Signalling and Communication in the Actinorhizal Symbiosis

  • Claudine FrancheEmail author
  • Didier Bogusz
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 11)


More than 200 species of non-legume dicotyledonous plants, mostly trees and shrubs, belonging to eight different families and 24 genera can enter actinorhizal symbioses with the nitrogen-fixing actinomycete Frankia. Actinorhizal nodules consist of multiple lobes, each of which displays a lateral root structure with infected cells in the expanded cortex. Whereas the key molecules involved in the molecular dialogue between the symbiotic partners have not yet been characterized, the development of genomic and molecular tools both in Frankia and in some actinorhizal plants has contributed to a better understanding of this original endosymbiosis.


Root Hair Infection Thread Frankia Strain Symbiotic Gene Actinorhizal Plant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Alloisio N, Felix S, Marechal J, Pujic P, Rouy Z, Vallenet D, Medigue C, Normand P (2007) Frankia alni proteome under nitrogen-fixing and nitrogen-replete conditions. Physiol Plant 130:440–453Google Scholar
  2. Alloisio N, Queiroux C, Fournier P, Pujic P, Normand P, Vallenet D, Médigue C, Yamaura M, Kakoi K, Kucho K-I (2010) The Frankia alni symbiotic transcriptome. Mol Plant Microbe Interact 23:593–607PubMedGoogle Scholar
  3. Auguy F, Abdel-Lateif K, Doumas P, Badin P, Guerin V, Bogusz D, Houcher V (2011) Isoflavonoids pathway activation in actinorhizal symbioses. Funct Plant Biol, in pressGoogle Scholar
  4. Bagnarol E, Popovici J, Alloisio N, Maréchal J, Pujic P, Normand P, Fernandez M (2007) Differential Frankia protein patterns induced by phenolic extracts from Myricaceae seeds. Physiol Plant 130:380–390Google Scholar
  5. Benoit LF, Berry AM (1997) Flavonoid-like compounds from red alder (Alnus rubra) influence nodulation by Frankia (Actinomycetales). Physiol Plant 99:588–593Google Scholar
  6. Benson DR, Clawson ML (2000) Evolution of the actinorhizal plant symbioses. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for analysis of biological process. Horizon Scientific Press, Wymondham, UK, pp 207–224Google Scholar
  7. Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–319PubMedCentralPubMedGoogle Scholar
  8. Berg RH (1990) Cellulose and xylans in the interface capsule in symbiotic cells of actinorhizae. Protoplasma 159:35–43Google Scholar
  9. Berg RH (1999) Frankia forms infection threads. Can J Bot 77:1327–1333Google Scholar
  10. Berg RH, McDowell L (1987) Endophyte differentiation in Casuarina actinorhizae. Protoplasma 136:104–117Google Scholar
  11. Berry AM, Sunnel LA (1990) The infection process and nodule development. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, New York, pp 61–81Google Scholar
  12. Berry AM, McIntyre L, McCully M (1986) Fine structure of root hair infection leading to nodulation in the Frankia-Alnus symbiosis. Can J Bot 64:292–305Google Scholar
  13. Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 90:6091–6094PubMedGoogle Scholar
  14. Bhattacharya A, Sood P, Citovsky V (2010) The roles of plant phenolics in defense and communication during Agrobacterium and Rhizobium infection. Mol Plant Pathol 11:705–719PubMedGoogle Scholar
  15. Bhuvaneswari TV, Solheim B (2000) Root-hair interactions in actinorhizal symbioses. In: Ridge RW, Emons AMC (eds) Root hairs – cell and molecular biology. Springer, Heidelberg, pp 311–327Google Scholar
  16. Callaham D, Torrey JG (1977) Prenodule formation and primary nodule development in roots of Comptonia (Myricaceae). Can J Bot 51:2306–2318Google Scholar
  17. Callaham D, DelTredici P, Torrey JG (1978) Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 199:899–902PubMedGoogle Scholar
  18. Callaham D, Newcomb W, Torrey JG, Peterson RL (1979) Root hair infection in actinomycete-induced root nodule initiation in Casuarina, Myrica and Comptonia. Bot Gaz 140:S1–S9Google Scholar
  19. Capoen W, Goormachtig S, De Rycke R, Schoeyers K, Holsters M (2005) SrSymRK, a plant receptor essential for symbiosome infection. Proc Natl Acad Sci USA 102:10369–10374PubMedGoogle Scholar
  20. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171PubMedGoogle Scholar
