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Flavonoids and Nod Factors: Importance in Legume-Microbe Interactions and Legume Improvement

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Microbes for Legume Improvement

Abstract

Biological nitrogen fixation is one of the most important physiological processes in which atmospheric nitrogen is reduced to ammonia by symbiotic bacteria called rhizobia belonging to α- and β-Proteobacteria. Legume plants (Fabaceae) enter into mutualistic symbiosis with nitrogen-fixing rhizobia which enable them to grow in nitrogen-limited agricultural soils. Infection of legumes by rhizobia involves a series of sequential steps in which plant flavonoids and rhizobial Nod factors activate plant transmission signaling and initiate nodule development. Inside the nodule, rhizobia multiply and differentiate into nitrogen-fixing bacteroids. Here, besides an overview of symbiosis, the role of signal molecules, flavonoids, and Nod factors in legume growth and yield enhancement is highlighted. Recent progress in the understanding of the functions of the symbiotic signaling factors in initiation and development of symbiosis is likely to facilitate successful application thereof in sustainable agriculture to promote growth and nodulation of legume plants.

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References

  • Andrade DS, Murphy PJ, Giller KJ (2002) The diversity of Phaseolus-nodulating rhizobial populations is altered by liming of acid soils planted with Phaseolus vulgaris L. in Brazil. Appl Environ Microbiol 68:4025–4034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atti S, Bonnell R, Prasher S, Smith DL (2005) Response of soybean (Glycine max (L.) Merr.) under chronic water deficit to LCO application during flowering and pod filling. Irrig Drain 54:15–30

    Article  Google Scholar 

  • Ballare CL (2011) Jasmonate-induced defences: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257

    Article  CAS  PubMed  Google Scholar 

  • Becker A, Fraysse N, Sharypova L (2005) Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol Plant Microbe Interact 18:899–905

    Article  CAS  PubMed  Google Scholar 

  • 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. J Exp Bot 152:1537–1543

    Article  Google Scholar 

  • Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore KS, Wen J, Oldroyd GE, Downie JA, Murray JD (2014) The root hair “Infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26:4680–4701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caetano-Anollés G, Crist-Estes DK, Bauer WD (1988) Chemotaxis of Rhizobium meliloti on the plant flavone luteolin requires functional nodulation genes. J Bacteriol 170:3164–3169

    Article  PubMed  PubMed Central  Google Scholar 

  • Cebolla A, Vinardell JM, Kiss E, Oláh B, Roudier F, Kondorosi A, Kondorosi E (1999) The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 18:4476–4484

    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 

  • Chen H-C, Feng J, Hou B-H, Li F-Q, Li Q, Hong G-F (2005) Modulating DNA bending affects NodD-mediated transcriptional control in Rhizobium leguminosarum. Nucleic Acids Res 33:2540–2548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, McIver J, Yang Y, Bai Y, Schultz B, McIver A (2006) Foliar application of lipo-chitooligosaccharides (Nod factors) to tomato (Lycopersicon esculentum) enhances flowering and fruit production. Can J Plant Sci 87:365–372

    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 

  • Cren M, Kondorosi A, Kondorosi E (1995) NoIR controls expression of the Rhizobium meliloti nodulation genes involved in the core Nod factor synthesis. Mol Microbiol 15:733–747

    Article  CAS  PubMed  Google Scholar 

  • Dakora FD (2003) Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytol 158:39–49

    Article  CAS  Google Scholar 

  • D’Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–105R

    Article  PubMed  Google Scholar 

  • Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat Rev Microbiol 7:312–320

    CAS  PubMed  Google Scholar 

  • Debellé F, Rosenberg C, Vasse J, Maillet F, Martinez E, Denarie J, Truchet G (1986) Assignment of symbiotic developmental phenotypes to common and specific nodulation (nod) genetic loci of Rhizobium meliloti. J Bacteriol 168:1075–1086

