Skip to main content
SpringerLink
Log in

Induction of Actinorhizal Nodules by Frankia

  • Chapter
  • First Online:
Prokaryotic Symbionts in Plants

Part of the book series: Microbiology Monographs ((MICROMONO,volume 8))

Abstract

Actinomycetous soil bacteria of the genus Frankia can induce the formation of nitrogen-fixing root nodules on a diverse group of host plants from eight angiosperm families, collectively called actinorhizal plants. Nodule induction involves the colonization of the root surface, followed by the elicitation of changes in the plant that lead to nodule primordium formation and to the entry of bacteria into the root. Like in legume–rhizobia symbioses, bacteria can enter the plant root either intracellularly through a curled root hair, or intercellularly without root hair involvement, and the entry mechanism is determined by the host plant species. Mature actinorhizal nodules are coralloid structures consisting of multiple nodule lobes each of which represents a modified lateral root without root cap, a superficial periderm, and infected cells in the expanded cortex. In this review, an overview of infection mechanisms and nodule structure is given; comparisons with the corresponding mechanisms in legume symbioses are presented. Recent results on the perception of bacterial signal factors are described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lévy J, Debellé F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    Article  PubMed  CAS  Google Scholar 

  • Armstrong W, Armstrong J (2005) Stem photosynthesis not pressurized ventilation is responsible for light-enhanced oxygen supply to submerged roots of alder (Alnus glutinosa). Ann Bot 96:591–612

    Article  PubMed  CAS  Google Scholar 

  • Arnone JA, Kohls SJ, Baker DD (1994) Nitrate effects on nodulation and nitrogenase activity of actinorhizal Casuarina studied in split root systems. Soil Biol Biochem 26:599–606

    Article  CAS  Google Scholar 

  • Baker A, Parsons R (1997) Evidence for N feedback regulation of N2 fixation in Alnus glutinosa L. J Exp Bot 48:67–73

    Article  CAS  Google Scholar 

  • Baker DD (1987) Relationships among pure cultured strains of Frankia based on host specificity. Physiol Plant 70:245–248

    Article  Google Scholar 

  • Baker DD, Mullin BC (1992) Actinorhizal symbioses. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 259–292

    Google Scholar 

  • Batzli JM, Dawson JO (1999) Development of flood-induced lenticels in red alder nodules prior to the restoration of nitrogenase activity. Can J Bot 77:1373–1377

    Article  CAS  Google Scholar 

  • Benson DR, Clawson ML (2000) Evolution of the actinorhizal plant symbiosis. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for analysis of a biological process. Horizon Scientific, Symondham, pp 207–224

    Google Scholar 

  • Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–319

    PubMed  CAS  Google Scholar 

  • Benson DR, Vanden Heuvel BD, Potter D (2004) Actinorhizal symbioses: diversity and biogeography. In: Gillings M (ed) Plant microbiology. BIOS Scientific, Oxford, pp 97–127

    Google Scholar 

  • Berg RH (1999) Frankia forms infection threads. Can J Bot 77:1327–1333

    Article  Google Scholar 

  • Berg RH, McDowell L (1987) Endophyte differentiation in Casuarina actinorhizae. Protoplasma 136:104–117

    Article  Google Scholar 

  • Berg RH, McDowell L (1988) Cytochemistry of the wall of infected cells in Casuarina actinorhizae. Can J Bot 66:2038–2047

    Google Scholar 

  • Berry A, Harriott O, Moreau R, Osman S, Benson D, Jones A (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 90:6091–6094

    Article  PubMed  CAS  Google Scholar 

  • Berry AM, McCully ME (1990) Callose-containing deposits in relation to root-hair infections of Alnus rubra by Frankia. Can J Bot 68:798–802

    Article  Google Scholar 

  • Berry AM, Sunell 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 61–81

    Google Scholar 

  • Berry AM, Torrey JG (1983) Root hair deformation in the infection process of Alnus rubra. Can J Bot 61:2863–2876

    Article  Google Scholar 

  • Berry AM, McIntyre L, McCully ME (1986) Fine structure of root hair infection leading to nodulation in the Frankia–Alnus symbiosis. Can J Bot 64:292–305

    Article  Google Scholar 

  • Berry AM, Rasmussen U, Bateman K, Huss-Danell K, Lindwall S, Bergman B (2002) Arabinogalactan proteins are expressed at the symbiotic interface in root nodules of Alnus spp. New Phytol 155:469–479