  21. Cérémonie H, Debellé F, Fernandez MP (1999) Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can J Bot 77:1293–1301Google Scholar
  22. Charron D, Pingret JL, Chabaud M, Journet EP, Barker DG (2004) Pharmacological evidence that multiple phospholipid signaling pathways link Rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses, including Ca2+ spiking and specific ENOD gene expression. Plant Physiol 136:3582–3593PubMedCentralPubMedGoogle Scholar
  23. Clawson ML, Bourret A, Benson DR (2004) Assessing the phylogeny of Frankia-related plant nitrogen-fixing root nodule symbioses with Frankia 16SRNA and glutamine synthetase gene sequences. Mol Phylogenet Evol 31:131–138PubMedGoogle Scholar
  24. D’Agostino IB, Deruère J, Kieber JJ (2000) Characterization of the response of the arabidopsis response regulator gene family to cytokinin. Plant Physiol 124:1706–1717PubMedCentralPubMedGoogle Scholar
  25. Dawson JO (1986) Actinorhizal plants: their use in forestry and agriculture. Outlook Agric 15(4):202–208Google Scholar
  26. Dawson JO (2008) Ecology of actinorhizal plants. In: Pawlowski K, Newton WE (eds) Nitrogen fixation research: origins and progress, vol VI, Nitrogen-fixing Actinorhizal symbioses. Springer, Heidelberg, pp 199–234Google Scholar
  27. Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipochitooligosaccharide nodulation factor: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535PubMedGoogle Scholar
  28. Diem HG, Dommergues YR (1990) Current and potential uses and management of Casuarinaceae in the tropics and subtropics. In: Schwintzer R, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, San Diego, pp 317–342Google Scholar
  29. Diouf D, Gherbi H, Prin Y, Franche C, Duhoux E, Bogusz D (1995) Hairy root nodulation of Casuarina glauca: a system for the study of symbiotic gene expression in an actinorhizal tree. Mol Plant Microbe Interact 8:532–537PubMedGoogle Scholar
  30. Diouf D, Sy M-O, Gherbi H, Bogusz D, Franche C (2008) Casuarinaceae. In: Kole CR, Scorza R, Hall TC (eds) Compendium of transgenic crop plants, vol 9, Transgenic forest tree species. Blackwell, Oxford, UK, pp 279–292Google Scholar
  31. Duhoux E, Diouf D, Gherbi H, Franche C, Ahée J, Bogusz D (1996) Le nodule actinorhizien. Acta bot Gallica 143:593–608Google Scholar
  32. Endre G, Kereszt A, Devei Z, Mihacea S, Kalo P, Kiss G (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966PubMedGoogle Scholar
  33. Franche C, Diouf D, Le QV, N’Diaye A, Gherbi H, Bogusz D, Gobé C, Duhoux E (1997) Genetic transformation of the actinorhizal tree Allocasuarina verticillata by Agrobacterium tumefaciens. Plant J 11:897–904Google Scholar
  34. Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59Google Scholar
  35. Geurts R, Federova E, Bisseling T (2005) Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol 8:346–352PubMedGoogle Scholar
  36. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008a) SymRK defines a common genetic basis for plant root endosymbioses with AM fungi, rhizobia and Frankia bacteria. Proc Natl Acad Sci USA 105:4928–4932PubMedGoogle Scholar
  37. Gherbi H, Nambiar-Veetil M, Zhong C, Félix J, Autran D, Girardin R, Vaissayre V, Auguy F, Bogusz D, Franche C (2008b) Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata. Mol Plant Microbe Interact 21:518–524PubMedGoogle Scholar
  38. Gordons A, Stevens JR, Berry AM (1988) Cytokinin secretion by Frankia sp. HFPArI3 in defined medium. Plant Physiol 87:15–16Google Scholar
  39. Hammad Y, Nalin R, Marechal J, Fiasson K, Pepin RAM, Normand P, Domenach AM (2003) A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia. Plant Soil 254:193–205Google Scholar
  40. Hann D (2008) Polyphasic taxonomy of the genus Frankia. In: Pawlowski K, Newton WE (eds) Nitrogen fixation research: origins and progress, vol VI, Nitrogen-fixing actinorhizal symbioses. Springer, Heidelberg, pp 25–47Google Scholar
  41. Hemerly AS, Bergouniou C, Van Montagu M, Inzé D, Ferreira P (1992) Gene regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidodpsis thaliana. Proc Natl Acad Sci USA 89:3295–3299PubMedGoogle Scholar
