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Evolution of nitrogen-fixing symbioses on the basis of bacterial migration from mycorrhizal fungi and soil into plant tissues

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Abstract

A hypothesis is proposed on the emergence of N2-fixing plant symbionts from soil diazotrophs and satellites of Glomeromycota fungi that form arbuscular mycorrhizae (AM). This universal form of plant-microbe symbiosis possibly appeared due to the integration of ancestral land plants (rhyniophytes, psylophytes) and microbial consortia composed of AM-fungi assimilating soil phosphates and bacteria fixing atmospheric CO2 and/or N2. The release of these bacteria from AM-fungal hyphae into plant tissues elicited the selection of genotypes capable of fungi-independent multiplication in plants, as well as the fixation in bacterial genomes of the genes for the synthesis of chitin-like signal factors stimulating the development of symbiotic structures. An early stage of this evolution might been represented by the formation of N2-fixing syncyanoses, and the late stage might have been realized by the formation of nodular symbioses of dicots from the Eurosid I clade with rhizobia (α- and β-proteobacteria) and with the actinobacteria Frankia. The emergence of these symbioses was possibly based on the migration of soil and endophytic bacteria into the storage organs (modified stems or lateral roots), where the optimal conditions were established not only for N2 fixation but also for the evolution of bacteria towards increased symbiotic activity. This evolution resulted in the emergence of primary rhizobia (Bradyrhizobium, Burkholderia), which acted as donors of sym genes for a broad spectrum of microbes transformed into secondary rhizobia (Rhizobium, Sinorhizobium). The subsequent evolution of nodular symbioses was directed at an increased efficiency of symbiotrophic nitrogen nutrition in host plants following two scenarios: (a) “expensive,” which is based on an increase in N2-fixing activity via the transformation of bacteria into nonreproducible bacteroids; (b) “economical,” based on the acquisition of the determinate nodule structure and ureide nitrogen assimilation.

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References

  • Bagirova, S.F., Dzhavakhiya, V.G., D’yakov, Yu.T., Ozeretskovskaya, O.L., Provorov, N.A., Tikhonovich, I.A., and Shcherbakova, L.A., Fundamental’naya fitopatologiya (Fundamental Phytopathology), Moscow: Krasand, 2012.

    Google Scholar 

  • Bal, A.K. and Khetmalas, M.B., Pre- and post-winter changes in the root nodules of Lathyrus maritimus (L.) Bigel. with special reference to storage organelles, Int. J. Plant Sci., 1996, vol. 157, no. 4, pp. 432–439.

    Article  Google Scholar 

  • Barea, J.-M., Pozo, M.-J., Azcon, R., and Azcon-Aguilar, C., Microbial cooperation in the rhizosphere, J. Exp. Bot., 2005, vol. 56, no. 14, pp. 1761–1788.

    Article  CAS  PubMed  Google Scholar 

  • Becker, A. and Pühler, A., Production of exopolysaccharides, in The Rhizobiaceae. Molecular Biology of Model Plant-Associated Bacteria, Spaink, H.P., Kondorosi, A., and Hooykaas, P.J.J., Eds., Dordrecht: Kluwer, 1998, pp. 87–118.

    Google Scholar 

  • Béreau, M. and Garbaye, J., First observations on the root morphology and symbioses of 21 major tree species in the primary tropical rain forest of French Guyana, Ann. For. Sci., 1994, vol. 51, no. 4, pp. 407–416.

    Article  Google Scholar 

  • Bhattacharya, D., Archibald, J.M., Weber, A.P., and Reyes-Prieto, A., How do endosymbionts become organelles? Understanding early events in plastid evolution, BioEssays, 2007, vol. 29, pp. 1239–1246.

    Article  CAS  PubMed  Google Scholar 

  • Bonfante, P. and Anca, I.A., Plants, mycorrhizal fungi, and bacteria: a network of interactions, Annu. Rev. Microbiol., 2009, vol. 63, pp. 363–383.

