Skip to main content
Log in

Macroevolution of symbiosis as self-organization of superspecies system controlled by natural selection

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

Mutualistic symbioses are convenient models for analyzing the ecological-genetic mechanisms of progressive evolution, which remains obscure for unitary (free-living) organisms. In the system of legume-rhizobia symbiosis, the hosting of N2-fixing bacteria within extracellular and intracellular compartments of nodules (infection threads, symbiosomes) acquired by plants during their coevolution with microbes induces in their populations, group selection is in favor of mutualistic traits (complete transfer of fixed nitrogen to hosts, differentiation of bacteria into the nonreproducible bacteroids). The colonization of infection threads by rhizobia increases the clonality in their populations that induce the interdeme selection for elevated nitrogenase activity. Its further increase may be due to colonization of symbiosomes, which induces the selection of kin in microbial populations in favor of irreversible bacteroid differentiation. The impact of these selection modes on bacteria resulted in the transition of anodular (rhizospheric, endophytic) plant-microbe associations based on the stimulation of root growth by auxins into nodular symbioses based on the effects of nitrogen fixation.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Amarger, N. and Lobreau, J.P., Quantitative study of nodulation competitiveness in Rhizobium strains, Appl. Environ. Microbiol., 1982, vol. 44, pp. 583–588.

    PubMed  CAS  Google Scholar 

  • Berg, L.S., Nomogenesis or evolution based on regularities, in Trudy po teorii evolyutsii (Transactions on Evolutionary Theory), Leningrad: Nauka, 1977, pp. 95–338.

    Google Scholar 

  • Beringer, J.E., Brewin, N.J., and Johnston, A.W.B., The genetic analysis of Rhizobium in relation to symbiotic nitrogen fixation, Heredity, 1980, vol. 45, pp. 161–186.

    Article  CAS  Google Scholar 

  • Bogatykh, B.A., Fraktal’naya priroda zhivogo (Fractal Nature of Animals), Moscow: Liberkom, 2012.

    Google Scholar 

  • Broughton, W.J., Samrey, U., and Stanley, J., Ecological genetics of Rhizobium meliloti: symbiotic plasmid transfer in the Medicago sativa rhizosphere, FEMS Microbiol. Lett., 1987, vol. 40, pp. 251–255.

    Article  CAS  Google Scholar 

  • Bryan, J.A., Berlyn, G.P., and Gordon, J.C., Towards a new concept of the evolution of symbiotic nitrogen fixation in the Leguminosae, Plant Soil, 1996, vol. 186, pp. 151–159.

    Article  CAS  Google Scholar 

  • Chernova, T.A., Aronshtam, A.A., and Simarov, B.V., Genetic nature of nonvirulent mutants CXM1-125 and CXM1-126 of Rhizobium meliloti, Genetika, 1986, vol. 22, no. 8, pp. 2066–2073.

    CAS  Google Scholar 

  • Deakin, W.J. and Broughton, W.J., Symbiotic use of pathogenic strategies: rhizobial protein secretion systems, Nature Rev. Microbiol., 2009, vol. 7, pp. 312–320.

    CAS  Google Scholar 

  • Denison, R.F. and Kiers, E.T., Lifestyle alternatives for rhizobia: mutualism, parasitism and foregoing symbiosis, FEMS Microbiol. Lett., 2004a, vol. 237, pp. 187–193.

    Article  PubMed  CAS  Google Scholar 

  • Denison, R.F. and Kiers, E.T., Why are most rhizobia beneficial to their plant hosts, rather than parasitic?, Microbes Infect., 2004b, vol. 6, pp. 1235–1239.

    Article  PubMed  CAS  Google Scholar 

  • Dodd, I.C., Zinovkina, N.Y., Safronova, V.I., and Belimov, A.A., Rhizobacterial mediation of plant hormone status, Ann. Appl. Biol., 2010, vol. 157, pp. 361–379.

    Article  CAS  Google Scholar 

  • Dorosinskii, L.M. and Lazareva, N.M., Specific rhizobial bacteria of soya and lupin, Mikrobiologiya, 1968, vol. 37, no. 1, pp. 115–121.

    CAS  Google Scholar 

  • Douglas, A.E., Symbiotic Interactions, Oxford: Oxford Univ. Press, 1994.

    Google Scholar 

  • Frank, S.A., Genetics of mutualism: the evolution of altruism between species, J. Theor. Biol., 1994, vol. 170, pp. 393–400.