    Article  PubMed  PubMed Central  Google Scholar 

  • Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631

    Article  CAS  PubMed  Google Scholar 

  • Duzan HM, Mabood F, Zhou X, Souleimanov A, Smith DL (2005) Nod factor induces soybean resistance to powdery mildew. Plant Physiol Biochem 43:1022–1030

    Article  CAS  PubMed  Google Scholar 

  • Esseling J, Lhuissier F, Emons A (2003) Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application. Plant Physiol 132:1982–1988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estévez J, Soria-Díaz ME, Fernández de Córdoba F, Morón B, Manyani H, Gil A, Thomas-Oathes J, van Brussel AAN, Dardanelli MS, Sousa C, Megías M (2009) Different and new Nod factors produced by Rhizobium tropici CIAT899 following Na+ stress. FEMS Microbiol Lett 293:220–231

    Article  PubMed  CAS  Google Scholar 

  • Faure D, Vereecke D, Leveau JH (2009) Molecular communication in the rhizosphere. Plant Soil 321:279–303

    Article  CAS  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 

  • Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, 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 

  • Fisher RF, Egelhoff TT, Mulligan JT, Long SR (1988) Specific binding of Rhizobium meliloti extracts containing nodD to DNA sequences upstream of inducible nodulation genes. Genes Dev 2:282–293

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Yoneyama K, Hugill C, Quittenden LJ, Reid JB (2013) Strigolactones: Internal and external signals in plant symbioses? Plant Signal Behav 8:e23168

    Article  PubMed  PubMed Central  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 

  • Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur J Biochem 270:1365–1380

    Article  CAS  PubMed  Google Scholar 

  • Fujishige NA, Lum MR, De Hoff PL, Whitelegge JP, Faull KF, Hirsch AM (2008) Rhizobium common nod genes are required for biofilm formation. Mol Microbiol 67:504–515

    Article  CAS  PubMed  Google Scholar 

  • Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geurts R, Fedorova E, Bisseling T (2005) Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol 8:346–352

    Article  CAS  PubMed  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 

  • Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Vermeglio A, Medigue C, Sadovsky M (2007) Legume symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312

    Article  PubMed  Google Scholar 

  • Graham PH, Vance CP (2003) Legumes: importance and constraints to greater utilization. Plant Physiol 131:872–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guasch-Vidal B, Estévez J, Dardanelli MS, Soria-Díaz ME, de Córdoba FF, Balog CI, Manyani H, Gil-Serrano A, Thomas-Oats J, Hensbergen PJ, Deeler AM, Megías M, van Brussel AA (2013) High NaCl concentrations induce the nod genes of Rhizobium tropici CIAT899 in the absence of flavonoid inducers. Mol Plant Microbe Interact 26:451–460

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18

    Article  CAS  Google Scholar 

  • Hungria M, Phillips DA (1993) Effects of a seed color mutation on rhizobial nod-gene-inducing flavonoids and nodulation in common bean. Mol Plant Microbe Interact 6:418–422

    Article  CAS  Google Scholar 

  • Hungria M, Stacey G (1997) Molecular signals exchanged between host plants and rhizobia: basic aspects and potential application in agriculture. Soil Biol Biochem 29:819–830

    Article  CAS  Google Scholar 

  • Jacobs TW, Egelhoff TT, Long SR (1985) Physical and genetic map of a Rhizobium meliloti nodulation gene region and nucleotide sequence of nodC. J Bacteriol 162:469–476

    CAS  PubMed  PubMed Central  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 

  • Kawaharada Y, Kelly S, Wibroe Nielsen M, Hjuler CT, Gysel K, Muszynski A, Carlson MB, Thygesen RW, Sandal N, Asmussen MH, Vinther M, Andersen SU, Krusell L, Thirup S, Jensen KJ, Ronson CW, Blaise M, Radutoiu S, Stougaard J (2015) Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523:308–312