    Article  CAS  PubMed  Google Scholar 

  • Brundrett, M.C., Coevolution of roots and mycorrhizas of land plants, New Phytol., 2002, vol. 154, pp. 275–304.

    Article  Google Scholar 

  • Brundrett, M.C. and Abbott, L.K., Roots of jarrah forest plants. I. Mycorrhizal associations of shrubs and herbaceous plants, Austral. J. Bot., 1991, vol. 39, pp. 445–457.

    Article  Google Scholar 

  • Caetano-Anollés, G. and Gresshoff, P.M., Plant genetic suppression of the non-nodulation phenotype of Rhizobium meliloti host-range nodH mutants: gene-for-gene interaction in the alfalfa-Rhizobium symbiosis? Theor. Appl. Genet., 1992, vol. 84, nos. 5–6, pp. 624–632.

    PubMed  Google Scholar 

  • Couzigou, J.M., Zhukov, V., Mondy, S., Heba, G.A., Cosson, V., et al., NODULE ROOT and COCHLEATA maintain nodule development and are legume orthologs of Arabidopsis BLADE-ON-PETIOLE genes, Plant Cell Online, 2012, vol. 24, no. 11, pp. 4498–4510.

    Article  CAS  Google Scholar 

  • Cruz, A.F. and Ishii, T., Arbuscular mycorrhizal fungal spores host bacteria that affect nutrient biodynamics and biocontrol of soil-borne plant pathogens, Biol. Open, 2011. doi 10.1242/bio.2011014

    Google Scholar 

  • Cyanobacteria in Symbiosis, Rai, A.N., Bergman, B., and Rasmussen, U., Eds., Dordrecht: Kluwer, 2002.

  • Cytryn, E.J., Jitacksorn, S., Giraud, E., and Sadowsky, M.J., Insights learned from pBTAi1, a 229-kb accessory plasmid from Bradyrhizobium sp. strain BTAi1 and prevalence of accessory plasmids in other Bradyrhizobium sp. strains, ISME J., 2008, vol. 2, no. 1, pp. 158–170.

    Article  CAS  PubMed  Google Scholar 

  • Czaja, L.F., Hogekamp, C., Lamm, P., Maillet, F., Martinez, E.A., Samain, E., Dénarié, J., Küster, H., and Hohnjec, N., Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFPand MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides, Plant Physiol., 2012, vol. 159, no. 4, pp. 1671–1685.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Haeze, W. and Holsters, M., Nod factor structures, responses, and perception during initiation of nodule development, Glycobiology, 2002, vol. 12, no. 1, pp. 79–105.

    Article  Google Scholar 

  • De Smet, I., Tetsumura T., De Rybel B., Frei dit Frey N., and Laplaze L., Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis, Development, 2007, vol. 134, pp. 681–690.

    Article  PubMed  CAS  Google Scholar 

  • Deusch, O., Landan, G., Roettger, M., Gruenheit, N., Kowallik, K.V., Allen, J.F., Martin, W., and Dagan, T., Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor, Mol. Biol. Evol., 2008, vol. 25, no. 4, pp. 748–761.

    Article  CAS  PubMed  Google Scholar 

  • Dickie, I.A. and Holdaway, R.J., Podocarp roots, mycorrhizas, and nodules, Smithsonian Contrib. Bot., 2010, vol. 95, no. 1, pp. 175–187.

    Google Scholar 

  • Engelke, T., Jagadish, M.N., and Pühler, A., Biochemical and genetical analysis of Rhizobial meliloti mutants defective in C4-dicarboxylates transport, J. Gen. Microbiol., 1987, vol. 133, no. 1, pp. 3019–3029.

    CAS  Google Scholar 

  • Engelke, T., Jording, D., Kapp, D., and Pühler, A., Identification and sequence analysis of the Rhizobium meliloti dctA gene encoding the C4-dicarboxylate carrier, J. Bacteriol., 1989, vol. 171, no. 12, pp. 5551–5560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estrada-De Los Santos, P., Bustillos-Cristales, R., and Caballero-Mellado, J., Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution, Appl. Environ. Microbiol., 2001, vol. 67, no. 6, pp. 2790–2798.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher, J.B. and Vovides, A.P., Mycorrhizae are present in cycad roots, Bot. Rev., 2004, vol. 70, no. 1, pp. 16–23.

