Neil M, Heckelman P, Koch C, Roman K, Kenny C, D’Arecca M (1996) The merck index: encyclopedia of chemicals, drugs and biological. Merck Publishing, Rahway, NJ

    Google Scholar 

  • Okazaki S, Tittabutr P, Teulet A, Thouin J, Fardoux J, Chaintreuil C, Gully D, Arrighi J-F, Furuta N, Miwa H, Yasuda M, Nouwen N, Teaumroong N, Giraud E (2016) Rhizobium-legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS. ISME J 10:64–74

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144

    Article  CAS  PubMed  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775

    Article  CAS  PubMed  Google Scholar 

  • Peck MC, Fisher RF, Long SR (2006) Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol 188:5417–5427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peck MC, Fisher RF, Bliss R, Long SR (2013) Isolation and characterization of mutant Sinorhizobium meliloti NodD1 proteins with altered responses to luteolin. J Bacteriol 195:3714–3723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16:1898–1911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peer WA, Blakeslee JJ, Yang HB, Murphy AS (2011) Seven things we think we know about auxin transport. Mol Plant 4:487–504

    Article  CAS  PubMed  Google Scholar 

  • Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial associations with legumes. Crit Rev Plant Sci 34:17–42

    Article  Google Scholar 

  • Pinior A, Wyss U, Piché Y, Vierheilig H (1999) Plants colonized by AM fungi regulate further root colonization by AM fungi through altered root exudation. Can J Bot 77:891–897

    Google Scholar 

  • Pollastri S, Tattini M (2011) Flavonols: old compounds for old roles. Ann Bot 108:1225–1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ponce M, Cervino M, Erra-Balsells R, Ocampo JA, Godeas A (2004) Flavonoids from shoots and roots of Trifolium repens (white clover) grown in presence or absence of the arbuscular mycorrhizal fungus Glomus intraradices. Phytochemistry 65:3131–3134

    Article  CAS  PubMed  Google Scholar 

  • Pumplin N, Harrison MJ (2009) Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 151:809–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2008) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Reid DE, Ferguson BJ, Hayashi S, Lin Y-H, Gresshoff PM (2011) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108:789–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Remigi P, Zhu J, Young JPW, Masson-Boivin C (2016) Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24:63–75

    Article  CAS  PubMed  Google Scholar 

  • Requena N, Breuninger M (2004) The old arbuscular mycorrhizal symbiosis in the light of the molecular era. In: Esser K, Lüttge U, Beyschlag W, Murata J (eds) Progress in botany. Springer, Berlin, Heidelberg, pp 323–356

    Chapter  Google Scholar 

  • Requena N, Serrano E, Ocón A, Breuninger M (2007) Plant signals and fungal perception during arbuscular mycorrhizal establishment. Phytochemistry 68:33–40

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro CW, Alloing G, Mandon K, Frendo P (2015) Redox regulation of differentiation in symbiotic nitrogen fixation. Biochim Biophys Acta 1850:1469–1478

    Article  CAS  PubMed  Google Scholar 

  • Rich MK, Schorderet M, Reinhardt D (2014) The role of the cell wall compartment in mutualistic symbioses of plants. Front Plant Sci 5:238. doi:10.3389/fpls.2014.00238

    Article  PubMed  PubMed Central  Google Scholar 

  • Riely BK, Lougnon G, Ané JM, Cook DR (2007) The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49:208–216

    Article  CAS  PubMed  Google Scholar 

  • Rose CM, Venkateshwaran M, Volkening JD, Grimsrud PA, Maeda J, Bailey DJ, Park K, Howes-Podoll M, den Os D, Yeun LH, Westphall MS, Sussman MR, Ane J-H, Coon JJ (2012) Rapid phosphoproteomic and transcriptomic changes in the rhizobia-legume symbiosis. Mol Cell Proteomics 11:724–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rossen L, Davis EO, Johnston AWB (1987) Plant-induced expression of Rhizobium genes involved in host specificity and early stages of nodulation. Trends Biochem Sci 12:430–433

    Article  CAS  Google Scholar 

  • Ryu H, Cho H, Choi D, Hwang I (2012) Plant hormonal regulation of nitrogen-fixing nodule organogenesis. Mol Cells 34:117–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito A, Keda S, Ezura H, Minamisawa K (2007) Microbial community analysis of the phytosphere using culture-independent methodologies. Microbes Environ 22:93–105

    Article  Google Scholar 

  • Saito K, Yonekura-Sakakibara K, Nakabayashi R, Higashi Y, Yamazaki M, Tohge T, Fernie AR (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiol Biochem 72:21–34

