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The diversity of actinorhizal symbiosis

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Abstract

Filamentous aerobic soil actinobacteria of the genus Frankia can induce the formation of nitrogen-fixing nodules on the roots of a diverse group of plants from eight dicotyledonous families, collectively called actinorhizal plants. Within nodules, Frankia can fix nitrogen while being hosted inside plant cells. Like in legume/rhizobia symbioses, bacteria can enter the plant root either intracellularly through an infection thread formed in a curled root hair, or intercellularly without root hair involvement, and the entry mechanism is determined by the host plant species. Nodule primordium formation is induced in the root pericycle as for lateral root primordia. Mature actinorhizal nodules are coralloid structures consisting of multiple lobes, each of which represents a modified lateral root without a root cap, a superficial periderm and with infected cells in the expanded cortex. In this review, an overview of nodule induction mechanisms and nodule structure is presented including comparisons with the corresponding mechanisms in legume symbioses.

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References

  • Arnholdt-Schmitt B (1999) On the physiology of yield production in carrots.—Implications for breeding towards nutrient efficiency. Gartenbauwissenschaft 64:26–32

    Google Scholar 

  • Arrighi J-F, Barre A, Ben Amor B, Bersoult A, Campos Soriano L, Mirabella R, de Carvalho-Niebel F, Journet E-P, Ghérardi M, Huguet T, Geurts R, Dénarié J, Rougé P, Gough C (2006) The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142:265–27

    Article  PubMed  CAS  Google Scholar 

  • Bassett B, Goodman RN, Novacky A (1977) Ultrastructure of soybean nodules. I: release of rhizobia from the infection thread. Can J Microbiol 23:573–582

    Article  PubMed  CAS  Google Scholar 

  • Beauchemin NJ, Furnholm T, Lavenus J, Svistoonoff S, Doumas P, Bogusz D, Laplaze L, Tisa LS (2012) Casuarina root exudates alter the physiology, surface properties, and plant infectivity of Frankia sp. strain CcI3. Appl Environ Microbiol 78:575–580

    Article  PubMed  CAS  Google Scholar 

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

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

    PubMed  CAS  Google Scholar 

  • Berg RH (1990) Cellulose and xylans in the interface capsule in symbiotic cells of actinorhizae. Protoplasma 159:35–43

    Article  CAS  Google Scholar 

  • Berg RH (1999a) Cytoplasmic bridge formation in the nodule apex of actinorhizal root nodules. Can J Bot 77:1351–1357

    Google Scholar 

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

    Google Scholar 

  • Berg RH, Langenstein B, Silvester WB (1999) Development in the Datisca-Coriaria nodule type. Can J Bot 77:1334–1350

    Google Scholar 

  • Bergman B, Johansson C, Söderbäck E (1992) The Nostoc–Gunnera symbiosis. New Phytol 122:379–400

    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 Press, San Diego, 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, 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 90:6091–6094

    Article  PubMed  CAS  Google Scholar 

  • Berry AM, Mendoza-Herrera A, Guo Y-Y, Hayashi J, Persson T, Barabote R, Demchenko K, Zhang S, Pawlowski K (2011) New perspectives on nodule nitrogen assimilation in actinorhizal symbioses. Funct Plant Biol 38:645–652

    Article  CAS  Google Scholar 

  • Boisson-Dernier A, Andriankaja A, Chabaud M, Niebel A, Journet EP, Barker DG, de Carvalho-Niebel F (2005) MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Mol Plant Microbe Interact 18:1269–1276

    Article  PubMed  CAS  Google Scholar 

  • Bonaldi K, Gourion B, Fardoux J, Hannibal L, Cartieaux F, Boursot M, Vallenet D, Chaintreuil C, Prin Y, Nouwen N, Giraud E (2010) Large-scale transposon mutagenesis of photosynthetic Bradyrhizobium sp. strain ORS278 reveals new genetic loci putatively important for nod-independent symbiosis with Aeschynomene indica. Mol Plant Microbe Interact 23:760–770

    Article  PubMed  CAS  Google Scholar 

  • Bonaldi K, Gargani D, Prin Y, Fardoux J, Gully D, Nouwen N, Goormachtig S, Giraud E (2011) Nodulation of Aeschynomene afraspera and A. indica by photosynthetic Bradyrhizobium sp. strain ORS285: the nod-dependent versus the nod-independent symbiotic interaction. Mol Plant Microbe Interact 24:1359–1371