    Article  CAS  PubMed  Google Scholar 

  • Kidaj D, Wielbo J, Skorupska A (2012) Nod factors stimulate seed germination and promote growth and nodulation of pea and vetch under competitive conditions. Microbiol Res 167:144–150

    Article  CAS  PubMed  Google Scholar 

  • Kondorosi E, Gyuris J, Schmidt J, John E, Hofmann DB, Schell J, Kondorosi A (1989) Positive and negative control of nod gene expression in Rhizobium meliloti is reqiured for optimal nodulation. EMBO J 8:1331–1340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kouchi H, Shimomura K, Hata S, Hirota A, Wu G-J, Kumagai H, Tajima S, Suganuma N, Suzuki A, Aoki T, Hayashi M, Yokoyama T, Ohyama T, Asamizu E, Kuwata C, Shibata D, Tabata S (2004) Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus. DNA Res 11:263–274

    Article  CAS  PubMed  Google Scholar 

  • 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. Mol Plant Microbe Interact 16:617–625

    Article  CAS  PubMed  Google Scholar 

  • Laguerre G, Courdr L, Nouaim R, Lamy I, Revellin C, Breuil MC, Chaussod R (2006) Response of rhizobial populations to moderate copper stress applied to an agricultural soil. Microb Ecol 52:426–435

    Article  CAS  PubMed  Google Scholar 

  • Lerouge P, Roche P, Faucher C, Maillet F, Denarie J, Prome J-C, Truchet G (1996) Substance with lipo-oligosachcaride structure capable of acting as plant-specific symbiotic signals, processes for producing them and their applications. US Patent 5,549,718, filed 30 Sept 1994 and issued 27 Aug 1996

    Google Scholar 

  • Leibovitch S, Migner P, 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 

  • Liu C-W, Breakspear A, Roy S, Murray JD (2015) Cytokinin responses counterpoint auxin signaling during rhizobial infection. Plant Signal Behav 10(6):e1019982

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Long SR (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mabood F, Jung WJ, Smith DL (2008) Signals in the underground: microbial signaling and plant productivity. In: Nautiyal CS, Dion PE, Chopra VL (eds) Molecular mechanism of plant and microbe coexistence. Springer-Verlag, Berlin, Heidelberg, pp 291–318

    Chapter  Google Scholar 

  • Macchiavelli RE, Brelles-Marino G (2004) Nod factor-treated Medicago truncatula roots and seeds show an increased number of nodules when inoculated with a limiting population of Sinorhizobium meliloti. J Exp Bot 55:2635–2640

    Article  CAS  PubMed  Google Scholar 

  • Madsen LH, Tirichine L, Jurkiewicz 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 1:10

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maj D, Wielbo J, Marek-Kozaczuk M, Skorupska A (2009) Pretreatment of clover seeds with Nod factors improves growth and nodulation of Trifolium pratense. J Chem Ecol 35:479–487

    Article  CAS  PubMed  Google Scholar 

  • Maj D, Wielbo J, Marek-Kozaczuk M, Skorupska A (2010) Response to flavonoids as a factor influencing competitiveness and symbiotic activity of Rhizobium leguminosarum. Microbiol Res 165:50–60

    Article  CAS  PubMed  Google Scholar 

  • Maroti G, Kondorosi E (2014) Nitrogen-fixing Rhizobium-legume symbiosis: are polyploidy and host peptide governed symbiont differentiation general principles of endosymbiosis? Front Microbiol 5(326):1–6

    Google Scholar 

  • Martinez-Abarca F, Herrera-Cervera JA, Bueno P, Sanjuan J, Bisseling T, Olivares J (1998) Involvement of salicylic acid in the establishment of the Rhizobium meliloti – alfalfa symbiosis. Mol Plant Microbe Interact 11:153–155

    Article  CAS  Google Scholar 

  • Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466

    Article  CAS  PubMed  Google Scholar 

  • Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset A.-E., Barloy-Hubler F, Galibert F, Kondorosi A, Kondorosi E (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proceedings of the National Academy of Sciences 103(13):5230–5235