    Article  Google Scholar 

  • Franche, C., Lindström, K., and Elmerich, C., Nitrogenfixing bacteria associated with leguminous and nonleguminous plants, Plant Soil, 2009, vol. 321, nos. 1–2, pp. 35–59.

    Article  CAS  Google Scholar 

  • Frey-Klett, P., Garbaye, J.P. and Tarkka, M., The mycorrhiza helper bacteria revisited, New Phytol., 2007, vol. 176, no. 1, pp. 22–36.

    Article  CAS  PubMed  Google Scholar 

  • Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., Fournier, J., Rochange, S., Bécard, G., Bonfante, P., and Barker, D.G., Shortchain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone, New Phytol., 2013, vol. 198, no. 1, pp. 190–202.

    Article  PubMed  Google Scholar 

  • Gianinazzi-Pearson, V., Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis, Plant Cell, 1996, vol. 8, no. 6, pp. 1871–1883.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibson, K.E., Kobayashi, H., and Walker, G.C., Molecular determinants of a symbiotic chronic infection, Ann. Rev. Genet., 2008, vol. 42, pp. 413–441.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., et al., Legume symbioses: absence of nod genes in photosynthetic bradyrhizobia, Science, 2007, vol. 316, no. 5829, pp. 1307–1312.

    Article  PubMed  Google Scholar 

  • Gualtieri, G. and Bisseling, T., The evolution of nodulation, Plant Mol. Biol., 2000, vol. 42, no. 1, pp. 181–194.

    Article  CAS  PubMed  Google Scholar 

  • Guan, D., Stacey, N., Liu, C., Wen, J., Mysore, K.S., Torres-Jerez, I., Vernié, T., Tadege, M., Zhou, G., Wang, Z., Udvardi, M.K., Oldroyd, G.E.D., and Murray, J.D., Rhizobial infection is associated with the development of peripheral vasculature in nodules of Medicago truncatula, Plant Physiol., 2013a, vol. 162, no. 1, pp. 107–115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan, S.H., Gris, C., Cruveiller, S., Pouzet, C., Tasse, L., Leru, A., Maillard A., Médigue, C., Batut, J., Masson-Boivin, C., and Capela, D., Experimental evolution of nodule intracellular infection in legume symbionts, ISME J., 2013b, vol. 7, no. 7, pp. 1367–1377.

    Google Scholar 

  • Gurusamy, C., Davis, P.J., and Bal, A.K., Seasonal changes in perennial nodules of beach pea (Lathyrus maritimus (L.) Bigel.) with special reference to oleosomes, Int. J. Plant Sci., 2000, vol. 161, no. 4, pp. 631–638.

    Article  CAS  Google Scholar 

  • Hildebrandt, U., Ouziad, F., Marner, F.J., and Bothe, H., The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores, FEMS Microb. Lett., 2006, vol. 254, no. 2, pp. 258–267.

    Article  CAS  Google Scholar 

  • Hirsch, A.M. and LaRue, T.A., Is the legume nodule a modified root or stem or an organ sui generis? Crit. Rev. Plant Sci., 1997, vol. 16, no. 4, pp. 361–392.

    Article  Google Scholar 

  • Hirsch, A.M., Lum, M.R., and Downie, J.A., What makes the rhizobia-legume symbiosis so special? Plant Physiol., 2001, vol. 127, no. 5, pp. 1484–1492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hocher, V., Alloisio, N., Bogusz, D., and Normand, P., Early signaling in actinorhizal symbioses, Plant Signaling Behav., 2011, vol. 6, no. 9, pp. 1377–1379.

