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Genetic and molecular basis of symbiotic adaptations

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We examined the population and molecular mechanisms of symbiotic adaptations contributing to the structural, functional, and genetic integration of nonrelated organisms. These adaptations are determined by group selection processes operating at the levels of integral super-species systems (holobionts) and their internal microbial communities. This type of selection is responsible for an increase in symbiosis integrity, which is dependent at the early stages of partners’ coevolution on their signaling interactions (cross-regulation of genes) and at the late stages on a allocation of hereditary material between partners (endosymbiotic gene transfer). The resulting increase in the adaptive potential of symbiotic systems is attributed to (i) intra- and interspecies partners’ altruism as a consequence of their mutualistic interactions; and (ii) the inheritance of microsymbionts by hosts as beneficial genetic determinants acquired from the environment in the course of adaptive coevolution. The first mechanism is attributed to the involvement of the host in cooperative adaptations arising within microbial populations and communities in the course of the inoculation and colonization of symbiotic niches. The second mechanism is attributed to realization of the pangenesis hypothesis, proposed by Ch. Darwin as a possible strategy for direct adaptation of organisms to the environment—an alternative to natural selection. In the course of symbiogenesis, this adaptation is implemented on the basis of ontogenetic programs that ensure transitions from an unstable (pseudo-vertical) transmission of facultative symbionts in host progenies towards a stable (transovarian, cytoplasmic) inheritance of obligatory symbionts and cellular organelles.

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References

  • Bary de, A., Die Erscheinung der Symbiose, Strasburg: Verlag von Karl J. Trübner, 1879.

    Google Scholar 

  • Batygina, T.B., Morphogenetic Developmental Programs. Stem Cells, New York: Nova Biomed. Books, 2011.

    Google Scholar 

  • Berg, L.S., Nomogenesis or evolution based on the principles, in Trudy po teorii evolyutsii (Scientific Works on the Theory of Evolution), Leningrad: Nauka, 1977, pp. 95–338.

    Google Scholar 

  • Bidartondo, M.I., The evolutionary ecology of mycoheterotrophy, New Phytol., 2005, vol. 167, pp. 335–352.

    Article  PubMed  Google Scholar 

  • Blyakher, L.Ya., Problema nasledovaniya priobretennykh priznakov (Problem of Inheritance of Acquired Features), Moscow: Nauka, 1971.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chan, C.X., Gross, J., Yoon, H.S., and Bhattacharya, D., Plastid origin and evolution: new models provide insights into old problems, Plant Physiol., 2011, vol. 155, no. 4, pp. 1552–1560.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Darwin, Ch., The Origin of Species by Means of Natural Selection, London: John Murray, 1859.

    Google Scholar 

  • Darwin, Ch., The Variation of Animals and Plants under Domestication, London: John Murray, 1868.

    Google Scholar 

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

    CAS  PubMed  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  CAS  PubMed  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 

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

    Google Scholar 

  • Ferguson, B.J., Indrasumunar, A., Hayshi, S., et al., Molecular analysis of legume nodule development and autoregulation, J. Integr. Plant Biol., 2010, vol. 52, pp. 61–76.

    Article  CAS  PubMed  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 

  • Galhardo, R.S., Hastings, P.J., and Rosenberg, S.M., Mutation as a stress response and the regulation of evolvability, Crit. Rev. Biochem. Mol. Biol., 2007, vol. 42, pp. 399–435.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gingeras, T.R., Origin of phenotypes: genes and transcripts, Genome Res., 2007, vol. 17, pp. 682–690.

    Article  CAS  PubMed  Google Scholar 

  • Gundel, P.E., Batista, W.B., Texeira, M., et al., Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency, Proc. R. Soc. B, 2008, vol. 275, pp. 897–905.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hamilton, W.D.J., The genetical evolution of social behavior, J. Theor. Biol., 1964, vol. 7, pp. 1–16.

    Article  CAS  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 

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

    Article  Google Scholar 

  • Koga, R., Tsuchida, T., and Fukatsu, T., Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid, Proc. R. Soc. B, 2003, vol. 270, pp. 2543–2550.

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu, Y.-S., Zhou, X.M., Zhu, M.-X., et al., Darwin’s con-tributions to genetics, J. Appl. Genet., 2009, vol. 50, pp. 177–184.

    Article  PubMed  Google Scholar 

  • Lobashev, M.E., Genetika (Genetics), Leningrad: Leningr. Gos. Univ., 1967, 2nd ed.

    Google Scholar 

  • Margulis, L., Symbiosis in Cell Evolution, New York: W.H. Freeman, 1981.

    Google Scholar 

  • Markov, A.V. and Zakharov, I.A., The parasitic bacterium Wolbachia and the origin of the eukaryotic cell, Paleontol. J., 2006, vol. 40, no. 2, pp. 115–124.

    Article  Google Scholar 

  • Martin, W., Gene transfer from organelles to the nucleus: frequent and in big chunks, Proc. Natl. Acad. Sci. U.S.A., 2003, vol. 100, pp. 8612–8614.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matveeva, T.V., Bogomaz, D.I., Pavlova, O.A., et al., Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature, Mol. Plant-Microbe Interact., 2012, vol. 25, pp. 1542–1551.

    Article  CAS  PubMed  Google Scholar 

  • Maynard Smith, J., Generating novelty by symbiosis, Nature, 1989, vol. 341, pp. 284–285.

    Article  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 

  • Mayr, E., Populations, Species, and Evolution: An Abridgment of Animal Species and Evolution, Harvard: Belknap Press, 1970.