    Article  PubMed  CAS  Google Scholar 

  • Callaham D, Torrey JG (1977) Prenodulae formation and primary nodule development in roots of Comptonia (Myricaceae). Can J Bot 51:2306–2318

    Article  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

    Google Scholar 

  • Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272

    Article  PubMed  CAS  Google Scholar 

  • Demchenko KN, Demchenko NP (2001) Changes of root structure in connection with the development of lateral root primordia in wheat and pumpkins. In: Recent advances of plant root structure and function: proceedings of the 5th International Symposium on Structure and Function of Roots; Stara Lesna, Slovakia, Slovakia, 1998. Gasparikova O, Ciamporova M, Mistrik I, Baluska F (eds), Developments in plant and soil sciences, Kluwer. Vol 90: 39–47

  • Den Herder J, Vanhee C, De Rycke R, Corich V, Holsters M, Goormachtig S (2007) Nod factor perception during infection thread growth fine-tunes nodulation. Mol Plant Microbe Interact 20:129–137

    Article  CAS  Google Scholar 

  • D’Haeze W, Gao M, De Rycke R, Van Montagu M, Engler G, Holsters M (1998) Roles for azorhizobial Nod factors and surface polysaccharides in intercellular invasion and nodule penetration, respectively. Mol Plant-Microbe Interact 11:999–1008

    Article  Google Scholar 

  • Doyle JJ (2011) Phylogenetic perspectives on the origins of nodulation. Mol Plant Microbe Interact 24:1289–1295

    Article  PubMed  CAS  Google Scholar 

  • Duhoux E, Rinaudo G, Diem HG, Auguy F, Fernandez D, Bogusz D, Franche C, Dommergues Y, Huguenin B (2001) Angiosperm Gymnostoma trees produce root nodules colonized by arbuscular mycorrhizal fungi related to Glomus. New Phytol 149:115–125

    Article  Google Scholar 

  • Fedorova EE, Zhiznevskaya GY, Kalibernaya ZV, Artemenko EN, Izmailov SF, Gus’kov AV (2000) IAA metabolism during development of symbiosis between Phaseolus vulgaris and Rhizobium phaseoli. Russ J Plant Physiol 47:203–206

    CAS  Google Scholar 

  • Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72

    Article  CAS  Google Scholar 

  • Franche C, Diouf D, Laplaze L, Auguy F, Frutz T, Rio M, Duhoux E, Bogusz D (1998) Soybean (lbc3), Parasponia, and Trema hemoglobin gene promoters retain symbiotic and nonsymbiotic specificity in transgenic Casuarinaceae: implications for hemoglobin gene evolution and root nodule symbioses. Mol Plant-Microbe Interact 11:887–894

    Article  CAS  Google Scholar 

  • Gabbarini LA, Wall LG (2008) Analysis of nodulation kinetics in Frankia-Discaria trinervis symbiosis reveals different factors involved in the nodulation process. Physiol Plant 133:776–785

    Article  PubMed  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 

  • Gilbert GA, Knight JD, Vance CP, Allan DL (2000) Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Ann Bot 85:921–928

    Article  CAS  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, Verméglio A, Médigue C, Sadowsky M (2007) Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312

    Article  PubMed  Google Scholar 

  • Gough C, Cullimore J (2011) Lipo-chitooligosaccharide signaling in endosymbiotic plant–microbe interactions. Mol Plant Microbe Interact 24:867–878

    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 

  • Hammad Y, Nalin R, Marechal J, Fiasson K, Pepin R, Berry AM, Normand P, Domenach A-M (2003) A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia. Plant Soil 254:193–205

    Article  CAS  Google Scholar 

  • Heidstra R, Geurts R, Franssen H, Spaink HP, Kammen A, van Bisseling T (1994) Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol 105:787–797

    PubMed  CAS  Google Scholar 

  • Hocher 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 actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol 156:700–711

    Article  PubMed  CAS  Google Scholar 

  • Huss-Danell K (1997) Tansley Review No. 93. Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405

    Article  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 

  • Imanishi L, Vayssières A, Franche C, Bogusz D, Wall L, Svistoonoff S (2011) Transformed hairy roots of Discaria trinervis: a valuable tool for studying actinorhizal symbiosis in the context of intercellular infection. Mol Plant Microbe Interact 24:1317–1324