    Article  CAS  Google Scholar 

  • Humphreys, C.P., Franks, P.J., Rees, M., Bidartondo, M.I., Leake, J.R., and Beerling, D.J., Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants, Nat. Commun., 2010, vol. 1, art. ID 103. doi 10.1038/ncomms1105

    Google Scholar 

  • Kaneko, T., Minamisawa, K., Isawa, T., Nakatsukasa, H., Mitsui, H., et al., Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510, DNA Res., 2010, vol. 17, pp. 37–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karatygin, I.V., Coevolution of fungi and plants, Tr. Bot. Inst., Ross. Akad. Nauk, 1993, no. 9, pp. 1–118.

    Google Scholar 

  • Karatygin, I.V., Snigirevskaya, N.S., and Demchenko, K.N., Species of the Glomites as plant mycobionts in Early Devonian ecosystems, Paleontol. J., 2006, vol. 40, no. 5, pp. 572–579.

    Article  Google Scholar 

  • Kelly, M.N. and Irving, H.R., Nod factors stimulate plasma membrane delimited phospholipase C activity in vitro, Physiol. Plant., 2001, vol. 113, no. 4, pp. 461–468.

    Article  CAS  Google Scholar 

  • Kluge, M., Mollenhauer, D., Wolf, E., and Schüler, A., The Nostoc–Geosiphon endocytobiosis, in Cyanobacteria in Symbiosis, Rai, A.N., Bergman, B., and Rasmussen, U., Eds., Dordrecht: Kluwer, 2002, pp. 19–30.

    Google Scholar 

  • Koske, R.E., Gemma, J.N., and Doyle, M.F., Mycorrhizal status of Gunnera petaloidea in Hawaii, Pac. Sci., 1992, vol. 46, no. 4, pp. 480–483.

    Google Scholar 

  • Krings, M., Hass, H., Kerp, H., Taylor, T.N., Agerer, R., and Dotzler, N., Endophytic cyanobacteria in a 400-million-yr-old land plant: a scenario for the origin of a symbiosis? Rev. Palaeobot. Palynol., 2009, vol. 153, no. 1, pp. 62–69.

    Article  Google Scholar 

  • Krings, M., Kerp, H., Hass, H., Taylor, T.N., and Dotzler, N., A filamentous cyanobacterium showing structured colonial growth from the Early Devonian Rhynie chert, Rev. Palaeobot. Palynol., 2007a, vol. 146, no. 2, pp. 265–276.

    Article  Google Scholar 

  • Krings, M., Taylor, T.N., Hass, H., Kerp, H., Dotzler, N., and Hermsen, E.J., Fungal endophytes in a 400-million- yr-old land plant: infection pathways, spatial distribution, and host responses, New Phytol., 2007b, vol. 174, no. 3, pp. 648–657.

    Article  PubMed  Google Scholar 

  • Lackner, G., Möbius, N., Scherlach, K., Partida-Martinez, L.P., Winkler, R., Schmitt, I., and Hertweck, C., Global distribution and evolution of a toxinogenic Burkholderia–Rhizopus symbiosis, Appl. Environ. Microbiol., 2009, vol. 75, no. 8, pp. 2982–2986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laplaze, L., Benková, E., Casimiro, I., Maes, L., and Vanneste, S., Cytokinins act directly on lateral root founder cells to inhibit root initiation, Plant Cell, 2007, vol. 19, pp. 3889–3900.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lodwig, E. and Poole, P., Metabolism of Rhizobium bacteroids, Crit. Rev. Plant Sci., 2003, vol. 22, no. 1, pp. 37–78.

    Article  CAS  Google Scholar 

  • Lumini, E., Bianciotto, V., Jargeat, P., Novero, M., Salvioli, A., Faccio, A., Bécard, G., and Bonfante, P., Presymbiotic growth and sporal morphology are affected in the arbuscular mycorrhizal fungus Gigaspora margarita cured of its endobacteria, Cell. Microbiol., 2007, vol. 9, no. 7, pp. 1716–1729.

    Article  CAS  PubMed  Google Scholar 

  • MacLean, A.M., Finan, T.M., and Sadowsky, M.J., Genomes of symbiotic nitrogen-fixing bacteria of legumes, Plant Physiol., 2007, vol. 144, no. 3, pp. 615–622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., et al., Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza, Nature, 2011, vol. 469, no. 7328, pp. 58–63.