    Article  CAS  Google Scholar 

  • Bolaños L, Brewin NJ, Bonilla I (1996) Effects of boron on Rhizobium–legume cell–surface interactions and nodule development. Plant Physiol 110:1249–1256

    PubMed  Google Scholar 

  • Bolaños L, Redondo-Nieto M, Bonilla I, Wall LG (2002) Boron requirement for growth, nitrogen fixation and nodulation of Frankia BCU110501. Physiol Plant 115:563–570

    Article  PubMed  Google Scholar 

  • Bosco M, Fernandez MP, Simonet P, Materassi R, Normand P (1992) Evidence that some Frankia sp. strains are able to cross boundaries between Alnus and Elaeagnus host specificity groups. Appl Environ Microbiol 58:1569–1576

    PubMed  CAS  Google Scholar 

  • Burggraaf AJP, Van der Linden J, Tak T (1983) Studies on the localization of infectible cells on Alnus glutinosa roots. Plant Soil 74:175–188

    Article  Google Scholar 

  • Caetano-Anollès G, Gresshoff PM (1991) Plant genetic control of nodulation. Annu Rev Microbiol 45:345–382

    Article  PubMed  Google Scholar 

  • Callaham D, Torrey JG (1977) Prenodule formation and primary nodule development in roots of Comptonia (Myricaceae). Can J Bot 55:2306–2318

    Article  Google Scholar 

  • 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 (Suppl) 140:S1–S9

    Article  Google Scholar 

  • Carroll BJ, McNeil DL, Gresshoff PM (1985) A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiol 78:34–40

    Article  PubMed  CAS  Google Scholar 

  • Céremonie H, Debelle F, Fernandez MP (1999) Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can J Bot 77:1293–1301

    Article  Google Scholar 

  • Chaia E, Raffaele E (2000) Spatial patterns of root branching and actinorhizal nodulation in Discaria trinervis seedlings. Symbiosis 29:329–341

    Google Scholar 

  • Clawson ML, Benson DR (1999) Natural diversity of Frankia strains in actinorhizal root nodules from promiscuous hosts in the family Myricaceae. Appl Environ Microbiol 65:4521–4527

    PubMed  CAS  Google Scholar 

  • Clawson ML, Carú M, Benson DR (1998) Diversity of Frankia strains in root nodules of plants from the families Elaeagnaceae and Rhamnaceae. Appl Environ Microbiol 64:3539–3543

    PubMed  CAS  Google Scholar 

  • Cooper JB, Long SR (1994) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6:215–225

    Article  PubMed  CAS  Google Scholar 

  • Dobritsa SV, Novik SN (1992) Feedback regulation of nodule formation in Hippophaë rhamnoides. Plant Soil 144:45–50

    Article  Google Scholar 

  • Doyle JJ (1998) Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3:473–478

    Article  Google Scholar 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    Article  PubMed  CAS  Google Scholar 

  • Fleischer A, Titel C, Ehwald R (1998) The boron requirement and cell wall properties of growing and stationary suspension-cultured Chenopodium album L. cells. Plant Physiol 117:1401–1410

    Article  PubMed  CAS  Google Scholar 

  • Fleming AI, Wittenberg JB, Wittenberg BA, Dudman WF, Appleby CA (1987) The purification, characterization and ligand-binding kinetics of hemoglobins from root nodules of the nonleguminous Casuarina glauca—Frankia symbiosis. Biochim Biophys Acta 911:209–220

    Article  CAS  Google Scholar 

  • Fontaine MS, Lancelle SA, Torrey JG (1984) Initiation and ontogeny of vesicles in cultured Frankia sp. strain HFPArI3. J Bacteriol 160:921–927

    PubMed  CAS  Google Scholar 

  • Frühling M, Hohnjec N, Schröder G, Küster H, Pühler A, Perlick AM (2000) Genomic organization and expression properties of the VfENOD5 gene from broad bean (Vicia faba L.). Plant Sci 155:169–178

    Article  PubMed  Google Scholar 

  • Gauthier D, Jaffre T, Prin Y (1999) Occurrence of both Casuarina-infective and Elaeagnus-infective Frankia strains within actinorhizae of Casuarina collina, endemic to New Caledonia. Eur J Soil Biol 35:9–15