  42. Hemerly AS, Ferreira PCG, de Almeida EJ, van Montagu M (1993) cdc2a expression in Arabidopsis thaliana is linked with competence for cell division. Plant Cell 5:1711–1723PubMedCentralPubMedGoogle Scholar
  43. Hocher V, Auguy F, Argout X, Laplaze L, Franche C, Bogusz D (2006) Expressed sequence – tag analysis in Casuarina glauca actinorhizal nodule and root. New Phytol 169:681–688PubMedGoogle Scholar
  44. Houcher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P, Normand P, Bogusz D (2011) Transcriptomics of actionorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol 56:700–771Google Scholar
  45. Hughes M, Donnelly C, Crozier A, Wheeler CT (1999) Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation. Can J Bot 77:1311–1315Google Scholar
  46. Huss-Danell K (1997) Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405Google Scholar
  47. John TR, Rice JM, Johnson JD (2001) Analysis of pFQ12, a 22.4-kb Frankia plasmid. Can J Microbiol 47:608–617PubMedGoogle Scholar
  48. Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant Microbe Interact 14:737–748PubMedGoogle Scholar
  49. Kucho K-I, Kakoi K, Yamaura M, Higashi S, Uchiumi T, Abe M (2009) Transient transformation of Frankia by fusion marker genes in liquid culture. Microbes Environ 24:231–240PubMedGoogle Scholar
  50. Laplaze L, Duhoux E, Franche C, Frutz T, Svistoonoff S, Bisseling T, Bogusz D, Pawlowski K (2000a) Casuarina glauca prenodule cells display the same differentiation as the corresponding nodule cells. Mol Plant Microbe Interact 13:107–112PubMedGoogle Scholar
  51. Laplaze L, Ribeiro A, Franche C, Duhoux E, Auguy F, Bogusz D, Pawlowski K (2000b) Characterization of a Casuarina glauca nodule-specific subtilisin-like protease gene, a homolog of Alnus glutinosa ag12. Mol Plant Microbe Interact 13:113–117PubMedGoogle Scholar
  52. Laplaze L, Svistoonoff S, Santi C, Auguy F, Franche C, Bogusz D (2008) Molecular biology of actinorhizal symbioses. In: Pawlowski K, Newton WE (eds) Nitrogen fixation research: origins and progress, vol VI, Nitrogen-fixing actinorhizal symbioses. Springer, Heidelberg, pp 235–259Google Scholar
  53. Lavire C, Cournoyer B (2003) Progress on the genetics of the N2-fixing actinorhizal symbiont Frankia. Plant Soil 254:125–137Google Scholar
  54. Lavire C, Louis D, Perriere G, Briolay J, Normand P, Cournoyer B (2001) Analysis of pFQ31, a 8551-bp cryptic plasmid from three symbiotic nitrogen-fixing actinomycete Frankia. FEMS Microbiol Lett 197:111–116PubMedGoogle Scholar
  55. Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet E, AnéJ-M LE, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364PubMedGoogle Scholar
  56. Liu Q, Berry AM (1991) The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis. Protoplasma 163:82–92Google Scholar
  57. Madsen LH, Tirichine L, Jurkiewicz A, 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 1:1–12PubMedCentralGoogle Scholar
  58. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Logn SR, Schultze M, Ratet P, Oldroyd GED (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335PubMedCentralPubMedGoogle Scholar
  59. Mastronunzio JE, Huang Y, Besnon DR (2009) Diminished exoproteome of Frankia spp. in culture and symbiosis. App Environ Microbiol 75:6721–6728Google Scholar
  60. McEwan NR, Green DC, Wheeler CT (1992) Utilisation of the root hair curling reaction in Alnus glutinosa for the assay of nodulation signal compounds. Acta Oecol 13:509–510Google Scholar
  61. Miller IM, Baker DD (1985) The initiation, development and structure of root nodules in Elaegnus angustifolia L. (Elaeagnaceae). Protoplasma 128:107–119Google Scholar
  62. Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Olroyd GE, Long SR (2004) A Ca2+/calmodulin dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705PubMedGoogle Scholar
  63. Newcomb WR, Wood S (1987) Morphogenesis and fine structure of Frankia (Actinomycetales): the microsymbiont of nitrogen-fixing actinorhizal root nodules. Int Rev Cytol 109:1–88PubMedGoogle Scholar
  64. Normand P, Fernandez MP (2009) Evolution and diversity of Frankia. Microbiol Monogr 8:103–125Google Scholar
  65. Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra AK (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of family Frankiaceae. Int J Syst Bacteriol 46:1–9PubMedGoogle Scholar