    Article  CAS  PubMed  Google Scholar 

  • Małek, W., Starch content of alfalfa nodules with effective and ineffective response, Acta Microbiol. Pol., 1980, vol. 29, no. 3, pp. 309–311.

    PubMed  Google Scholar 

  • Marchetti, M., Capela, D., Glew, M., Cruveiller, S., Chane-Woon-Ming, B., Gris, C., Timmers, T., Poinsot, V., Gilbert, L.B., Heeb, P., Médigue, C., Batut, J., and Masson-Boivin, C., Experimental evolution of a plant pathogen into a legume symbiont, PLoS Biol., 2010, vol. 8, no. 1. doi 10.1371/journal.pbio.1000280

    Google Scholar 

  • Markmann, K. and Parniske, M., Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci., 2009, vol. 14, no. 1, pp. 77–86.

    Article  CAS  PubMed  Google Scholar 

  • Mathesius, U., Auxin: at the root of nodule development? Funct. Plant Biol., 2008, vol. 35, pp. 651–668.

    Article  CAS  Google Scholar 

  • Meeks, J.C. and Elhai, J., Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states, Microbiol. Mol. Biol. Rev., 2002, vol. 66, no. 1, pp. 94–121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minerdi, D., Fani, R., Gallo, R., Boarino, A., and Bonfante, P., Nitrogen fixation genes in an endosymbiotic Burkholderia strain, Appl. Environ. Microbiol., 2001, vol. 67, no. 3, pp. 725–732.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moulin, L., Munive, A., Dreyfus, B., and Boivin-Masson, C., Nodulation of legumes by members of the β-subclass of Proteobacteria, Nature, 2001, vol. 411, no. 6840, pp. 948–950.

    Article  CAS  PubMed  Google Scholar 

  • Naumann, M., Schüßler, A., and Bonfante, P., The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes, ISME J., 2010, vol. 4, no. 7, pp. 862–871.

    Article  PubMed  Google Scholar 

  • Newman, J.D., Schultz, B.W., and Noel, K.D., Dissection of nodule development by supplementation of Rhizobum leguminosarum biovar phaseoli purine auxotrophs with 4 aminoimidazol-5-carboxamide riboside, Plant Physiol., 1992, vol. 99, no. 2, pp. 401–408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noel, K.D., Vandenbosch, K.A., and Kulpaca, B., Mutations in Rhizobum phaseoli that lead to arrested development of infection threads, J. Bacteriol., 1986, vol. 168, no. 3, pp. 1392–1401.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norstog, K.J. and Nicholls, T.J., The Biology of the Cycads, Ithaca; NY: Cornell Univ. Press, 1997.

    Google Scholar 

  • Ohyama, T., Ohtake, N., Sueyoshi, K., Tewari, K., Takahashi, Y., Ito, S., Nishiwaki, T., Nagumo, Y., Ishii, S., and Sato, T., Nitrogen fixation and metabolism in soybean plants, in Nitrogen Fixation Research Progress, Couto, G.N., Ed., New York: Nova Science, 2008, pp. 15–109.

    Google Scholar 

  • Oldroyd, G.E.D. and Downie, J.A., Coordinating nodule morphogenesis with rhizobial infection in legumes, Annu. Rev. Plant Biol., 2008, vol. 59, pp. 519–546.

    Article  CAS  PubMed  Google Scholar 

  • Ormeño-Orrillo, E., Hungria, M., and Martínez-Romero, E., Dinitrogen-fixing prokaryotes, in The Prokaryotes, Berlin: Springer-Verlag, 2013, pp. 427–451.

    Chapter  Google Scholar 

  • Parsons, R., Nodule function and regulation in Gunnera–Nostoc symbioses, Proc. Irish R. Acad. Sci. B, 2002, vol. 102, no. 1, pp. 41–43.