    Google Scholar 

  • Mehrotra, S. and Goyal, V., Agrobacterium-mediated gene transfer in plants and biosafety considerations, Appl. Biochem. Biotechnol., 2012, vol. 168, pp. 1953–1975.

    Article  CAS  PubMed  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. U.S.A., 2006, vol. 103, pp. 5230–5235.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Merezhkovskii, K.S., Teoriya dvykh plazm kak osnova simbiogenezisa, novogo ucheniya o proiskhozhdenii organizmov (Theory of Two Plasmas as the Basis of Symbiogenesis, New Theory on the Origin of the Organisms), Kazan: Imper. Univ., 1909.

    Google Scholar 

  • Mikheyev, A.S., Mueller, U.G., and Boomsma, J.J., Population genetic signatures of diffuse co-evolution between leaf-cutting ants and their cultivar fungi, Mol. Ecol., 2007, vol. 1, pp. 209–216.

    Google Scholar 

  • Moore, C.E. and Archibald, J.M., Nucleomorph genomes, Annu. Rev. Genet., 2009, vol. 43, pp. 251–264.

    Article  CAS  PubMed  Google Scholar 

  • Moran, N.A., Genome evolution in symbiotic bacteria, ASM News, 2002, vol. 68, pp. 499–505.

    Google Scholar 

  • Nardon, P. and Charles, H., Morphological aspects of symbiosis, in Symbiosis: Mechanisms and Model Systems, Seckbach, J., Ed., Dordrecht: Kluwer, 2002, pp. 13–44.

    Google Scholar 

  • Negri, I., Franchini, A., Gonella, E., et al., Unraveling the Wolbachia evolutionary role: the reprogramming of the host genomic imprinting, Proc. Biol. Sci., 2009, vol. 276, pp. 2485–2491.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nikoh, N., Tanaka, K., Shibata, F., et al., Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes, Genome Res., 2008, vol. 18, pp. 272–280.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pichon, S., Bouchon, D., Cordaux, R., et al., Conservation of the type IV secretion system throughout Wolbachia evolution, Biochem. Biophys. Res. Commun., 2009, vol. 385, pp. 557–562.

    Article  CAS  PubMed  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 Central  PubMed  Google Scholar 

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

    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 Tikhonovich, I.A., Super-species genetic systems, Zh. Obshch. Biol., 2014, vol. 75, no. 4, pp. 247–260.

    Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Population genetics of nodule bacteria: simulation of cyclic processes in bacterial-plant system, Russ. J. Genet., 1998, vol. 34, no. 12, pp. 1704–1711.

    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, no. 3, pp. 262–272.

    Article  PubMed  Google Scholar 

  • Provorov, N.A. and Vorobyov, N.I., Co-evolution 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 Principles of Evolution of the Plant-Microbe Symbiosis), Tikhonovich, I.A., Ed., St. Petersburg: Inform-Navigator, 2012b.

  • Ran, L., Larsson, J., Vigil-Stenman, T., et al., Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular Cyanobacterium, PLoS One, 2010, vol. 5, pp. 1–11.

    Article  Google Scholar 

  • Raven, J.A. and Allen, J.F., Genomics and chloroplast evolution: what did cyanobacteria do for plants? Genome Biol., 2003, vol. 209, p. R209.

    Article  Google Scholar 

  • Simoes, M. C., Simoes, L., and Vieira, M.J., A review of current and emergent biofilm control strategies, Food Sci. Technol., 2010, vol. 43, pp. 573–583.

    CAS  Google Scholar 

  • Sprent, J.I., West African legumes: the role of nodulation and nitrogen fixation, New Phytol., 2005, vol. 167, pp. 326–330.

    Article  CAS  PubMed  Google Scholar 

  • Sugawara, M., Epstein, B., Badgley, B., et al., Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies, Genome Biol., 2013, vol. 14, p. R17.

    Article  PubMed Central  PubMed  Google Scholar 

  • Thompson, J.N. and Burdon, J., Gene-for-gene co-evolution between plants and parasites, Nature, 1992, vol. 360, pp. 121–125.

    Article  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 

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

    Google Scholar 

  • van der Giezen, M., Tovar, J., and Clark, C.G., Mitochondrion-derived organelles in protists and fungi, Int. Rev. Cytol., 2005, vol. 244, pp. 175–225.

    Article  PubMed  Google Scholar 

  • Vorobyov, N.I. and Provorov, N.A., Simulation of evolution of legumes-rhizobial symbiosis in conditions of environmental changes, Ekol. Genet., 2014, (in press).

    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 

  • Wells, J.E. and Russell, J.B., Why do many ruminal bacteria die and lyse so quickly? J. Dairy Sci., 1996, vol. 79, pp. 1487–1495.

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson, D.M., Bacterial ecology, antibiotics and selection for virulence, Ecol. Lett., 1999, vol. 2, pp. 207–209.

    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 

  • Zimmer, C., Wolbachia: a tale of sex and survival, Science, 2001, vol. 292, pp. 1093–1095.

    Article  CAS  PubMed  Google Scholar 

Download references

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Correspondence to N. A. Provorov.

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Original Russian Text © N.A. Provorov, I.A. Tikhonovich, 2014, published in Uspekhi Sovremennoi Biologii, 2014, Vol. 134, No. 3, pp. 211–226.

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Provorov, N.A., Tikhonovich, I.A. Genetic and molecular basis of symbiotic adaptations. Biol Bull Rev 4, 443–456 (2014). https://doi.org/10.1134/S2079086414060061

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