Abstract
Mutualistic symbioses represent the favorable models for analyzing the tradeoff between progressive and adaptive evolution which remains unclear for the unitary (“free-living”) organisms. Using the model of N2-fixing legume-rhizobia symbiosis we demonstrate that acquisition by plants of the novel extracellular and intracellular compartments (infection threads, symbiosomes) for hosting the bacteria induce in their populations novel selective pressures in favor of host-beneficial (“altruistic”) traits (intensive in planta N2 fixation, export of fixed nitrogen into the plant tissues, differentiation into the non-reproducible bacteroids). Due to colonization of extracellular infection threads, the degree of clonality is increased in the endosymbiotic bacterial populations which opens prospects for the interdeme selection for an increased activity of symbiotic N2 fixation. When bacteria colonize the intracellular symbiosomes, this activity is further elevated due to the kin selection in favor of irreversible bacteroid differentiation. The revealed feedbacks between the macroevolutionary events occurring in hosts and the selective pressures induced in microsymbionts may be responsible for the rapid filiations from regulatory-type anodular rhizospheric/endophytic associations (based on stimulation of the growth and assimilatory capacities of roots by the bacteria-produced auxins) to the nutritional-type nodular symbioses (based on the novel organogenesis ensuring conditions optimal for the symbiotic N2 fixation).
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References
Amarger N, Lobreau JP (1982) Quantitative study of nodulation competitiveness in Rhizobium strains. Appl Environ Microbiol 44:583–588
Berg LS (1969) Nomogenesis or evolution determined by law. MIT Press, Massachusetts
Beringer JE, Brewin NJ, Johnston AWB (1980) The genetic analysis of Rhizobium in relation to symbiotic nitrogen fixation. Heredity 45:161–186
Brewin NJ (2004) Plant cell wall remodeling in the Rhizobium-legume symbiosis. Crit Rev Plant Sci 23:1–24
Bronstein JL (2009) The evolution of facilitation and mutualism. J Ecol 97:1160–1170
Broughton WJ, Samrey U, Stanley J (1987) Ecological genetics of Rhizobium meliloti: symbiotic plasmid transfer in the Medicago sativa rhizosphere. FEMS Microbiol Lett 40:251–255
Bryan JA, Berlyn GP, Gordon JC (1996) Towards a new concept of the evolution of symbiotic nitrogen fixation in the Leguminosae. Plant Soil 186:151–159
Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat Rev Microbiol 7:312–320
Denison RF, Kiers ET (2004a) Lifestyle alternatives for rhizobia: mutualism, parasitism and foregoing symbiosis. FEMS Microbiol Lett 237:187–193
Denison RF, Kiers ET (2004b) Why are most rhizobia beneficial to their plant hosts, rather than parasitic? Microbes Infect 6:1235–1239
Dorosinsky LM, Lazareva NM (1968) On the specificity of soybean and lupine nodule bacteria. Mikrobiologia [in Russian] 37:115–121
Douglas AE (1994) Symbiotic interactions. Oxford University Press, Oxford
Frank SA (1994) Genetics of mutualism: the evolution of altruism between species. J Theor Biol 170:393–400
Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, 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 WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Verméglio A, Médigue C, Sadowsky M (2007) Legume symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312
Gorsuch RL (1983) Factor analysis. Lawrence Erlbaum Associates, Hillsdale
Ichige A, Walker GC (1997) Genetic analysis of the Rhizobium meliloti bacA gene: functional interchangeability with the Escherichia coli sbmA gene and phenotypes of mutants. J Bacteriol 179:209–216
Iordansky NN (2010) Charles Darwin and the problem of evolutionary progress. Zhurnal Obshei Biologii [in Russian] 71:488–496
Janzen DH (1980) When is it coevolution? Evolution 34:611–612