    Article  Google Scholar 

  • Pawlowski, K., Induction of actinorhizal nodules by Frankia, in Prokaryotic Symbionts in Plants, Microbiol. Monogr., vol. 8, Pawlowski, K., Ed., Berlin: Springer-Verlag, 2009, pp. 127–154.

    Chapter  Google Scholar 

  • Péret, B., Swarup, R., Jansen, L., Devos, G., Auguy, F., Collin, M., Santi, C., Hocher, V., Franche, C., Bogusz, D., Bennett, M., and Laplaze, L., Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca, Plant Physiol., 2007, vol. 144, no. 5, pp. 1852–1862.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perrine-Walker, F., Doumas, P., Lucas, M., Vaissayre, V., Beauchemin, N.J., Band, L.R., Chopard, J., Crabos, A., Conejero, G., Péret, B., King, J.R., Verdeil, J.-L., Hocher, V., Franche, C., Bennett, M.J., et al., Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules, Plant Physiol., 2010, vol. 154, no. 4, pp. 1372–1380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pini, F., Galardini, M., Bazzicalupo, M., and Mengoni, A., Plant–bacteria association and symbiosis: are there common genomic traits in Alphaproteobacteria? Genes, 2011, vol. 2, pp. 1017–1032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Provorov, N.A., Plant-microbe symbioses as an evolutionary continuum, Zh. Obshch. Biol., 2009, vol. 70, no. 1, pp. 10–34.

    CAS  PubMed  Google Scholar 

  • Provorov, N.A. and Andronov, E.E., Evolution of root nodule bacteria: reconstruction of the speciation processes resulting from genomic rearrangements in a symbiotic system, Microbiology (Moscow), 2016, vol. 85, no. 2, pp. 131–139.

    Article  CAS  Google Scholar 

  • Provorov, N.A. and Dolgikh, E.E., Metabolic integration of the organisms in symbiotic systems, Zh. Obshch. Biol., 2006, vol. 67, no. 6, pp. 403–423.

    CAS  PubMed  Google Scholar 

  • Provorov, N.A. and Vorob’ev, N.I., Geneticheskie osnovy evolyutsii rastitel’no-mikrobnogo simbioza (Genetic Principles of Evolution of the Plant-Microbe Symbiosis), Tikhonovich, I.A., Ed., St. Petersburg: Inform- Navigator, 2012.

    Google Scholar 

  • Provorov, N.A. and Vorobyev, N.I., Evolution of host-beneficial traits in nitrogen-fixing bacteria: Modeling and construction of systems for interspecies altruism, Appl. Biochem. Microbiol., 2015, vol. 51, no. 4, pp. 381–387.

    Article  CAS  Google Scholar 

  • Ran, L., Larsson, J., Vigil-Stenman, T., Nylander, J.A., Ininbergs, K., Zheng, W.W., Lapidus, A., Lowry, S., Haselkorn, R., and Bergman, B., Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium, PLoS One, 2010, vol. 5, no. 7. e11486.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rasmussen, B., Fletcher, I.R., Brocks, J.J., and Kilburn, M.R., Reassessing the first appearance of eukaryotes and cyanobacteria, Nature, 2008, vol. 455, no. 3, pp. 1101–1104.

    Article  CAS  PubMed  Google Scholar 

  • Reddell, P., Hopkins, M.S., and Graham, A.W., Functional association between apogeotropic aerial roots, mycorrhizas and paper-barked stems in a lowland tropical rainforest in North Queensland, J. Trop. Ecol., 1996, vol. 12, pp. 763–777.

    Article  Google Scholar 

  • Reiter, N., Lawrie, A., and Walsh, N., The mycorrhizal associations of Borya mirabilis, an endangered Australian native plant, Muelleria, 2013, vol. 31, no. 1, pp. 81–88.

    Google Scholar 

  • Remy, W., Taylor, T.N., Hass, H., and Kerp, H., Four hundred million-year-old vesicular arbuscular mycorrhizas, Proc. Natl. Acad. Sci. U.S.A., 1994, vol. 91, pp. 11841–11843.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Barrueco, C. and de Castro, F.B., Cytokinininduced pseudonodules on Alnus glutinosa, Physiol. Plant, 1973, vol. 29, pp. 227–280.