    Article  PubMed  CAS  Google Scholar 

  • Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J.C., 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, W.L., Chang, W.S., Saunders, E., Bruce, D., Richardson, P., Normand, P., Dreyfus, B., Pignol, D., Stacey, G., Emerich, D., Verméglio, A., Medigue, C., and Sadowsky, M., Legume symbioses: absence of nod genes in photosynthetic bradyrhizobia, Science, 2007, vol. 316, pp. 1307–1312.

    Article  PubMed  Google Scholar 

  • Gorsuch, R.L., Factor Analysis, New York: Lawrence Erlbaum Assoc., 1983.

    Google Scholar 

  • Iordanskii, N.N., Charles Darwin and the problem of evolutionary progress, Zh. Obshch. Biol., 2010, vol. 71, no. 6, pp. 488–496.

    PubMed  CAS  Google Scholar 

  • Janzen, D.H., When is it co-evolution?, Evolution, 1980, vol. 34, pp. 611–612.

    Article  Google Scholar 

  • Kalevitch, M.V., Kefeli, V.I., Borsari, B., Davis, J., and Bolous, G., Final version chemical signaling during organisms’ growth and development, J. Cell Mol. Biol., 2004, vol. 3, pp. 95–102.

    Google Scholar 

  • Kaneko, T., Minamisawa, K., Isawa, T., Nakatsukasa, H., Mitsui, H., Kawaharada, Y., Nakamura, Y., Watanabe, A., Kawashim, K., Ono, A., Shimizu, Y., Takahashi, C., Minami, C., Fujishiro, T., Kohara, M., Katoh, M., Nakazaki, N., Nakayama, S., Yamada, M., Tabata, S., and Sato, S., Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510, DNA Res., 2010, vol. 17, pp. 37–50.

    Article  PubMed  CAS  Google Scholar 

  • Kistner, C. and Parniske, M., Evolution of signal transduction in intercellular symbiosis, Trends Plant Sci., 2002, vol. 7, pp. 511–518.

    Article  PubMed  CAS  Google Scholar 

  • Kulaichev, A.P., Metody i sredstva kompleksnogo analiza dannykh (Methods and Tools of Complex Data Analysis), Moscow: FORUM-INFRA-M, 2006.

    Google Scholar 

  • Maillet, F., Poinsot, V., Andre, O., Puech-Pages, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Martinez, E.A., Driguez, H., Becard, G., and Denarie, J., Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza, Nature, 2011, vol. 469, pp. 58–65.

    Article  PubMed  CAS  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., Medigue, C., Batut, J., and Masson-Boivin, C., Experimental evolution of a plant pathogen into legume symbionts, PLoS Biol., 2010, vol. 8, pp. 1–10.

    Article  Google Scholar 

  • Margulis, L., Symbiogenesis. A new principle of evolution rediscovery of Boris Mikhaylovich Kozo-Polyansky (1890–1957), Charles Darwin and Modern Biology, Kolchinsky, E.I., Ed., St. Petersburg: Nestor-Historia, 2010, pp. 34–48.

    Google Scholar 

  • Maynard Smith, J., Feil, E.J., and Smith, N.H., Population structure and evolutionary dynamics of pathogenic bacteria, BioEssays, 2000, vol. 22, pp. 1115–1122.

    Article  Google Scholar 

  • Maynard Smith, J., Smith, N.H., O’Rourke, M., and Spratt, B.G., How clonal are bacteria?, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 4384–4388.

    Article  Google Scholar 

  • Michod, R.D. and Roze, D., Transitions in individuality, Proc. Roy. Soc. Lond. B, 1997, vol. 264, pp. 953–857.

    Article  Google Scholar 

  • Ochman, H., Elwyn, S., and Moran, N.A., Calibrating bacterial evolution, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 12638–12643.

    Article  PubMed  CAS  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, Nitrogen Fixation Research Progress, Couto, G.N., Ed., New York: NOVA Sci. Publ., 2008, pp. 15–109.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pretorius-Güth, I.M., Pühler, A., and Simon, R., Conjugal transfer of megaplasmid 2 between Rhizobium meliloti strains in alfalfa nodules, Appl. Environ. Microbiol., 1990, vol. 56, pp. 2354–2359.

    PubMed  Google Scholar 

  • Provorov, N.A., Relationship between taxonomy of legumes and specificity their interaction with nodule bacteria, Bot. Zh., 1992, vol. 77, no. 8, pp. 21–32.