    Article  Google Scholar 

  • Gentili F, Huss-Danell K (2002) Phosphorus modifies the effects of nitrogen on nodulation in split-root systems of Hippophaë rhamnoides. New Phytol 153:53–61

    Article  CAS  Google Scholar 

  • Gentili F, Huss-Danell K (2003) Local and systemic effects of phosphorus and nitrogen on nodulation and nodule function in Alnus incana. J Exp Bot 54:2757–2767

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Gherbi H, Duhoux E, Franche C, Pawlowski K, Berry AM, Bogusz D (1997) Cloning of a full-length symbiotic hemoglobin cDNA and in situ localization of the corresponding mRNA in Casuarina glauca root nodule. Physiol Plant 99:608–616

    Article  CAS  Google Scholar 

  • Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 105:4928–4932

    Article  PubMed  CAS  Google Scholar 

  • Greene EA, Erard M, Dedieu A, Barker DG (1998) MtENOD16 and 20 are members of a family of phytocyanin-related early nodulins. Plant Mol Biol 36:775–783

    Article  PubMed  CAS  Google Scholar 

  • Hafeez F, Akkermans ADL, Chaudhary AH (1984) Observations on the ultrastructure of Frankia sp. in root nodules of Datisca cannabina L. Plant Soil 79:383–402

    Article  Google Scholar 

  • Heckmann AB, Hebelstrup KH, Larsen K, Micaelo NM, Jensen EØ (2006) A single hemoglobin gene in Myrica gale retains both symbiotic and non-symbiotic specificity. Plant Mol Biol 61:769–779

    Article  PubMed  CAS  Google Scholar 

  • Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA 86:1244–1248

    Article  PubMed  CAS  Google Scholar 

  • Huang J-B, Zhao Z-Y, Chen G-X, Liu H-C (1985) Host range of Frankia endophytes. Plant Soil 87:61–65

    Article  Google Scholar 

  • Huguet V, Mergeay M, Cervantes E, Fernandez MP (2004) Diversity of Frankia strains associated to Myrica gale in Western Europe: impact of host plant (Myrica vs. Alnus) and of edaphic factors. Environ Microbiol 6:1032–1041

    Article  PubMed  CAS  Google Scholar 

  • Huguet V, Gouy M, Normand P, Zimpfer JF, Fernandez MP (2005) Molecular phylogeny of Myricaceae: a reexamination of host-symbiont specificity. Mol Phylogenet Evol 34:557–685

    Article  PubMed  CAS  Google Scholar 

  • Huss-Danell K, Bergman B (1990) Nitrogenase in Frankia from root nodules of Alnus incana (L.) Moench: immunolocalization of the Fe- and MoFe proteins during vesicle differentiation. New Phytol 116:443–455

    Article  Google Scholar 

  • Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531

    Article  PubMed  CAS  Google Scholar 

  • Israel DW (1993) Symbiotic dinitrogen fixation and host-plant growth during development of and recovery from phosphorus deficiency. Physiol Plant 88:294–300

    Article  CAS  Google Scholar 

  • Jacobsen-Lyon K, Jensen EØ, Jorgensen JE, Marcker KA, Peacock WJ, Dennis ES (1995) Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. Plant Cell 7:213–223

    Article  PubMed  CAS  Google Scholar 

  • Kistner D, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518

    Article  PubMed  CAS  Google Scholar 

  • Knowlton S, Berry AM, Torrey JG (1980) Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia. Can J Microbiol 26:971–977

    Article  PubMed  CAS  Google Scholar 

  • Kohls SJ, Baker DD (1989) Effects of substrate nitrate concentration on symbiotic nodule formation in actinorhizal plants. Plant Soil 118:171–179

    Article  CAS  Google Scholar 

  • Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426

    Article  PubMed  CAS  Google Scholar 

  • Lalonde M (1979) Techniques and observations of the nitrogen fixing Alnus root nodule symbiosis. In: Subba Rao NS (ed) Recent advances in biological nitrogen fixation. Oxford University Press and IBH, New Delhi, pp 421–434

    Google Scholar 

  • 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 13:107–112

    Article  PubMed  CAS  Google Scholar 

  • 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 13:113–117

    Article  PubMed  CAS  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 

  • Ligero F, Caba JM, Lluch C, Olivares J (1991) Nitrate inhibition of nodulation can be overcome by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiol 97:1221–1225

    Article  PubMed  CAS  Google Scholar 

  • Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–633

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Berry AM (1991a) The infection process and nodule initiation in the Frankia–Ceanothus root nodule symbiosis: a structural and histochemical study. Protoplasma 163:82–92