    Article  PubMed  CAS  Google Scholar 

  • Jacobsen-Lyon K, Østergaard-Jensen E, Jørgensen J-E, Marcker KA, Peacock J, Dennis E (1995) Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. Plant Cell 7:213–223

    PubMed  CAS  Google Scholar 

  • Jeong J, Suh SJ, Guan C, Tsay Y-F, Moran N, Oh CJ, An CS, Demchenko K, Pawlowski K, Lee Y (2004) A nodule-specific dicarboxylate transporter from Alnus glutinosa. Plant Physiol 134:969–978

    Article  PubMed  CAS  Google Scholar 

  • Joshi PA, Caetano-Anollés G, Graham ET, Gresshoff PM (1993) Ultrastructure of transfer cells in spontaneous nodules of alfalfa (Medicago sativa). Protoplasma 172:64–76

    Article  Google Scholar 

  • Knowlton S, Berry A, 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 

  • Lancelle SA, Torrey JG (1984a) Early development of Rhizobium-induced root nodules of Parasponia rigida. I. Infection and early nodule initiation. Protoplasma 123:26–37

    Article  Google Scholar 

  • Lancelle SA, Torrey JG (1984b) Early development of Rhizobium-induced root nodules of Parasponia rigida. II. Nodule morphogenesis and symbiotic development. Can J Bot 63:25–35

    Article  Google Scholar 

  • Landsberg EC (1996) Hormonal regulation of iron–stress response in sunflower roots: a morphological and cytological investigation. Protoplasma 194:69–80

    Article  CAS  Google Scholar 

  • Laplaze L, Duhoux E, Franche C, Frutz T, Svistoonoff S, Bisseling T, Bogusz D, Pawlowski K (2000) 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 

  • Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root meristems is a two stage process. Dev 121:3303–3310

    CAS  Google Scholar 

  • Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, Bisseling T, Geurts R (2005a) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102:10375–10380

    Article  PubMed  CAS  Google Scholar 

  • Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, Bisseling T, Geurts R (2005b) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102:10375–10380

    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 

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

    Article  PubMed  CAS  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 

  • Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14:77–86

    Article  PubMed  CAS  Google Scholar 

  • Mastronunzio JE, Tisa LS, Normand P, Benson DR (2008) Comparative secretome analysis suggests low plant cell wall degrading capacity in Frankia symbionts. BMC Genom 9:47

    Article  CAS  Google Scholar 

  • Miller IM, Baker DD (1985) The initiation development and structure of root nodules in Elaeagnus angustifolia (Elaeagnaceae). Protoplasma 128:107–119

    Article  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 

  • Moran NA (2003) Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6:512–518

    Article  PubMed  CAS  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 

  • Naisbitt T, James EK, Sprent JI (1992) The evolutionary significance of the legume genus Chamaecrista, as determined by nodule structure. New Phytol 122:487–492

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Newcomb WR, Wood S (1987) Morphogenesis and fine structure of Frankia (Actinomycetales): the microsymbiont of nitrogen-fixing actinorhizal root nodules. Int Rev Cytol 109:1–88

    Article  PubMed  CAS  Google Scholar 

  • Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra A (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Internat J Syst Bacteriol 46:1–9

    Article  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 

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

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju JS, Kudrna D, Wing R, Untergasser A, Bisseling T, Geurts R (2011) LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331:909–912

    Article  PubMed  CAS  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 

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

    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 

  • Pawlowski K (2002) Actinorhizal symbioses. In: Leigh GJ (ed) Nitrogen fixation at the millennium. Elsevier, Amsterdam

    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 

  • 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 144:1852–1862

    Article  PubMed  CAS  Google Scholar 

  • Perrine-Walker F, Doumas P, Lucas M, Vaissayre V, Beauchemin NJ, Band LR, Chopard J, Crabos A, Conejero G, Péret B, King JR, Verdeil JL, Hocher V, Franche C, Bennett MJ, Tisa LS, Laplaze L (2010) Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules. Plant Physiol 154:1372–1380