    Google Scholar 

  • Provorov, N.A., The interdependence between taxonomy of legumes and specificity of their interaction with rhizobia in relation to evolution of the symbiosis, Symbiosis, 1994, vol. 17, pp. 183–200.

    Google Scholar 

  • Provorov, N.A., Coevolution of rhizobia with legumes: facts and hypotheses, Symbiosis, 1998, vol. 24, pp. 337–367.

    Google Scholar 

  • Provorov, N.A., Molecular basis of symbiogenic evolution: from free-living bacteria towards organelles, Zh. Obshch. Biol., 2005, vol. 66, no. 5, pp. 371–388.

    PubMed  CAS  Google Scholar 

  • Provorov, N.A. and Tikhonovich, I.A., Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis, Genet. Res. Crop. Evol., 2003a, vol. 50, pp. 89–99.

    Article  CAS  Google Scholar 

  • Provorov, N.A. and Tikhonovich, I.A., Ecological and genetic principles of the plant breeding to improve symbiosis with bacteria, S.-kh. Biol., 2003b, no. 3, pp. 11–25.

    Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Population genetics of nodule bacteria: simulation of cyclic processes in bacterial-plant systems, Russ. J. Genet., 1998a, vol. 34, no. 12, pp. 1455–1461.

    CAS  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., A role of interstrain competition in the evolution of genetically polymorphic populations of nodule bacteria, Russ. J. Genet., 1998b, vol. 34, no. 12, pp. 1462–1468.

    CAS  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Population genetics of nodule bacteria: construction and analysis of an “infection and release” model, J. Theor. Biol., 2000, vol. 205, pp. 105–119.

    Article  PubMed  CAS  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Microevolution of nodule bacteria upon generation of mutants with altered survival in the plant-soil system, Russ. J. Genet., 2003, vol. 39, no. 12, pp. 1349–1359.

    Article  CAS  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Interplay of Darwinian and frequency-dependent selection in the host-associated microbial populations, Theor. Popul. Biol., 2006, vol. 70, pp. 262–272.

    Article  PubMed  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Equilibrium between the “genuine mutualists” and “symbiotic cheaters” in the bacterial population co-evolving with plants in a facultative symbiosis, Theor. Populat. Biol., 2008, vol. 74, pp. 345–355.

    Article  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Host plant as on organizer of microbial evolution in the beneficial symbioses, Phytochem. Rev., 2009, vol. 8, pp. 519–534.

    Article  CAS  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Evolutionary Genetics of Plant-Microbe Symbioses, New York: NOVA Sci. Publ., 2010a.

    Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Simulation of evolution implemented in the mutualistic symbioses towards enhancing their ecological efficiency, functional integrity and genotypic specificity, Theor. Populat. Biol., 2010b, vol. 78, pp. 259–269.

    Article  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Co-evolution of partners and the integrity of symbiotic systems, Zh. Obshch. Biol., 2012, vol. 73, no. 1, pp. 21–36.

    PubMed  CAS  Google Scholar 

  • Rodriguez, R.J., Freeman, D.C., McArthur, E.D., Kim, Y.O., and Redman, R.S., Symbiotic regulation of plant growth, development and reproduction, Commun. Integr. Biol., 2009, vol. 2, pp. 141–143.

    PubMed  Google Scholar 

  • Ruse, M., Limits to our knowledge of evolution, Evolutionary Biology, Clegg, M.T., Hecht, M.K., and MacIntryre, R.J., Eds., New York: Kluwer, 2000, vol. 32, pp. 3–31.

    Chapter  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, pp. 1296–1300.

    CAS  Google Scholar 

  • Seckbach, J., Symbiosis: Mechanisms and Model Systems, Dordrecht: Kluwer, 2002.

    Google Scholar 

  • Shaposhnikov, G.Kh., Living systems with less integrity, Zh. Obshch. Biol., 1975, vol. 36, pp. 323–335.

    Google Scholar 

  • Shmalgauzen, I.I., Puti i zakonomernosti evolyutsionnogo protsess (The Development and Pattern of Evolution), Moscow: Nauka, 1983.

    Google Scholar 

  • Shtark, O.Y., Borisov, A.Y., Zhukov, V.A., Provorov, N.A., and Tikhonovich, I.A., Intimate associations of beneficial soil microbes with host plants, Soil Microbiology and Sustainable Crop Production, Dixon, R. and Tilston, E., Eds., Berlin: Springer, 2010, pp. 119–196.