    Article  Google Scholar 

  • Liu Q, Berry AM (1991b) Localization and characterization of pectic polysaccharides in roots and root nodules of Ceanothus spp. during intercellular infection by Frankia. Protoplasma 164:93–101

    Article  Google Scholar 

  • Lumini E, Bosco M, Fernandez MP (1996) PCR-RFLP and total DNA homology revealed three related genomic species among broad-host-range Frankia strains. FEMS Microbiol Ecol 21:303–311

    Article  CAS  Google Scholar 

  • Maggia L, Bousquet J (1994) Molecular phylogeny of the actinorhizal Hamamelidae and relationships with host promiscuity toward Frankia. Mol Ecol 3:459–467

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic M (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34

    Article  PubMed  CAS  Google Scholar 

  • McConnell JT, Bond G (1957) A comparison of the effects of combined nitrogen on nodulation in non-legumes and legumes. Plant Soil 8:378–386

    Article  Google Scholar 

  • Miller IM, Baker DD (1986) The initiation development and structure of root nodules in Elaeagnus angustifolia (Elaeagnaceae). Protoplasma 128:107–119

    Article  Google Scholar 

  • Mirza MS, Hahn D, Akkermans ADL (1992) Isolation and characterization of Frankia strains from Coriaria nepalensis. Syst Appl Microbiol 15:289–295

    Google Scholar 

  • Mirza S, Pawlowski K, Hafeez FY, Chaudhary AH, Akkermans ADL (1994) Ultrastructure of the endophyte and localization of nifH transcripts in root nodules of Coriaria nepalensis Wall. by in situ hybridization. New Phytol 126:131–136

    Article  Google Scholar 

  • Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104

    Article  PubMed  CAS  Google Scholar 

  • Navarro E, Jaffre T, Gauthier D, Gourbiere F, Rinaudo G, Simonet P, Normand P (1999) Distribution of Gymnostoma spp. microsymbiotic Frankia strains in New Caledonia is related to soil type and to host-plant species. Mol Ecol 8:1781–1788

    Article  PubMed  Google Scholar 

  • Navarro E, Nalin R, Gauthier D, Normand P (1997) The nodular microsymbionts of Gymnostoma spp. are Elaeagnus-infective Frankia strains. Appl Environ Microbiol 63:1610–1616

    PubMed  CAS  Google Scholar 

  • Newcomb W, Pankhurst CE (1982) Fine structure of actinorhizal nodules of Coriaria arborea (Coriariaceae). NZJ Bot 20:93–103

    Google Scholar 

  • Nishimura R, Hayashi M, Wu G-J, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429

    Article  PubMed  CAS  Google Scholar 

  • 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, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15

    Article  PubMed  Google Scholar 

  • Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328

    Article  PubMed  CAS  Google Scholar 

  • Parsons R, Silvester WB, Harris S, Gruijters WTM, Bullivant S (1987) Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase. Plant Physiol 83:728–731

    Article  PubMed  CAS  Google Scholar 

  • Parsons R, Stanforth A, Raven JA, Sprent JI (1993) Nodule growth and activity may be regulated by a feedback mechanism involving phloem nitrogen. Plant Cell Environ 16:125–136

    Article  CAS  Google Scholar 

  • Pathirana SM, Tjepkema JD (1995) Purification of hemoglobin from the actinorhizal root nodules of Myrica gale L. Plant Physiol 107:827–831

    PubMed  CAS  Google Scholar 

  • Pawlowski K (2008) Nodules and oxygen. Plant Biotechnol 25:291–298

    CAS  Google Scholar 

  • Pawlowski K, Twigg P, Dobritsa S, Guan C, Mullin BC (1997) A nodule-specific gene family from Alnus glutinosa encodes glycine- and histidine-rich proteins expressed in the early stages of actinorhizal nodule development. Mol Plant Microbe Interact 10:656–664

    Article  PubMed  CAS  Google Scholar 

  • Pawlowski K, Swensen S, Guan C, Hadri A-E, Berry AM, Bisseling T (2003) Distinct patterns of symbiosis-related gene expression in actinorhizal nodules from different plant families. Mol Plant Microbe Interact 16:796–807