    Article  Google Scholar 

  • Rodríguez-Llorente, I.D., Pérez-Hormaeche, J., Mounadi, K.E., Dary, M., Caviedes, M.A., Cosson, V., Kondorosi, A., Ratet, P., and Palomares, A.J., From pollen tubes to infection threads: recruitment of Medicago floral pectic genes for symbiosis, Plant J., 2004, vol. 39, no. 4, pp. 587–598.

    Article  PubMed  CAS  Google Scholar 

  • Rossbach, S., Gloudemans, T., Bisseling, T., Studer, D., Kaluza, B., Ebeling, S., and Hennecke, H., Genetic and physiologic characterization of a Bradyrhizobium japonicum mutant defective in early bacteroid development, Mol. Plant-Microbe Interact., 1989, vol. 2, no. 1, pp. 233–240.

    Article  Google Scholar 

  • Russell, A.J., Bidartondo, M.I., and Butterfield, B.G., The root nodules of the Podocarpaceae harbor arbuscular mycorrhizal fungi, New Phytol., 2002, vol. 156, no. 2, pp. 283–295.

    Article  Google Scholar 

  • Saikia, S.P., Jain, V., Khetarpal, S., and Aravind, S., Dinitrogen fixation activity of Azospirillum brasilense in maize (Zea mays), Curr. Sci., 2007, vol. 93, no. 4, pp. 1296–1300.

    CAS  Google Scholar 

  • Scannerini, S. and Bonfante, P., Bacteria and bacteria like objects in endomycorrhizal fungi (Glomaceae), in Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis, Margulis, L. and Fester, R., Eds. Cambridge, MA: Mass. Inst. Technol., 1991, pp. 273–287.

    Google Scholar 

  • Scheres, B., van De Wiel, C., Zalensky, A., Horvath, B., Spaink, H., van Eck, H., Zwartkruis, F., Wolters, A.M., Gloudemans, T., van Kammen, A., and Bisseling, T., The ENOD12 gene product is involved in the infection process during the Pea–Rhizobium interaction, Cell. 1990, vol. 60, no. 2, pp. 281–294.

    Article  CAS  PubMed  Google Scholar 

  • Schüßler, A., Molecular phylogeny, taxonomy and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi, Plant Soil, 2002, vol. 244, no. 1, pp. 75–83.

    Article  Google Scholar 

  • Schüßler, A., Martin, H., Cohen, D., Fitz, M., and Wipf, D., Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi, Nature, 2006, vol. 444, no. 7121, pp. 933–936.

    Article  PubMed  CAS  Google Scholar 

  • Shirtliffe, S.J. and Vessey, J.K., A nodulation (Nod–/Fix–) mutant of Phaseolus vulgaris L. has nodule-like structures lacking peripheral vascular bundles (Pvb–) and is resistant to mycorrhizal infection (Myc–), Plant Sci., 1996, vol. 118, no. 1, pp. 209–220.

    Article  CAS  Google Scholar 

  • Smith, S.E. and Read, D., Mycorrhizal Symbiosis, New York: Elsevier, 2008.

    Google Scholar 

  • Sprent, J.I., Nodulation in Legumes, Kew: Cromwell, 2001.

    Google Scholar 

  • Steenhoudt, O. and Vanderleyden, J., Azospirillum, a freeliving nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects, FEMS Microbiol. Rev., 2000, vol. 24, no. 4, pp. 487–506.

    Article  CAS  PubMed  Google Scholar 

  • Suzaki, T., Ito, M., and Kawaguchi, M., Genetic basis of cytokinin and auxin functions during root nodule development, Front. Plant Sci., 2013, vol. 4, no. 1, pp. 1–6.