  66. Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Martinez M, Mastronunzio JE, Mullin BC, Nieman J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tvares F, Tomkins JP, Vallenet D, Valverde C, Wall L, Wang Y, Medigue C, Benson DR (2007a) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15PubMedGoogle Scholar
  67. Normand P, Queiroux C, Tisa LS, Benson DR, Rouy Z, Cruveiller S, Medigue C (2007b) Exploring the genomes of Frankia. Physiol Plant 130:331–343Google Scholar
  68. Oldroyd GED, Downie JA (2008) Coordinating nodule morphologenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546PubMedGoogle Scholar
  69. Parsons R, Silvester WB, Harris S, Gruijters WTM, Bullivant S (1987) Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase. Plant Physiol 83:728–731PubMedCentralPubMedGoogle Scholar
  70. Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8:1899–1913PubMedCentralPubMedGoogle Scholar
  71. Pawlowski K, Sprent J (2008) Comparison between actinorhizal and legume symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, The Netherlands, pp 261–288Google Scholar
  72. Péret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, Franche C, Bogusz D, Bennett M, Laplaze L (2007) Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiol 144:1852–1862PubMedCentralPubMedGoogle Scholar
  73. Prin Y, Rougier M (1987) Preinfection events in the establishment of Alnus-Frankia symbiosis: study of the root hair deformation step. Plant Physiol 6:99–106Google Scholar
  74. Rawnsley T, Tisa LS (2007) Development of a physical map for three Frankia strains and a partial genetic map for Frankia EuI1c. Physiol Plant 130:427–439Google Scholar
  75. Reddy SM, Hitchin S, Melayah D, Pandey AK, Raffier C, Henderson J, Marmeisse R, Gay G (2006) The auxin-inducible GH3 homologue Pp-GH3.16 is downregulated in Pinus pinaster root systems on ectomycorrhizal symbiosis establishment. New Phytol 170:391–400PubMedGoogle Scholar
  76. Rodriguez-Barrueco F, De Castro B (1973) Cytokinin-induced pseudonodules in Alnus glutinosa. Physiol Plant 29:277–280Google Scholar
  77. Santi C, von Groll U, Ribeiro A, Chiurazzi M, Auguy F, Bogusz D, Franche C, Pawlowski K (2003) Comparison of nodule induction in legume and actinorhizal symbiosis: the induction of actinorhizal nodules does not involve ENOD40. Mol Plant Microbe Interact 16:808–816PubMedGoogle Scholar
  78. Savouré A, Sallaud C, El-Turk J, Zuanazzi J, Ratet P, Schultze M, Kondorosi A, Esnault R, Kondorosi E (1997) Distinct response of Medicago suspension cultures ad roots to Nod factors and chitin oligomers in the elicitation of defense-related responses. Plant J 11:277–287Google Scholar
  79. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195PubMedGoogle Scholar
  80. Silvester WB (1976) Ecological and economic significance of the non-legume symbiosis. In: Newton WE, Nyman CJ (eds) Proceedings first international symposium on nitrogen fixation. Washington University Press, PullmanGoogle Scholar
  81. Smolander A, Sarsa M-L (1990) Strains of soil under Betula pendula: behaviour in soil and pure culture. Plant Soil 122:129–136Google Scholar
  82. Stacey G, Libault M, Brechenmacher L, Wan J, May G (2006) Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 9:110–121PubMedGoogle Scholar
  83. Stevens GA, Berry AM (1988) Cytokinin secretion by Frankia sp. HFPAr13 in defined medium. Plant Physiol 87:15–16PubMedCentralPubMedGoogle Scholar
  84. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962PubMedGoogle Scholar
  85. Svistoonoff S, Laplaze L, Auguy F, Runions CJ, Duponnois R, Haseloff J, Franche C, Bogusz D (2003) Cg12 expression is specifically linked to infection of root hairs and cortical cells during Casuarina glauca and Allocasuarina verticillata actinorhizal nodule development. Mol Plant Microbe Interact 16:600–607PubMedGoogle Scholar
  86. Svistoonoff S, Laplaze L, Liang J, Ribeiro A, Gouveia MC, Auguy F, Fevereiro P, Franche C, Bogusz D (2004) Infection-related activation of the Cg12 promoter is conserved between actinorhizal and legume-rhizobia root nodule symbiosis. Plant Physiol 136:3191–3197PubMedCentralPubMedGoogle Scholar