    Article  PubMed  CAS  Google Scholar 

  • Pawlowski K, Jacobsen KR, Alloisio N, Ford Denison R, Klein M, Tjepkema JD, Winzer T, Sirrenberg A, Guan C, Berry AM (2007) Truncated hemoglobins in actinorhizal nodules of Datisca glomerata. Plant Biol 9:776–785

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Peters NK, Crist-Estes DK (1989) Nodule formation is stimulated by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiol 91:690–693

    Article  PubMed  CAS  Google Scholar 

  • Pizelle G (1965) L'azote minéral et la nodulation de l'aune glutineux (Alnus glutinosa). Observations sur des plantes cultivées avec systémes racinaires compartimentés. Bulletin de l'Ecole Nationale Supérieure Agronomique 7:55–63

    Google Scholar 

  • Pizelle G (1966) L'azote minéral et la nodulation de l'aune glutineux (Alnus glutinosa). II. Observations sur l'action inhibitrice de l'azote minéral a l'égard de la nodulation. Ann Inst Pasteur (Paris) 111:259–264

    Google Scholar 

  • Pommer EH (1956) Beiträge zur Anatomie und Biologie der Wurzelknöllchen von Alnus glutinosa (L.) Gaertn. Flora 143:603–634

    Google Scholar 

  • Prayitno J, Rolfe BG, Mathesius U (2006) The ethylene insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiol 142:168–180

    Article  PubMed  CAS  Google Scholar 

  • Racette S, Torrey JG (1989) Root nodule initiation in Gymnostoma (Casuarinaceae) and Shephardia (Elaeagnaceae) induced by Frankia strain HFPGpI1. Can J Bot 67:2873–2879

    Article  Google Scholar 

  • Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592

    Article  PubMed  CAS  Google Scholar 

  • Ramirez-Saad H, Janse JD, Akkermans ADL (1998) Root nodules of Ceanothus caeruleus contain both the N2-fixing Frankia endophyte and a phylogenetically related Nod−/Fix− actinomycete. Can J Microbiol 44:140–148

    Article  CAS  Google Scholar 

  • Reddell P, Yun Y, Shipton WA (1997) Do Casuarina cunninghamiana seedlings dependent on symbiotic N2 fixation have higher phosphorus requirements than those supplied with adequate fertilizer nitrogen? Plant Soil 189:213–219

    Article  CAS  Google Scholar 

  • Redondo-Nieto M, Rivilla R, El-Hamdaoui A, Bonilla I, Bolaños L (2001) Boron deficiency affects early infection events in the pea–Rhizobium symbiotic interaction. Aust J Plant Physiol 28:819–823

    Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro A, Akkermans AD, van Kammen A, Bisseling T, Pawlowski K (1995) A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7:785–794

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Barrueco C, de Castro FB (1973) Cytokinin-induced pseudonodules on Alnus glutinosa. Physiol Plant 29:227–280

    Article  Google Scholar 

  • Santi C (2003) Approche moléculaire de la mise en place du nodule actinorhiyien chez les arbres tropicaux de la famille des Casuarinaceae. PhD dissertation, Université Montpellier II

    Google Scholar 

  • Sasakawa H, Hiyoshi T, Sugiyama T (1988) Immuno-gold localization of nitrogenase in root nodules of Elaeagnus pungens Thunb. Plant Cell Physiol 29:1147–1152

    CAS  Google Scholar 

  • Sasakura F, Uchiumi T, Shimoda Y, Suzuki A, Takenouchi K, Higashi S, Abe M (2006) A class 1 hemoglobin gene from Alnus firma functions in symbiotic and nonsymbiotic tissues to detoxify nitric oxide. Mol Plant Microbe Interact 19:441–450

    Article  PubMed  CAS  Google Scholar 

  • Scheidle H, Gross A, Niehaus K (2005) The lipid A substructure of the Sinorhizobium meliloti lipopolysaccharides is sufficient to suppress the oxidative burst in host plants. New Phytol 165:559–565

    Article  PubMed  CAS  Google Scholar 

  • Scheres B, Van Engelen F, Van der Knap E, Van de Wiel C, Van Kammen A, Bisseling T (1990) Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 2:687–700

    Article  PubMed  CAS  Google Scholar 

  • Schmidt JS, Harper JE, Hoffman TK, Bent AF (1999) Regulation of soybean nodulation independent of ethylene signaling. Plant Physiol 119:951–960

    Article  PubMed  CAS  Google Scholar 

  • Schnabel E, Journet EP, De Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58:809–822