    Chapter  Google Scholar 

  • Souza, V., Nguyen, T.T., Hudson, R.R., Pinero, D., and Lenski, R.E., Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex?, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 8389–8393.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Sprent, J.I., Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation, New Phytol., 2007, vol. 174, pp. 11–25.

    Article  PubMed  CAS  Google Scholar 

  • Stougaard, J., Genetics and genomics of root symbiosis, Curr. Opin. Plant Biol., 2001, vol. 4, pp. 328–335.

    Article  PubMed  CAS  Google Scholar 

  • Streeter, J., Integration of plant and bacterial metabolism in nitrogen fixing systems, Nitrogen Fixations: Fundamentals and Applications, Tikhonovich, I.A., Provorov, N.A., Romanov, V.I., and Newton, W.E., Eds., Dordrecht: Kluwer, 1995, pp. 67–76.

    Chapter  Google Scholar 

  • Tikhonovich, I.A. and Provorov, N.A., From plant-microbe interactions to symbiogenetics: a universal paradigm for the inter-species genetic integration, Ann. Appl. Biol., 2009, vol. 154, pp. 341–350.

    Article  Google Scholar 

  • Tikhonovich, I.A. and Provorov, N.A., Epigenetics of ecological niches, Ekol. Genet., 2010, vol. 8, no. 4, pp. 30–38.

    Google Scholar 

  • Tikhonovich, I.A. and Provorov, N.A., Development of symbiogenetic approaches for studying variation and heredity of superspecies systems, Russ. J. Genet., 2012, vol. 48, no. 4, pp. 357–368.

    Article  CAS  Google Scholar 

  • Tort, L., Balasch, J.C., and Mackenzie, S., Fish immune system. The crossroads between innate and adaptive responses, Immunologia, 2003, vol. 22, pp. 277–286.

    Google Scholar 

  • Velde van de, W., Zehirov, G., Szatmari, A., Debreczeny, M., Ishihara, H., Kevei, Z., Farkas, A., Mikulass, K., Nagy, A., Tiricz, H., Satiat-Jeunemaitre, B., Alunni, B., Bourge, M., Kucho, K., Abe, M., Keresz, A., Maroti, G., Toshiki, T., Kondorosi, E., and Mergaert, P., Plant peptides govern terminal differentiation of bacteria in symbiosis, Science, 2010, vol. 327, pp. 1122–1126.

    Article  PubMed  Google Scholar 

  • Vieille, C. and Elmerich, C., Characterization of two Azospirillum brasilense Sp7 plasmid genes homologous to Rhizobium meliloti nodPQ, Mol. Plant-Microbe Interact., 1990, vol. 6, pp. 389–400.

    Article  Google Scholar 

  • Vieille, C. and Elmerich, C., Characterization of an Azospirillum brasilense Sp7 plasmid gene homologous to Alcaligenes eutrophic phbB and Rhizobium meliloti nodG, Mol. Gen. Genet., 1992, vol. 231, pp. 375–384.

    Article  PubMed  CAS  Google Scholar 

  • Vorobyov, N.I. and Provorov, N.A., Modeling of evolution of legume-rhizobial symbiosis during multi-strain competition of bacteria for inoculation of symbiotic niches, Ekol. Genet., 2008, vol. 6, no. 4, pp. 3–11.

    Google Scholar 

  • Vorobyov, N.I. and Provorov, N.A., Modeling of evolution of legume-rhizobial symbiosis for enhancement of functional integrity of the partners and ecologic efficiency of their interaction, Ekol. Genet., 2010, vol. 8, no. 3, pp. 16–26.

    Google Scholar 

  • Vorontsov, N.N., Razvitie evolyutsionnykh idei v biologii (Development of Evolutionary Concepts in Biology), Moscow: Progress-Traditsiya, 1999.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. A. Provorov.

Additional information

Original Russian Text © N.A. Provorov, N.I. Vorobyov, 2013, published in Uspekhi Sovremennoi Biologii, 2013, Vol. 133, No. 1, pp. 35–49.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Provorov, N.A., Vorobyov, N.I. Macroevolution of symbiosis as self-organization of superspecies system controlled by natural selection. Biol Bull Rev 3, 274–285 (2013). https://doi.org/10.1134/S2079086413040063

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086413040063

Keywords

Navigation