  87. Svistoonoff S, Gherbi H, Nambiar-Veetil M, Zhong C, Michalak Z, Laplaze L, Vaissayre V, Auguy F, Hocher V, Doumas P, Bonneau J, Bogusz D, Franche C (2010a) Contribution of transgenic Casuarinaceae to our knowledge of the actinorhizal symbioses. Symbiosis 50:3–11Google Scholar
  88. Svistoonoff S, Sy M-O, Diagne N, Barker D, Bogusz D, Franche C (2010b) Infection-specific activation of the Medicago truncatula Enod11 early nodulin gene promoter during actinorhizal root nodulation. Mol Plant Microbe Interact 23:740–747PubMedGoogle Scholar
  89. Swensen SM, Benson DR (2008) Evolution of actinorhizal host plants and Frankia endosymbionts. In: Pawlowski K, Newton WE (eds) Nitrogen fixation research: origins and progress, vol VI, Nitrogen-fixing Actinorhizal symbioses. Springer, Heidelberg, pp 73–104Google Scholar
  90. Sy M-O, Constans L, Obertello M, Geney C, Laplaze L, Auguy F, Hocher V, Bogusz D, Franche C (2006) Analysis of the expression pattern conferred by the PsEnod12B promoter from the early nodulin gene of Pisum sativum in transgenic actinorhizal trees of the Casuarinaceae family. Plant Soil 281:281–289Google Scholar
  91. Sy M-O, Hocher V, Gherbi H, Laplaze L, Auguy F, Bogusz D, Franche C (2007) The cell-cycle promoter cdc2aAt from Arabidopsis thaliana is induced in the lateral roots of the actinorhizal tree Allocasuarina verticillata during the early stages of the symbiotic interaction with Frankia. Physiol Plant 130:409–417Google Scholar
  92. Torrey JG, Tjepkema JD (1979) Symbiotic nitrogen fixation in actinomycete-nodulated plants. Bot Gaz 140(Suppl):i–iiGoogle Scholar
  93. Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623PubMedCentralPubMedGoogle Scholar
  94. Valdes M (2008) Frankia ecology. In: Pawlowski K, Newton WE (eds) Nitrogen fixation research: origins and progress, vol VI, Nitrogen-fixing actinorhizal symbioses. Springer, Heidelberg, pp 49–72Google Scholar
  95. Valverde C, Wall LG (1999) Time course of nodule development in Discaria trinervis (Rhamnaceae) – Frankia symbiosis. New Phytol 141:345–354Google Scholar
  96. van Ghelue M, Lovaas E, Ringo E, Solheim B (1997) Early interaction between Alnus glutinosa and Frankia strain Arl3. Production and specificity of root hair deformation factors. Physiol Plant 99:579–587Google Scholar
  97. Vessey JK, Pawlowski K, Bergman B (2005) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads. Plant Soil 274:51–78Google Scholar
  98. Vijn I, Christiansen H, Lauridsen P, Kardailsky I, Quandt H-J, Broer II, Drenth J, Ostergaard E, van Kammen A, Bisseling T (1995) A 200 bp region of the pea ENOD12 promoter is sufficient for nodule-specific and nod factor induced expression. Plant Mol Biol 28:1103–1110PubMedGoogle Scholar
  99. Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182PubMedGoogle Scholar
  100. Wall LG, Berry AM (2008) Early interactions, infection and nodulation in actinorhizal symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, The Netherlands, pp 147–166Google Scholar
  101. Wan X, Hontelez J, Lillo A, Guarnerio C, van de Peut D, Fedorova E, Bisseling T, Franssen H (2007) Medicago truncatula ENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development. J Exp Bot 58:2033–2041PubMedGoogle Scholar
  102. Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, De Pamphilis CW, Ma H (2004) Genomic wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 135:1084–1099PubMedCentralPubMedGoogle Scholar
  103. Wheeler CT, Henson IE (1979) Hormones in plants bearing actinomycete nodules. Bot Gaz 140:52–57Google Scholar
  104. Wheeler CT, Crozier A, Sandberg G (1984) The biosynthesis of indole-3 acetic acid by Frankia. Plant Soil 78:99–104Google Scholar
  105. Xu XD, Kong RQ, de Bruijn FJ, He SY, Murry MA, Newman T, Wolk P (2002) DNA sequence and genetic characterization of plasmid pFQ11 from Frankia alni strain CpI1. FEMS Microbiol Lett 207:103–107PubMedGoogle Scholar
  106. Zhong C, Zhang Y, Chen Y, Jiang Q, Chen Z, Liang J, Pinyopusarek K, Franche C, Bogusz D (2010) Casuarina research and applications in China. Symbiosis 50:107–114Google Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Equipe RhizogénèseUMR DIADE, Institut de Recherche pour le DéveloppementMontpellier Cedex 5France

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