    Article  PubMed  CAS  Google Scholar 

  • Schröder P (1989) Aeration of the root system in Alnus glutinosa L. Gaertn. Ann Sci Forest 46:310–314

    Article  Google Scholar 

  • Schwintzer CR, Berry AM, Disney LD (1982) Seasonal patterns of root nodule growth, endophyte morphology, nitrogenase activity, and shoot development in Myrica gale. Can J Bot 60:746–757

    Article  Google Scholar 

  • Sequerra J, Capellano A, Faure-Raynard M, Moiroud A (1994) Root hair infection process and myconodule formation of Alnus incana by Penicillium nodositatum. Can J Bot 72:955–962

    Article  Google Scholar 

  • Sequerra J, Capellano A, Gianinazzi-Pearson V, Moiroud A (1995) Ultrastructure of cortical root cells of Alnus incana infected by Penicillium nodositatum. New Phytol 130:545–555

    Article  Google Scholar 

  • Silvester WB, Silvester JK, Torrey JG (1988a) Adaptation of nitrogenase to varying oxygen tension and the role of the vesicle in root nodules of Alnus incana ssp. rugosa. Can J Bot 66:1772–1779

    Google Scholar 

  • Silvester WB, Whitbeck J, Silvester JK, Torrey JG (1988b) Growth, nodule morphology and nitrogenase activity of Myrica gale grown with roots at various oxygen levels. Can J Bot 66:1762–1771

    Google Scholar 

  • Silvester WB, Harris SL, Tjepkema JD (1990) Oxygen regulation and hemoglobin. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, New York, pp 157–176

    Google Scholar 

  • Silvester WB, Langenstein B, Berg RH (1999) Do mitochondria provide the oxygen diffusion barrier in root nodules of Coriaria and Datisca? Can J Bot 77:1358–1366

    Article  Google Scholar 

  • Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92:2647–2651

    Article  PubMed  CAS  Google Scholar 

  • Stokkermans TJW, Peters NK (1994) Bradyrhizobium elkanii lipooligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc. Planta 193:413–420

    Article  PubMed  CAS  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 417:959–9562

    Article  PubMed  CAS  Google Scholar 

  • Suharjo UKJ, Tjepkema JD (1995) Occurence of hemoglobin in the nitrogen-fixing root nodules of Alnus glutinosa. Physiol Plant 95:247–252

    Article  CAS  Google Scholar 

  • Swensen SM (1996) The evolution of actinorhizal symbioses—evidence for multiple origins of the symbiotic association. Am J Bot 83:1503–1512

    Article  Google Scholar 

  • Swensen SM, Mullin BC (1997) Phylogenetic relationships among actinorhizal plants. The impact of molecular systematics and implications for the evolution of actinorhizal symbioses. Physiol Plant 99:565–573

    Article  CAS  Google Scholar 

  • Tellström V, Usadel B, Thimm O, Stitt M, Küster H, Niehaus K (2007) The lipopolysaccharide of Sinorhizobium meliloti suppresses defense-associated gene expression in cell cultures of the host plant Medicago truncatula. Plant Physiol 143:825–837

    Article  PubMed  CAS  Google Scholar 

  • Thomas KA, Berry AM (1989) Effects of continuous nitrogen application and nitrogen preconditioning on nodulation and growth of Ceanothus griseus var. horizontalis. Plant Soil 118:181–187

    Article  Google Scholar 

  • Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107

    Article  PubMed  CAS  Google Scholar 

  • Tjepkema JD (1978) The role of oxygen diffusion from the shoots and the nodule roots in nitrogen fixation by root nodules of Myrica gale. Can J Bot 56:1365–1371

    Article  CAS  Google Scholar 

  • Torrey JG (1990) Cross-inoculation groups within Frankia. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, New York, pp 83–106

    Google Scholar 

  • Truchet G, Roche P, Lerouge P, Vasse J, Camut S, De Billy F, Promé JC, Dénarié J (1991) Sulfated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351:670–673

    Article  CAS  Google Scholar 

  • Valverde C, Wall LG (1999a) Time course of nodule development in the Discaria trinervis (Rhamnaceae)–Frankia symbiosis. New Phytol 141:345–354

    Article  Google Scholar 

  • Valverde C, Wall LG (1999b) Regulation of nodulation in Discaria trinervis (Rhamnaceae)–Frankia symbiosis. Can J Bot 77:1302–1310