    Google Scholar 

  • Talbi, C., Delgado, M.J., Girard, L., RamÍrez-Trujillo, A., Caballero-Mellado, J., and Bedmar, E.J., Burkholderia phymatum strains capable of nodulating Phaseolus vulgaris are present in Moroccan soils, Appl. Environ. Microbiol., 2010, vol. 76, no. 13, pp. 4587–4591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tirichine, L., Sandal, N., Madsen, L.H., Radutoiu, S., Albrektsen, A.S., Sato, S., Asamizu, E., Tabata, S., and Stougaard, J., A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis, Science, 2007, vol. 315, no. 5808, pp. 104–107.

    Article  CAS  PubMed  Google Scholar 

  • Tromas, A., Parizot, B., Diagne, N., Champion, A., Hocher, V., Cissoko, M., Crabos, A., Prodjinoto, H., Lahouze, B., Bogusz, D., Laplaze, L., and Svistoonoff, S., Heart of endosymbioses: transcriptomics reveals a conserved genetic program among arbuscular mycorrhizal, actinorhizal and legume-rhizobial symbioses, PLoS One, 2012, vol. 7, no. 9, p. e44742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsyganov, V.E., Voroshilova, V.A., Herrera-Cervera, J.A., Sanjuan-Pinilla, J.M., Borisov, A.Y., Tikhonovich, I.A., Priefer, U.B., Olivares, J., and Sanjuan, J., Developmental down-regulation of rhizobial genes as a function of symbiosome differentiation in symbiotic root nodules of Pisum sativum L., New Phytol., 2003, vol. 159, no. 2, pp. 521–530.

    Article  CAS  Google Scholar 

  • Vance, C.P., Amide biosynthesis in root nodules of temperate legumes, in Prokaryotic Nitrogen Fixation, Triplett, E., Ed., Wymondham: Horizon Scientific, 2000, pp. 589–607.

    Google Scholar 

  • van de Velde, W., Zehirov, G., Szatmari, A., Debreczeny, M., Ishihara, H., et al., Plant peptides govern terminal differentiation of bacteria in symbiosis, Science, 2010, vol. 327, no. 5969, pp. 1122–1126.

    Article  PubMed  CAS  Google Scholar 

  • Wang, D., Yang, S., Tang, F., and Zhu, H., Symbiosis specificity in the legume—rhizobial mutualism, Cell Microbiol., 2012, vol. 14, no. 3, pp. 334–342.

    Article  PubMed  CAS  Google Scholar 

  • Wong, F.C. and Meeks, J.C., Establishment of a functional symbiosis between the cyanobacterium Nostoc punctiforme and the bryophyte Anthoceros punctatus requires genes involved in nitrogen control and initiation of heterocyst differentiation, Microbiology, 2002, vol. 148, no. 1, pp. 315–323.

    Article  CAS  PubMed  Google Scholar 

  • Yurgel, S.N. and Kahn, M.L., Dicarboxylate transport by rhizobia, FEMS Microbiol. Rev., 2004, vol. 28, no. 4, pp. 489–501.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, W., Du, Y., Khudyakov, I., Fan, Q., Gao, H., Ning, D., Wolk, C.P., and Xu, X., A gene cluster that regulates both heterocyst differentiation and pattern formation in Anabaena sp. strain PCC 7120, Mol. Microbiol., 2007, vol. 66, no. 6, pp. 1429–1443.

    Article  CAS  PubMed  Google Scholar 

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  1. All-Russia Research Institute for Agricultural Microbiology, St.Petersburg, 196608, Russia

    N. A. Provorov, O. Yu. Shtark & E. A. Dolgikh

  2. International Research Center, Biotechnologies of the Third Millennium, ITMO University, St. Petersburg, 191002, Russia

    N. A. Provorov

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  1. N. A. Provorov
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Original Russian Text © N.A. Provorov, O.Yu. Shtark, E.A. Dolgikh, 2016, published in Zhurnal Obshchei Biologii, 2016, Vol. 77, No. 5, pp. 329–345.

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Provorov, N.A., Shtark, O.Y. & Dolgikh, E.A. Evolution of nitrogen-fixing symbioses on the basis of bacterial migration from mycorrhizal fungi and soil into plant tissues. Biol Bull Rev 7, 355–368 (2017). https://doi.org/10.1134/S2079086417050061

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