Kalevitch MV, Kefeli VI, Borsari B, Davis J, Bolous G (2004) Final version chemical signaling during organisms’ growth and development. J Cell Molec Biol 3:95–102
Kaneko T, Minamisawa K, Isawa T, Nakatsukasa H, Mitsui H, Kawaharada Y, Nakamura Y, Watanabe A, Kawashima K, Ono A, Shimizu Y, Takahashi C, Minami C, Fujishiro T, Kohara M, Katoh M, Nakazaki N, Nakayama S, Yamada M, Tabata S, Sato S (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17:37–50
Kennedy IR (1996) Facilitating the evolution of an effective N2-fixing association between Azospirillum and wheat. In: Abstracts of the 7th International Symposium on Biological Nitrogen Fixation, Haisalabad, p 46
Kistner C, Parniske M (2002) Evolution of signal transduction in intercellular symbiosis. Trends Plant Sci 7:511–518
Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Becard G, Denarie J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–65
Marchetti M, Capela D, Glew M, Cruveiller S, Chane-Woon-Ming B, Gris C, Timmers T, Poinsot V, Gilbert LB, Heeb P, Medigue C, Batut J, Masson-Boivin C (2010) Experimental evolution of a plant pathogen into legume symbionts. PLoS Biol 8:1–10
Margulis L (2009) Symbiogenesis. A new principle of evolution rediscovery of Boris Mikhaylovich Kozo-Polyansky (1890–1957) In: Kolchinsky EI (ed) Charles Darwin and modern biology. Nestor-Historia, St-Petersburg, pp 34–48
Maynard Smith J, Feil EJ, Smith NH (2000) Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 22:1115–1122
Maynard Smith J, Smith NH, O’Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci U S A 90:4384–4388
Michod RD, Roze D (1997) Transitions in individuality. Proc Roy Soc Lond B 264:853–857
Ochman H, Elwyn S, Moran NA (1999) Calibrating bacterial evolution. Proc Natl Acad Sci U S A 96:12638–12643
Ohyama T, Ohtake N, Sueyoshi K, Tewari K, Takahashi Y, Ito S, Nishiwaki T, Nagumo Y, Ishii S, Sato T (2008) Nitrogen fixation and metabolism in soybean plants. In: Couto GN (ed) Nitrogen fixation research progress. Nova Science Publishers, New York, pp 15–109
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Rev Microbiol 6:763–775
Pretorius-Güth IM, Pühler A, Simon R (1990) Conjugal transfer of megaplasmid 2 between Rhizobium meliloti strains in alfalfa nodules. Appl Environ Microbiol 56:2354–2359
Provorov NA (1994) The interdependence between taxonomy of legumes and specificity of their interaction with rhizobia in relation to evolution of the symbiosis. Symbiosis 17:183–200
Provorov NA (1998) Coevolution of rhizobia with legumes: facts and hypotheses. Symbiosis 24:337–367
Provorov NA, Tikhonovich IA (2003) Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis. Genet Res Crop Evolut 50:89–99
Provorov NA, Vorobyov NI (2000) Population genetics of rhizobia: construction and analysis of an “infection and release” model. J Theor Biol 205:105–119
Provorov NA, Vorobyov NI (2006) Interplay of Darwinian and frequency-dependent selection in the host-associated microbial populations. Theor Popul Biol 70:262–272
Provorov NA, Vorobyov NI (2008) Equilibrium between the “genuine mutualists” and “symbiotic cheaters” in the bacterial population co-evolving with plants in a facultative symbiosis. Theor Populat Biol 74:345–355
Provorov NA, Vorobyov NI (2009) Host plant as on organizer of microbial evolution in the beneficial symbioses. Phytochem Rev 8:519–534
Provorov NA, Vorobyov NI (2010a) Tikhonovich IA (ed) Evolutionary genetics of plant–microbe symbioses. NOVA Science Publishers, New York
Provorov NA, Vorobyov NI (2010b) Simulation of evolution implemented in the mutualistic symbioses towards enhancing their ecological efficiency, functional integrity and genotypic specificity. Theor Populat Biol 78:259–269
Ruse M (2000) Limits to our knowledge of evolution. In: Clegg MT, Hecht MK, MacIntryre RJ (eds) Evolutionary biology, vol 32. Kluwer Academic Publishers, New York, pp 3–31
Saikia SP, Jain V, Khetarpal S, Aravind S (2007) Dinitrogen fixation activity of Azospirillum brasilense in maize (Zea mays). