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.
Similar content being viewed by others
References
Arnholdt-Schmitt B (1999) On the physiology of yield production in carrots.—Implications for breeding towards nutrient efficiency. Gartenbauwissenschaft 64:26–32
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
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
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
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
Berg RH (1990) Cellulose and xylans in the interface capsule in symbiotic cells of actinorhizae. Protoplasma 159:35–43
Berg RH (1999a) Cytoplasmic bridge formation in the nodule apex of actinorhizal root nodules. Can J Bot 77:1351–1357
Berg RH (1999b) Frankia forms infection threads. Can J Bot 77:1327–1333
Berg RH, Langenstein B, Silvester WB (1999) Development in the Datisca-Coriaria nodule type. Can J Bot 77:1334–1350
Bergman B, Johansson C, Söderbäck E (1992) The Nostoc–Gunnera symbiosis. New Phytol 122:379–400
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
Berry AM, Torrey JG (1983) Root hair deformation in the infection process of Alnus rubra. Can J Bot 61:2863–2876
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
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
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
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
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
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
Callaham D, Torrey JG (1977) Prenodulae formation and primary nodule development in roots of Comptonia (Myricaceae). Can J Bot 51:2306–2318
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
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
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
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
Doyle JJ (2011) Phylogenetic perspectives on the origins of nodulation. Mol Plant Microbe Interact 24:1289–1295
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
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
Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72
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
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
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
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
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
Gough C, Cullimore J (2011) Lipo-chitooligosaccharide signaling in endosymbiotic plant–microbe interactions. Mol Plant Microbe Interact 24:867–878
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
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
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
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
Huss-Danell K (1997) Tansley Review No. 93. Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405
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
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
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
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
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
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
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
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
Landsberg EC (1996) Hormonal regulation of iron–stress response in sunflower roots: a morphological and cytological investigation. Protoplasma 194:69–80
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
Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root meristems is a two stage process. Dev 121:3303–3310
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
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
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
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
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
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
Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14:77–86
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
Miller IM, Baker DD (1985) The initiation development and structure of root nodules in Elaeagnus angustifolia (Elaeagnaceae). Protoplasma 128:107–119
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
Moran NA (2003) Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6:512–518
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
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
Newcomb W, Pankhurst CE (1982) Fine structure of actinorhizal nodules of Coriaria arborea (Coriariaceae). N Zeal J Bot 20:93–103
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
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
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
Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546
Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume–rhizobial symbiosis. Annu Rev Genet 45:119–144
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
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
Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
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
Pawlowski K (2002) Actinorhizal symbioses. In: Leigh GJ (ed) Nitrogen fixation at the millennium. Elsevier, Amsterdam
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
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
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
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
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
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
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
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
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
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
Schröder P (1989) Aeration of the root system in Alnus glutinosa L. Gaertn. Annales des Sciences Forestières 46:310–314
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
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
Séguin A, Lalonde M (1989) Detection of pectolytic activity and pel homologous sequences in Frankia. Plant Soil 118:221–229
Shah VK, Brill WJ (1977) Isolation of an iron–molybdenum cofactor from nitrogenase. Proc Natl Acad Sci USA 74:3249–3253
Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125
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
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
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
Skene KR (1998) Cluster roots: some ecological considerations. J Ecol 86:1060–1064
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
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
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
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
Swensen SM (1996) The evolution of actinorhizal symbioses—evidence for multiple origins of the symbiotic association. Am J Bot 83:1503–1512
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
Torrey JG (1976) Initiation and development of root nodules of Casuarina (Casuarinaceae). Am J Bot 63:335–344
Valverde C, Wall LG (1999) Time course of nodule development in the Discaria trinervis (Rhamnaceae) Frankia symbiosis. New Phytol 141:345–354
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: David Robinson
Rights and permissions
About this article
Cite this article
Pawlowski, K., Demchenko, K.N. The diversity of actinorhizal symbiosis. Protoplasma 249, 967–979 (2012). https://doi.org/10.1007/s00709-012-0388-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-012-0388-4