    Google Scholar 

  • Morón B, Soria-Díaz ME, Ault J, Verroios G, Noreen S, Rodríguez-Navarro DN, Gol-Serrano A, Thomas-Oathes J, Megías M, Sousa C (2005) Low pH changes the profile of nodulation factors produced by Rhizobium tropici CIAT899. Chem Biol 12:1029–1040

    Article  PubMed  CAS  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of proteobacteria. Nature 411:948–950

    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 

  • Newton WE (2007) Physiology, biochemistry and molecular biology of nitrogen fixation. In: Bothe H, Ferguson S, Newton WE (eds) Biology of nitrogen cycle. Elsevier, Amsterdam, pp 109–130

    Chapter  Google Scholar 

  • Okazaki S, Kaneko T, Sato S, Saeki K (2013) Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proc Natl Acad Sci U S A 110:17131–17136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oláh B, Brière C, Bécard G, Dénarié J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44:195–207

    Article  PubMed  CAS  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 GE, 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 

  • Oono R, Schmitt I, Sprent JI, Denison RF (2010) Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation. New Phytol 187:508–520

    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 

  • Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275:527–530

    Article  CAS  PubMed  Google Scholar 

  • Penterman J, Abo RP, De Nisco NJ, Arnold MFF, Longhi R, Zanda M, Walker GC (2014) Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis. Proc Natl Acad Sci U S A 111:3561–3566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peoples MB, Brockwell J, Herridge DF, Rochester IJ, Alves BJR, Urquiaga S, Boddey RM, Dakora FD, Bhattarai S, Maskey SL, Sampet C, Rerkasem B, Khan DF, Hauggaard-Nielsen H, Jensen ES (2009) The contribution of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48:1–17

    Article  CAS  Google Scholar 

  • Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:917–1008

    Article  Google Scholar 

  • Podleśny J, Wielbo J, Podleśna A, Kidaj D (2014a) The pleiotropic effects of extract containing rhizobial Nod factors on pea growth and yield. Centr Eur J Biol 9:396–409

    Google Scholar 

  • Podleśny J, Wielbo J, Podleśna A, Kidaj D (2014b) The responses of two pea genotypes to Nod factors (LCOs) treatment. J Food Agric Environ 12:554–558

    Google Scholar 

  • Podleśna A, Wielbo J, Podleśny J, Kidaj D (2015) Effect of sulfur and Nod factors (LCOs) on some physiological features and yield of pea (Pisum sativum L.) In: De Kok LJ et al (eds) Molecular physiology and ecophysiology of sulfur proceedings of the international plant sulfur workshop. Springer International Publishing, Switzerland, pp 221–226

    Chapter  Google Scholar 

  • Prell J, Poole P (2006) Metabolic changes of rhizobia in legume nodules. Trends Microbiol 14:161–168

    Article  CAS  PubMed  Google Scholar 

  • Prithiviraj B, Zhou X, Souleimanov A, Kahn WM, Smith DL (2003) A host-specific bacteria-to-plant signal molecule (Nod factor) enhances germination and early growth of diverse crop plants. Planta 21:437–445

    Google Scholar 

  • Promé (1996) Signaling events elicited in plants by defined oligosaccharide structures. Curr Opin Struct Biol 6:671–678

    Article  PubMed  Google Scholar 

  • Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature 323:632–634

    Article  CAS  Google Scholar 

  • Roche P, Debellé F, Maillet F, Lerouge P, Faucher C, Truchet G, Dénarie J, Promé J-C (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67:1131–1143

    Article  CAS  PubMed  Google Scholar 

  • Ruvkun GB, Ausubel FM (1980) Interspecies homology of nitrogenase genes. Proc Natl Acad Sci U S A 77:191–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32:33–57