    Article  CAS  PubMed  Google Scholar 

  • Saslowsky DE, Warek U, Winkel BSJ (2005) Nuclear localization of flavonoid enzymes in Arabidopsis. J Biol Chem 280:23735–23740

    Article  CAS  PubMed  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005a) Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomus species in the presence of root flavonoids. J Plant Physiol 162:625–633

    Article  CAS  PubMed  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005b) Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycol Res 109:789–794

    Article  CAS  PubMed  Google Scholar 

  • 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. Can J Microbiol 53:702–709

    Article  CAS  PubMed  Google Scholar 

  • Scervino JM, Ponce MA, Monica ID, Vierheilig H, Ocampo JA, Godeas A (2009) Development of arbuscular mycorrhizal fungi in the presence of different patterns of Trifolium repens shoot flavonoids. J Soil Sci Plant Nutr 9:102–115

    Google Scholar 

  • Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–112

    Article  CAS  PubMed  Google Scholar 

  • Shaw LJ, Hooker JE (2008) The fate and toxicity of the flavonoids naringenin and formononetin in soil. Soil Biol Biochem 40:528–536

    Article  CAS  Google Scholar 

  • Shaw LJ, Morris P, Hooker JE (2006) Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ Microbiol 8:1867–1880

    Article  CAS  PubMed  Google Scholar 

  • Shtark OY, Sulima AS, Zhernakov AI, Kliukova MS, Fedorina JV, Pinaev AG, Kryukov AA, Akhtemova GA, Tikhonovich IA, Zhukov VA (2016) Arbuscular mycorrhiza development in pea (Pisum sativum L.) mutants impaired in five early nodulation genes including putative orthologs of NSP1 and NSP2. Symbiosis 68:129–144

    Article  CAS  Google Scholar 

  • Singh DP, Prabha R, Meena KK, Sharma L, Sharma AK (2014) Induced accumulation of polyphenolics and flavonoids in cyanobacteria under salt stress protects organisms through enhanced antioxidant activity. Am J Plant Sci 5(5):43916. doi:10.4236/ajps.2014.55087

    Google Scholar 

  • Sinharoy S, Liu C, Breakspear A, Guan D, Shailes S, Nakashima J, Zhang S, Wen J, Torres-Jerez I, Oldroyd G, Murray JD, Udvardi MK (2016) A Medicago truncatula cystathionine-b-synthase-like domain-containing protein is required for rhizobial infection and symbiotic nitrogen fixation. Plant Physiol 170:2204–2217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siqueira JO, Safir GR, Nair MG (1991a) Significance of phenolic compounds in plant-soil-microbial systems. Crit Rev Plant Sci 10:63–121

    Article  CAS  Google Scholar 

  • Siqueira JO, Safir GR, Nair MG (1991b) Stimulation of vesicular arbuscular mycorrhiza formation and growth of white clover by flavonoid compounds. New Phytol 118:87–93

    Article  CAS  Google Scholar 

  • Skorupska A, Wielbo J, Kidaj D, Marek-Kozaczuk M (2010) Enhancing Rhizobium-legume symbiosis using signaling factors. In: Khan MS (ed) Microbes for legume improvement. Springer, Wien, pp 27–54

    Chapter  Google Scholar 

  • Smit G, Puvanesarajah V, Carlson RW, Barbour WM, Stacey G (1992) Bradyrhizobium japonicum nodD1 can be specifically induced by soybean flavonoids that do not induce the nodYABCSUIJ operon. J Biol Chem 267:310–318

    CAS  PubMed  Google Scholar 

  • Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial nod factor-induced transcription. Science 308:1789–1791

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, Inc., San Diego, CA

    Google Scholar 

  • Smith DL, Zhang F (1999) Composition for enhancing grain yield and protein yield of legumes grown under environmental conditions that inhibit or delay nodulation thereof. US Patent-5922316

    Google Scholar 

  • Smith DL, Praslickova D, Ilangumaran G (2015) Inter-organismal signaling and management of the phytomicrobiome. Front Plant Sci 6:722. doi:10.3389/fpls.2015.00722

    PubMed  PubMed Central  Google Scholar 

  • Sosa T, Valares C, Alias JC, Lobon NC (2010) Persistence of flavonoids in Cictus landanifer soils. Plant Soil 337:51–63

    Article  CAS  Google Scholar 

  • Soyano T, Kawaguchi M (2014) Systemic regulation of root nodule formation. Division of Symbiotic Systems, National Institute for Basic Biology, Okazaki, Aichi. Available via doi:10.5772/56991