    Article  Google Scholar 

  • Valverde C, Wall LG (2003) The regulation of nodulation, nitrogen fixation and ammonium assimilation under a carbohydrate shortage stress in the Discaria trinervis–Frankia symbiosis. Plant Soil 254:155–165

    Article  CAS  Google Scholar 

  • Valverde C, Wall LG (2005) Ethylene modulates the susceptibility of the root for nodulation in actinorhizal Discaria trinervis. Physiol Plant 124:121–131

    Article  CAS  Google Scholar 

  • Valverde C, Ferrari A, Wall LG (2002) Phosphorus and the regulation of nodulation in the actinorhizal symbiosis between Discaria trinervis (Rhamnaceae) and Frankia BCU110501. New Phytol 153:43–52

    Article  CAS  Google Scholar 

  • Van Brussel AAN, Bakhuizen R, Van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJJ (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257:70–71

    Article  PubMed  Google Scholar 

  • Van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiol 140:1494–506

    Article  PubMed  CAS  Google Scholar 

  • Vanden Heuvel BD, Benson DR, Bortiri E, Potter D (2004) Low genetic diversity among Frankia spp. strains nodulating sympatric populations of actinorhizal species of Rosaceae, Ceanothus (Rhamnaceae) and Datisca glomerata (Datiscaceae) west of the Sierra Nevada (California). Can J Microbiol 50:989–1000

    Article  PubMed  CAS  Google Scholar 

  • Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182

    PubMed  CAS  Google Scholar 

  • Wall LG, Huss-Danell K (1997) Regulation of nodulation in Alnus-Frankia symbiosis. Physiol Plant 99:594–600

    Article  CAS  Google Scholar 

  • Wall LG, Hellsten A, Huss-Danell K (2000) Nitrogen, phosphorus, and the ratio between them affect nodulation in Alnus incana and Trifolium pratense. Symbiosis 29:91–105

    Google Scholar 

  • Wall LG, Valverde C, Huss-Danell K (2003) Regulation of nodulation in the absence of N2 is different in actinorhizal plants with different infection pathways. J Exp Bot 54:1253–1258

    Article  PubMed  CAS  Google Scholar 

  • Wheeler CT, Gordon JC, Ching TM (1979) Oxygen relations of the root nodules of Alnus rubra Bong. New Phytol 82:449–457

    Article  CAS  Google Scholar 

  • Wheeler CT, Watts SH, Hillman JR (1983) Changes in carbohydrates and nitrogenous compounds in the root nodules of Alnus glutinosa in relation to dormancy. New Phytol 95:209–218

    Article  CAS  Google Scholar 

  • Wopereis J, Pajuelo E, Dazzo FB, Jiang Q, Gresshoff PM, De Bruijn FJ, Stougaard J, Szczyglowski K (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 23:97–114

    Article  PubMed  CAS  Google Scholar 

  • Yang W-C, de Blank C, Meskiene I, Hirt H, Bakker J, van Kammen A, Franssen H, Bisseling T (1994) Rhizobium Nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell 6:1415–1426

    Article  PubMed  CAS  Google Scholar 

  • Yang Y (1995) The effect of phosphorus on nodule formation and function in the Casuarina–Frankia symbiosis. Plant Soil 176:161–169

    Article  CAS  Google Scholar 

  • Yang Y, Shipton WA, Reddel P (1997) Effects of phosphorus supply on in vitro growth and phosphatase activity of Frankia isolates from Casuarina. Plant Soil 189:75–79

    Article  CAS  Google Scholar 

  • Zhang Z, Torrey JG (1985) Studies of an effective strain of Frankia from Allocasuarina lehmanniana of the Casuarinaceae. Plant Soil 97:1–16

    Google Scholar 

  • Zhang Z, Lopez MF, Torrey JG (1984) A comparison of cultural characteristics and infectivity of Frankia isolates from root nodules of Casuarina species. Plant Soil 78:79–90

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, Stockholm University, 10691, Stockholm, Sweden

    Katharina Pawlowski

Authors
  1. Katharina Pawlowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katharina Pawlowski .

Editor information

Katharina Pawlowski

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Pawlowski, K. (2008). Induction of Actinorhizal Nodules by Frankia . In: Pawlowski, K. (eds) Prokaryotic Symbionts in Plants. Microbiology Monographs, vol 8. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2008_123

Download citation

Publish with us

Policies and ethics

Search

Navigation