    Article  CAS  PubMed  Google Scholar 

  • Siczek A, Frąc M, Nawrocka A, Wielbo J, Kidaj D (2015) The response of rhizosphere microbial properties to flavonoids and Nod factors. Acta Agric Scand B 65:125–131

    CAS  Google Scholar 

  • Siczek A, Lipiec J, Wielbo J, Kidaj D, Szarlip P (2014) Symbiotic activity of pea (Pisum sativum) after application of nod factors under field conditions. Int J Mol Sci 15:7344–7351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skorupska A, Białek U, Urbanik-Sypniewska T, Van Lammeren A (1995) Two types of nodules induced on Trifolium pratense by mutants of Rhizobium leguminosarum bv. trifolii deficient in exopolysaccharide production. J Plant Physiol 147:93–100

    Article  CAS  Google Scholar 

  • Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Fact 5:1–19

    Article  CAS  Google Scholar 

  • Skorupska A, Wielbo J, Maj D, Marek-Kozaczuk M (2010) Enhancing rhizobium–legume symbiosis using signaling factors. In: Khan MS et al (eds) Microbes for legume improvement. Springer-Verlag, Wien, pp 27–54

    Chapter  Google Scholar 

  • Smith DL, Bo P, Deng Y, Migner P, Zhang F, Prithiviraj B, Habib A (2005a) Composition for accelerating seed germination and plant growth. US Patent 6,979,664B1, filed 21 July 1999 and issued 27 December 2005

    Google Scholar 

  • Smith S, Habib A, Kang Y, Legget M, Diaz-Zorita M (2015) LCO applications provide improved response with legumes and nonlegumes. In: De Brujin FJ (ed) Biological nitrogen fixation. John Wiley & Sons, New York, pp 1077–1085

    Chapter  Google Scholar 

  • Smith RS, Osburn RM (2009) Lipo-oligosaccharide and flavonoid combination for enhanced plant growth and yield. Patent WO2009/049747A2, filed 23 September 2008 and issued 23 April 2009

    Google Scholar 

  • Smith RS, Osburn RM (2010) Lipo-chitooligosaccharide compositions for enhanced plant growth and yield. US Patent 2010/0093537A1, filed 8 January 2008 and issued 15 April 2010

    Google Scholar 

  • Smith RS, Osburn RM, Kosanke JW (2005b) Methods and compositions providing agronomically beneficial effects in legumes and non-legumes. Patent WO2005062899, filed 23 December 2004 and issued 3 November 2005

    Google Scholar 

  • Soto MJ, Fernández-Aparicio M, Castellanos-Morales V, García-Garrido JM, Okampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:383–385

    Article  CAS  Google Scholar 

  • Souleimanov A, Prithiviraj B, Smith DL (2002) The major Nod factor of Bradyrhizobium japonicum promotes early growth of soybean and corn. J Exp Bot 376:1929–1934

    Article  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Okon Y (2009) Plant growth promoting actions of rhizobacteria. Adv Bot Res 51:283–320

    Article  CAS  Google Scholar 

  • Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annu Rev Microbiol 54:257–288

    Article  CAS  PubMed  Google Scholar 

  • Staehelin C, Schultze M, Kondorosi E, Kondorosi A (1995) Lipo-chitooligosaccharide nodulation signals from Rhizobium meliloti induce their rapid degradation by the host plant alfalfa. Plant Physiol 108:1607–1614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staehelin C, Schultze M, Tokuyasu K, Poinsot V, Promé J-C, Kondorosi E, Kondorosi A (2000) N-deacetylation of Sinorhizobium meliloti Nod factors increases their stability in the Medicago sativa rhizosphere and decreases their biological activity. Mol Plant Microbe Interact 13:72–79

    Article  CAS  PubMed  Google Scholar 

  • Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273

    Article  CAS  PubMed  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 

  • Suzaki T, Yoro E, Kawaguchi M (2015) Leguminous plants: inventors of root nodules to accommodate symbiotic bacteria. Int Rev Cell Mol Biol 316:111–158