  • Spini G, Decorosi F, Cerboneschi M, Tegli S, Mengoni A, Viti C, Giovannetti L (2016) Effect of the plant flavonoid luteolin on Ensifer meliloti 3001 phenotypic responses. Plant Soil 399:159–178

    Article  CAS  Google Scholar 

  • Stafford HA (1997) Roles of flavonoids in symbiotic and defense functions in legume roots. Bot Rev 63:27–39

    Article  Google Scholar 

  • Steinkellner S, Lendzemo V, Langer I, Schweiger I, 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

    Article  CAS  PubMed  Google Scholar 

  • Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962

    Article  CAS  PubMed  Google Scholar 

  • 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 Physiol 137:1345–1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subramanian S, Stacey G, Yu O (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends Plant Sci 12:282–285

    Article  CAS  PubMed  Google Scholar 

  • 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 Physiol 144:2000–2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama A, Yamazaki Y, Yamashita K, Takahashi S, Nakayama T, Yazaki K (2016) Developmental and nutritional regulation of isoflavone secretion from soybean roots. Biosci Biotechnol Biochem 80:89–94

    CAS  Google Scholar 

  • Suzaki T, Kawaguchi M (2014) Root nodulation: a developmental program involving cell fate conversion triggered by symbiotic bacterial infection. Curr Opin Plant Biol 21:16–22

    Article  CAS  PubMed  Google Scholar 

  • 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. J Biol Chem 281:30251–30259

    Article  CAS  PubMed  Google Scholar 

  • Taurian T, Morón B, Soria-Díaz ME, Angelini JG, Tejero-Mateo P, Gil-Serrano A, Megías M, Fabra A (2008) Signal molecules in the groundnut-Bradyrhizobia interaction. Arch Microbiol 189:345–356

    Article  CAS  PubMed  Google Scholar 

  • Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323

    Article  CAS  PubMed  Google Scholar 

  • Tian F, Jia T, Yu B (2014) Physiological regulation of seed soaking with soybean isoflavones on drought tolerance of Glycine max and Glycine soja. Plant Growth Regul 74:229–237

    Article  CAS  Google Scholar 

  • Timmers ACJ, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126:3617–3628

    CAS  PubMed  Google Scholar 

  • Tóth K, Stacey G (2015) Does plant immunity play a critical role during initiation of the legume-Rhizobium symbiosis? Front Plant Sci 6:401. doi:10.3389/fpls.2015.00401

    PubMed  PubMed Central  Google Scholar 

  • Tsai SM, Phillips DA (1991) Flavonoids released naturally from alfalfa promote development of symbiotic Glomus spores in vitro. Appl Environ Microbiol 57:1485–1488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsvetkova G, Teofilova T, Georgiev GI (2006) Effect of naringein and quercetin on activity of nodabc genes of strain d293 and following nodulation and nitrogen fixation response of inoculated pea plants (Pisum sativum l.). Gen Appl Plant Physiol Special Issue:67–71

    Google Scholar 

  • van Zeijl A, Op den Camp RHM, Deinum EE, Charnikhova T, Franssen H, Op den Camp HJM, Bouwmeester H, Kohlen W, Bisseling T, Geurts R (2015) Rhizobium lipo-chitooligosaccharide signaling triggers accumulation of cytokinins in Medicago truncatula roots. Mol Plant 8:1213–1226

    Article  PubMed  CAS  Google Scholar 

  • Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21:187–198

    Article  CAS  PubMed  Google Scholar 

  • Vieira RF, Mendes IC, Reis-Junior FB, Hungria M (2010) Symbiotic nitrogen fixation in tropical food grain legumes: current status. In: Khan MS, Musarrat J, Zaidi A (eds) Microbes for legume improvement. Springer, Dordercht, Heidelberg, London, New York, pp 427–472. doi:10.1007/978-3-211-99753-6

    Chapter  Google Scholar 

  • Vierheilig H (2004a) Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176

    Article  CAS  Google Scholar 

  • Vierheilig H (2004b) Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. J Plant Physiol 161:339–341

    Article  CAS  PubMed  Google Scholar 

  • Vierheilig H, Piché Y (1995) Facteurs biochimiques potentiellement impliqués dans les interactions entre les champignons endomycorhiziens et leurs plantes non-hôtes. In: Fortin JA, Charest C, Picheé Y (eds) La symbiose mycorhizienne. Orbis Frelighsburg, Québec, pp 109–124

    Google Scholar 

  • Vierheilig H, Piché Y (2002) Signalling in arbuscular mycorrhiza: facts and hypotheses. In: Buslig B, Manthey J (eds) Flavonoids in cell functions. Kluwer/Plenum, New York, pp 23–39

