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Adaptive and progressive evolution of plant-microbial symbiosis

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Russian Journal of Genetics: Applied Research

Abstract

In the N2-fixing symbionts of legumes (rhizobia), the evolution of (altruistic) characters that are useful for a host occurs in the populations colonizing the subscellular compartments of nodules (infection threads, symbiosomes). These compartments appear as a result of the coevolution of partners, which is associated with the complication of the trophic and regulatory interactions determining the ecological efficiency of symbiosis. Their analysis allows us to study the correlation of the mechanisms of the adaptive and progressive evolution of symbiosis, which is still unclear for free-living organisms.

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References

  • de Bary, A., Die Erscheinung der Symbiose, Strassburg: Verlag Von Karl J. Trubner, 1879.

    Google Scholar 

  • Berg, L.S., Trudy po teorii evolyutsii (Works on the Theory of Evolution), Leningrad: Nauka, 1977.

    Google Scholar 

  • Borisov, A., Rozov, S.M., Tsyganov, V.E., et al., Sequential functioning of sym-13 and sym-31, two genes affecting symbiosome development in root nodules of pea (Pisum sativum L.), Mol. Gen. Genet., 1997, vol. 254, pp. 592–598.

    Article  CAS  PubMed  Google Scholar 

  • Brewin, N.J., Development of the legume root nodule, Annu. Rev. Cell Biol., 1991, vol. 7, pp. 191–226.

    Article  CAS  PubMed  Google Scholar 

  • Brewin, N.J., Plant cell wall remodeling in the Rhizobium-legume symbiosis, Crit. Rev. Plant Sci., 2004, vol. 23, pp. 1–24.

    Article  Google Scholar 

  • Bronstein, J.L., The evolution of facilitation and mutualism, J. Ecol., 2009, vol. 97, pp. 1160–1170.

    Article  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 

  • Cheng, J., Sibley, C.D., Zaheer, R., and Finan, T.M., A Sinorhizobium minE mutant has an altered morphology and exhibits defects in legume symbiosis, Microbiology, 2007, vol. 153, pp. 375–387.

    Article  CAS  PubMed  Google Scholar 

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

    Article  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  CAS  PubMed  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 

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

    Google Scholar 

  • Downie, J.A. and Young, J.P.W., The ABC of symbiosis, Nature, 2001, vol. 412, pp. 597–598.

    Article  CAS  PubMed  Google Scholar 

  • Doyle, J.J., Chappill, J.A., Bailey, C.D., and Kajita, T., Towards a comprehensive phylogeny of legumes: evidence from rbcL sequences and non-molecular data, in Advances in Legume Systematics, Herendeen, P.S. and Bruneau, A., Eds., Roy. Botan. Gardens: Key, 2000, pp. 1–20.

    Google Scholar 

  • Filipcenko, J., Variabilitat und Variation, Berlin: Borntrager, 1927.

    Google Scholar 

  • Franche, C., Lindstrom, K., and Elmerich, C., Nitrogenfixing bacteria associated with leguminous and non-leguminous plants, Plant Soil, 2009, vol. 321, pp. 35–59.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Van Ham, R.C., Kamerbeek, J., Palacios, C., et al., Reductive genome evolution in Buchnera aphidicola, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 581–586.

    Article  PubMed Central  PubMed  Google Scholar 

  • Heinrich, K., Ryder, M.H., and Murphy, P.J., Early production of rhizopine in nodules induced by Sinorhizobium meliloti strain L5-30, Can. J. Microbiol., 2001, vol. 47, pp. 165–171.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • Karunakaran, R., Haag, A.F., East, A.K., et al., Baca is essential for bacteroid development in nodules of galegoid, but not phaseoloid legumes, J. Bacteriol., 2010, vol. 192, pp. 2920–2928.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krishnan, H.B. and Chronis, D., Functional nodule genes are present in Sinorhizobium sp. strain MUS10, a symbiont of the tropical legume Sesbania rostrata, Appl. Environ. Microbiol., 2008, vol. 74, pp. 2921–2923.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maillet, F., Poinsot, V., Andre, O., et al., Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza, Nature, 2011, vol. 469, pp. 58–65.

    Article  CAS  PubMed  Google Scholar 

  • Mayr, E., Populations, Species, and Evolution, Cambridge (Massachusetts): Harvard Univ., 1970.

    Google Scholar 

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

    Google Scholar 

  • Margulis, L. and Sagan, D., Acquiring Genomes. A Theory of the Origins of Species, New York: Basic Books, 2002.

    Google Scholar 

  • Markmann, K. and Parniske, M., Evolution of root endosymbiosis with bacteria: how novel are nodules?, Trends Plant Sci., 2008, vol. 14, pp. 77–86.

    Article  Google Scholar 

  • Mergaert, P., Uchiumi, T., Alunni, B., et al., Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 5230–5235.

    Article  CAS  PubMed Central  PubMed  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 

  • Nazarov, V.I., Evolyutsiya ne po Darvinu (Non-Darwinian Evolution), Moscow: KomKniga, 2005.

    Google Scholar 

  • Oono, R., Denison, R.F., and Kiers, E.T., Controlling the reproductive fate of rhizobia: how universal are legume sanctions?, New Phytol., 2009, vol. 183, pp. 967–979.

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Popov, I.Yu., Ortogenez protiv darvinizma (Orthogenesis against Darwinism), St. Petersburg: Izd. S.-Peterb. Gos. Univ., 2005.

    Google Scholar 

  • Provorov, N.A., The relationship between the taxonomy of legumes and specificity of their interactions with rhizobia, Bot. Zh., 1992, vol. 77, no. 8, pp. 21–32.

    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 to organelles, Zh. Obshch. Biol., 2005, vol. 66, no. 5, pp. 371–388.