    Article  PubMed  Google Scholar 

  • Tian Y, Liu W, Cai J, Zhang LY, Wong KB, Feddermann N, Boller T, Xie ZP, Staehelin C (2013) The nodulation factor hydrolase of Medicago truncatula: characterization of an enzyme specifically cleaving rhizobial nodulation signals. Plant Physiol 163:1179–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timmers AC, 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 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toth K, Stacey G (2015) Does plant immunity play a critical role during initiation of the legume-rhizobium symbiosis? Front Plant Sci 6:401

    PubMed  PubMed Central  Google Scholar 

  • Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, Satiat-Jeunemaître B, Alunni B, Bourge M, Kucho K, Abe M, Kereszt A, Maroti G, Uchiumi T, Kondorosi E, Mergaert P (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122–1126

    Article  PubMed  CAS  Google Scholar 

  • Vasse J, de Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172:4295–4306

    Article  CAS  PubMed  PubMed Central  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 

  • 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 

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

    Article  Google Scholar 

  • Yates RJ, Howieson JG, Reeve WG, O’Hara GW (2011) A re-appraisal of the biology and terminology describing rhizobial success in nodule occupancy of legumes in agriculture. Plant Soil 348:255–267

    Article  CAS  Google Scholar 

  • Yeh KC, Peck MC, Long SR (2002) Luteolin and GroESL modulate in vitro activity of NodD. J Bacteriol 184:525–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaat SA, Wijffelman CA, Mulders IHM, van Brussel AAN, Lugtenberg BJJ (1988) Root exudates of various host plants of Rhizobium leguminosarum contain different sets of inducers of Rhizobium nodulation genes. Plant Physiol 86:1298–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaat SA, Schripsema J, Wijffelman CA, van Brussel AAN, Lugtenberg BJJ (1989) Analysis of the major inducers of the Rhizobium nodA promoter from Vicia sativa root exudate and their activity with different nodD genes. Plant Mol Biol 13:175–188

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Smith DL (1995) Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean at suboptimal root zone temperatures. Plant Physiol 108:961–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Smith DL (1996) Inoculation of soybean (Glycine max (L.) Merr.) with genistein-preincubated Bradyrhizobium japonicum or genistein directly applied into soil increases soybean protein and dry matter yield under short season conditions. Plant Soil 179:233–241

    Article  CAS  Google Scholar 

  • Zhang J, Subramanian S, Stacey G, Yu O (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J 57:171–183

    Article  CAS  PubMed  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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Acknowledgments

This study is included in the framework of following Research Project from Polish National Centre for Research and Development PBS3/A8/28/2015 SEGENMAS.

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Authors and Affiliations

  1. Department of Genetics and Microbiology, Maria Curie-Skłodowska University, Akademicka 19, 20-033, Lublin, Poland

    Anna Skorupska, Dominika Kidaj & Jerzy Wielbo

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  1. Anna Skorupska
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  2. Dominika Kidaj
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  3. Jerzy Wielbo
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Correspondence to Anna Skorupska .

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Editors and Affiliations

  1. Dept of Agricultural Microbiology, Faculty of Agricultural Sciences, Aligarh Muslim University, Aligarh, India

    Almas Zaidi

  2. Dept of Agricultural Microbiology, Faculty of Agricultural Sciences, Aligarh Muslim University, Aligarh, India

    Mohammad Saghir Khan

  3. Dept of Agricultural Microbiology, Faculty of Agricultural Sciences, Aligarh Muslim University, Aligarh, India

    Javed Musarrat

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Skorupska, A., Kidaj, D., Wielbo, J. (2017). Flavonoids and Nod Factors: Importance in Legume-Microbe Interactions and Legume Improvement. In: Zaidi, A., Khan, M., Musarrat, J. (eds) Microbes for Legume Improvement. Springer, Cham. https://doi.org/10.1007/978-3-319-59174-2_3

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