    Article  PubMed  CAS  Google Scholar 

  • Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P, Chertkov O, Teshima H, Bruce BC, Detter C, Tapia R, Han S, Han J, Woyke T, Pitluck S, Pennacchio L, Nolan M, Ivanova N, Pati A, Land ML, Pawlowski K, Berry AM (2011) The genome of Candidatus Frankia datiscae Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J Bacteriol 193:7017–7018

    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 

  • 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 Bot 44:140–148

    CAS  Google Scholar 

  • Roth LE, Stacey G (1989) Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49:13–23

    PubMed  CAS  Google Scholar 

  • Schlaman HRM, Horvath B, Vijgenboom E, Okker RJH, Lugtenberg BJJ (1991) Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. J Bacteriol 173:4277–4287

    PubMed  CAS  Google Scholar 

  • Schröder P (1989) Aeration of the root system in Alnus glutinosa L. Gaertn. Annales des Sciences Forestières 46:310–314

    Article  Google Scholar 

  • Schubert M, Koteyeva NK, Wabnitz PW, Santos P, Büttner M, Sauer N, Demchenko K, Pawlowski K (2011) Plasmodesmata distribution and sugar partitioning in nitrogen-fixing root nodules of Datisca glomerata. Planta 233:139–152

    Article  PubMed  CAS  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 

  • Séguin A, Lalonde M (1989) Detection of pectolytic activity and pel homologous sequences in Frankia. Plant Soil 118:221–229

    Article  Google Scholar 

  • Shah VK, Brill WJ (1977) Isolation of an iron–molybdenum cofactor from nitrogenase. Proc Natl Acad Sci USA 74:3249–3253

    Article  PubMed  CAS  Google Scholar 

  • Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125

    Article  CAS  Google Scholar 

  • Sharma SB, Signer ER (1990) Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Genes Dev 4:344–356

    Article  PubMed  CAS  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 Press, San Diego, 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

    Google Scholar 

  • Skene KR (1998) Cluster roots: some ecological considerations. J Ecol 86:1060–1064

    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 

  • Svistoonoff S, Laplaze L, Auguy F, Runions J, 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 16:600–607

    Article  PubMed  CAS  Google Scholar 

  • 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 136:3191–3197

    Article  PubMed  CAS  Google Scholar 

  • Svistoonoff S, Sy MO, Diagne N, Barker DG, Bogusz D, Franche C (2010) Infection-specific activation of the Medicago truncatula Enod11 early nodulin gene promoter during actinorhizal root nodulation. Mol Plant Microbe Interact 23:740–747

    Article  PubMed  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 

  • Timmers ACJ, Auriac M-C, de Billy F, Truchet G (1998) Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development 125:339–349

    PubMed  CAS  Google Scholar 

  • Torrey JG (1976) Initiation and development of root nodules of Casuarina (Casuarinaceae). Am J Bot 63:335–344

    Article  Google Scholar 

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

    Article  Google Scholar 

  • van Brussel AAN, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJ, Kijne JW (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257:70–72

    Article  PubMed  Google Scholar 

  • van Ghelue M, Lovaas E, Ringo E, Solheim B (1997) Early interactions between Alnus glutinosa and Frankia strain ArI3—production and specificity of root hair deformation factor(s). Physiol Plant 99:579–587

    Article  Google Scholar 

  • Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Horvath G, Kelemen Z, Tarayre S, Roudier F, Mergaert P, Kondorosi A, Kondorosi E (2003) Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15:2093–2105

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, Davis CC, Latvis M, Manchester SR, Soltis DE (2009) Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA 106:3853–3858

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the Swedish Research councils VR and FORMAS and the Russian Foundation for Basic Research (11-04-02022) as well as the Ministry of Education and Sciences of the Russian Federation (GC # 16.552.11.7047, 14.740.11.1226) for their support. We are indebted to Dr. Maria A. Osipova for her help with preparing Fig. 3.

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Authors and Affiliations

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

    Katharina Pawlowski

  2. Laboratory of Anatomy and Morphology, Komarov Botanical Institute, Russian Academy of Sciences, Prof. Popov St. 2, 197376, St. Petersburg, Russia

    Kirill N. Demchenko

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  1. Katharina Pawlowski
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  2. Kirill N. Demchenko
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Correspondence to Katharina Pawlowski.

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Pawlowski, K., Demchenko, K.N. The diversity of actinorhizal symbiosis. Protoplasma 249, 967–979 (2012). https://doi.org/10.1007/s00709-012-0388-4

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