    Chapter  Google Scholar 

  • Vierheilig H, Albrecht C, Bago B, Piché Y (1996) Do flavonoids play a role in root colonization by AM fungi? First International Conference on Mycorrhizae, Berkeley, CA

    Google Scholar 

  • Vierheilig H, Bago B, Albrecht C, Poulin MJ, Piché Y (1998) Flavonoids and arbuscular mycorrhizal fungi. In: Manthey J, Buslig B (eds) Flavonoids in the living system. Plenum Press, New York, pp 9–33

    Chapter  Google Scholar 

  • Vierheilig H, Steinkellner S, Khaosaad T, Garcia-Garrido JM (2008) The biocontrol effect of mycorrhization on soilborne fungal pathogens and the autoregulation of the AM symbiosis: one mechanism, two effects? In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer, Berlin, Heidelberg, pp 307–320

    Chapter  Google Scholar 

  • Volpin H, Elkind Y, Okon Y, Kapulnik Y (1994) A vesicular-arbuscular mycorrhizal fungus (Glomus intraradix) induces a defense response in alfalfa roots. Plant Physiol 104:683–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wais RJ, Keating DH, Long SR (2002) Structure-function analysis of nod factor-induced root hair calcium spiking in Rhizobium-legume symbiosis. Plant Physiol 129:211–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Yang S, Tang F, Zhu H (2012) Symbiosis specificity in the legume-rhizobial mutualism. Cell Miocrobiol 14:334–342

    Article  CAS  Google Scholar 

  • 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. Plant Cell 18:1617–1629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weerasinghe RR, Bird DMK, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc Natl Acad Sci USA 102:3147–3152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297

    Article  CAS  PubMed  Google Scholar 

  • Wilde P, Manal A, Stodden M, Sieverding E, Hilderbrandt U, Bothe H (2009) Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 11:1548–1561

    Article  PubMed  Google Scholar 

  • Williams CA, Grayer RJ (2004) Anthocyanins and other flavonoids. Nat Prod Rep 21:539–573

    Article  CAS  PubMed  Google Scholar 

  • Winkel-Shirley B (2001) It takes a garden. How work on diverse plant species has contributed to an understanding of flavonoid metabolism. Plant Physiol 127:1399–1404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong PP, Evans HJ (1971) Poly-ß-hydroxybutyrate utilization by soybean (Glycine max Merr.) nodules and assessment of its role in maintenance of nitrogenase activity. Plant Physiol 47:750–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Z-P, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ, Vögeli-Lange R, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol 108:1519–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie ZP, Muller J, Wiemken A, Broughton WJ, Boller T (1997) Nod factors and tri-iodobenzoic acid stimulate mycorrhizal colonization and affect carbohydrate partitioning in mycorrhizal roots of Lablab purpureus. New Phytol 139:361–366

    Article  Google Scholar 

  • Xie F, Murray JD, Kim J, Heckmann AB, Edwards A, Oldroyd GE, Downie JA (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci USA 109:633–638

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki A, Hayashi M (2015) Building the interaction interfaces: host responses upon infection with microorganisms. Curr Opin Plant Biol 23:132–139

    Article  PubMed  Google Scholar 

  • Yang S, Tang F, Gao M, Krishnan HB, Zhu H (2010) R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc Natl Acad Sci USA 107:18735–18740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci USA 105:20540–20545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokota S, Mizuo K, Moriya N, Oshio S, Sugawara I, Takeda K (2009) Effect of prenatal exposure to diesel exhaust on dopaminergic system in mice. Neurosci Lett 449:38–41

    Article  CAS  PubMed  Google Scholar 

  • Zhang JA, Subramanian S, Zhang YS, Yu O (2007) Flavone synthases from Medicago truncatula are flavanone-2-hydroxylases and are important for nodulation. Plant Physiol 144:741–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149:916–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Dixon RA (2010) The ‘ins’ and ‘outs’ of flavonoid transport. Trends Plant Sci 15:72–80

    Article  CAS  PubMed  Google Scholar 

  • Zhuang X, Gao J, Ma A, Fu S, Zhuang G (2013) Bioactive molecules in soil ecosystems: masters of the underground. Int J Mol Sci 14:8841–8868

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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. Mol Plant Microbe Interact 11:784–794

    Article  CAS  Google Scholar 

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Singla, P., Garg, N. (2017). Plant Flavonoids: Key Players in Signaling, Establishment, and Regulation of Rhizobial and Mycorrhizal Endosymbioses. In: Varma, A., Prasad, R., Tuteja, N. (eds) Mycorrhiza - Function, Diversity, State of the Art. Springer, Cham. https://doi.org/10.1007/978-3-319-53064-2_8

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