    CAS  PubMed  Google Scholar 

  • Provorov, N.A. and Tikhonovich, I.A., Ecological and genetic principles of plant breeding to increase the efficiency of interaction with microorganisms, S.-Kh. Biol., 2003, no. 3, pp. 11–25.

    Google Scholar 

  • Provorov, N.A. and Vorob’ev, N.I., The role of horizontal gene transfer in the evolution of nodule bacteria directed by the host plant, Usp. Sovrem. Biol., 2010, vol. 130, no. 4, pp. 336–345.

    Google Scholar 

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

    Article  CAS  PubMed  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. Popul. Biol., 2008, vol. 74, pp. 345–355.

    Article  PubMed  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, Tikhonovich, I.A., Ed., New York: NOVA Sci. Publ., 2010a.

  • 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. Popul. Biol., 2010b, vol. 78, pp. 259–269.

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

  • Provorov, N.A. and Vorobyov, N.I., Reconstruction of the adaptively advantages macro-evolutionary events in the mutualistic symbioses, in Evolutionary Biology: Mechanisms and Trends, Pontarotti, P., Ed., Heidelberg: Springer, 2012c, pp. 169–188.

    Chapter  Google Scholar 

  • Rodriguez, R.J., Freeman, D.C., McArthur, E.D., et al., Symbiotic regulation of plant growth, development and reproduction, Commun. Integrat. Biol., 2009, vol. 2, pp. 141–143.

    Google Scholar 

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

    Google Scholar 

  • Schmalhausen, I.I., Organizm kak tseloe v individual’nom i istoricheskom razvitii (Organism as a Whole in Individual and Historical Development), Moscow: Nauka, 1982.

    Google Scholar 

  • Schmalhausen, I.I., Puti i zakonomernosti evolyutsionnogo protsessa (Pathways and Patterns of the Evolutionary Process), Moscow: Nauka, 1983.

    Google Scholar 

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

    Chapter  Google Scholar 

  • Sprent, J.I., Nodulation in Legumes, Kew: Cromwell Press Ltd., 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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tikhonovich, I.A. and Provorov, N.A., From plantmicrobe 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., Microbiology is the basis of sustainable agriculture: an opinion, Ann. Appl. Biol., 2011, vol. 159, pp. 155–168.

    Article  CAS  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 

  • Timmers, A.C.S., Soupene, E., Auriac, M.C., et al., Saprophytic intracellular rhizobia in alfalfa nodules, Mol. Plant-Microbe Interact., 2000, vol. 13, pp. 1204–1213.

    Article  CAS  PubMed  Google Scholar 

  • Timofeev-Resovskii, N.V., Vorontsov, N.N., and Yablokov, A.V., Kratkii ocherk teorii evolyutsii (A Brief Sketch of the Theory of Evolution), 2nd ed., Moscow: Nauka, 1977.

    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 

  • Tsyganov, V.E., Voroshilova, V.A., Herrera-Cervera, J.A., et al., 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, pp. 521–530.

    Article  CAS  Google Scholar 

  • Tsyganova, A.V., Tsyganov, V.E., Borisov, A.Yu., et al., Comparative cytochemical analysis of the distribution of hydrogen peroxide in the nodules of pea mutant SGEFix-1 (sym40) and the original line SGE, Ekol. Genet., 2009, vol. 7, pp. 3–9.

    Google Scholar 

  • Udvardi, M.K. and Kahn, M.L., Evolution of the (brady) Rhizobium-legume symbiosis: why do bacteroids fix nitrogen?, Symbiosis, 1992, vol. 14, pp. 87–101.

    Google Scholar 

  • Veening, J.W., Stewart, E.J., Berngruber, T.W., et al., Bethedging and epigenetic inheritance in bacterial cell development, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 4393–4398.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van de Velde, W., Zehirov, G., Szatmari, A., et al., Plant peptides govern terminal differentiation of bacteria in symbiosis, Science, 2010, vol. 327, pp. 1122–1126.

    Article  PubMed  Google Scholar 

  • Vorobyov, N.I. and Provorov, N.A., Modeling the evolution of the legume-Rhizobium symbiosis to improve functional integration partners and ecological efficiency of their interaction, Ekol. Genet., 2010, vol. 8, no. 3, pp. 16–26.

    Google Scholar 

  • Vorobyeva, E.I., Problem of organism integrity and its perspectives, Biol. Bull. (Moscow), 2006, vol. 33, no. 5, pp. 427–436.

    Article  Google Scholar 

  • Wang, D., Yang, S., Tang, F., and Zhu, H., Symbiosis specificity in the legume-rhizobial mutualism, Cell. Microbiol., 2012, vol. 14, pp. 334–342.

    Article  PubMed  Google Scholar 

  • Yakovlev, G.P., Bobovye zemnogo shara (Legumes of the World), Leningrad: Nauka, 1991.

    Google Scholar 

  • Young, J.P.W., Crossman, L.C., Johnston, A.W.B., et al., The genome of Rhizobium leguminosarum has recognizable core and accessory components, Genome Biol., 2006, vol. 7, p. 34.

    Article  Google Scholar 

  • Zilber-Rosenberg, I. and Rosenberg, E., Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution, FEMS Microbiol. Rev., 2008, vol. 32, pp. 723–735.

    Article  CAS  PubMed  Google Scholar 

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Original Russian Text © N.A. Provorov, N.I. Vorobyov, 2013, published in Ekologicheskaya Genetika, 2013, Vol. 11, No. 1, pp. 12–22.

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Provorov, N.A., Vorobyov, N.I. Adaptive and progressive evolution of plant-microbial symbiosis. Russ J Genet Appl Res 4, 88–97 (2014). https://doi.org/10.1134/S2079059714020075

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