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.
Berg, L.S., Trudy po teorii evolyutsii (Works on the Theory of Evolution), Leningrad: Nauka, 1977.
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.
Brewin, N.J., Development of the legume root nodule, Annu. Rev. Cell Biol., 1991, vol. 7, pp. 191–226.
Brewin, N.J., Plant cell wall remodeling in the Rhizobium-legume symbiosis, Crit. Rev. Plant Sci., 2004, vol. 23, pp. 1–24.
Bronstein, J.L., The evolution of facilitation and mutualism, J. Ecol., 2009, vol. 97, pp. 1160–1170.
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.
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.
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.
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.
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.
Douglas, A.E., Symbiotic Interactions, Oxford: Oxford Univ. Press, 1994.
Downie, J.A. and Young, J.P.W., The ABC of symbiosis, Nature, 2001, vol. 412, pp. 597–598.
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.
Filipcenko, J., Variabilitat und Variation, Berlin: Borntrager, 1927.
Franche, C., Lindstrom, K., and Elmerich, C., Nitrogenfixing bacteria associated with leguminous and non-leguminous plants, Plant Soil, 2009, vol. 321, pp. 35–59.
Frank, S.A., Genetics of mutualism: the evolution of altruism between species, J. Theor. Biol., 1994, vol. 170, pp. 393–400.
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.
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.
Iordanskii, N.N., Charles Darwin and the problem of evolutionary progress, Zh. Obshch. Biol., 2010, vol. 71, no. 6, pp. 488–496.
Janzen, D.H., When is it coevolution?, Evolution, 1980, vol. 34, pp. 611–612.
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.
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.
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.
Maillet, F., Poinsot, V., Andre, O., et al., Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza, Nature, 2011, vol. 469, pp. 58–65.
Mayr, E., Populations, Species, and Evolution, Cambridge (Massachusetts): Harvard Univ., 1970.
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.
Margulis, L. and Sagan, D., Acquiring Genomes. A Theory of the Origins of Species, New York: Basic Books, 2002.
Markmann, K. and Parniske, M., Evolution of root endosymbiosis with bacteria: how novel are nodules?, Trends Plant Sci., 2008, vol. 14, pp. 77–86.
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.
Michod, R.D. and Roze, D., Transitions in individuality, Proc. Roy. Soc. Lond. B, 1997, vol. 264, pp. 953–857.
Nazarov, V.I., Evolyutsiya ne po Darvinu (Non-Darwinian Evolution), Moscow: KomKniga, 2005.
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.
Parniske, M., Arbuscular mycorrhiza: the mother of plant root endosymbioses, Nature. Rev. Microbiol., 2008, vol. 6, pp. 763–775.
Popov, I.Yu., Ortogenez protiv darvinizma (Orthogenesis against Darwinism), St. Petersburg: Izd. S.-Peterb. Gos. Univ., 2005.
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.
Provorov, N.A., Coevolution of rhizobia with legumes: facts and hypotheses, Symbiosis, 1998, vol. 24, pp. 337–367.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Seckbach, J., Symbiosis: Mechanisms and Model Systems, Dordrecht: Kluwer Acad. Publ., 2002.
Schmalhausen, I.I., Organizm kak tseloe v individual’nom i istoricheskom razvitii (Organism as a Whole in Individual and Historical Development), Moscow: Nauka, 1982.
Schmalhausen, I.I., Puti i zakonomernosti evolyutsionnogo protsessa (Pathways and Patterns of the Evolutionary Process), Moscow: Nauka, 1983.
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.
Sprent, J.I., Nodulation in Legumes, Kew: Cromwell Press Ltd., 2001.
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.
Stougaard, J., Genetics and genomics of root symbiosis, Curr. Opin. Plant Biol., 2001, vol. 4, pp. 328–335.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Vorobyeva, E.I., Problem of organism integrity and its perspectives, Biol. Bull. (Moscow), 2006, vol. 33, no. 5, pp. 427–436.
Wang, D., Yang, S., Tang, F., and Zhu, H., Symbiosis specificity in the legume-rhizobial mutualism, Cell. Microbiol., 2012, vol. 14, pp. 334–342.
Yakovlev, G.P., Bobovye zemnogo shara (Legumes of the World), Leningrad: Nauka, 1991.
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.
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.
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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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DOI: https://doi.org/10.1134/S2079059714020075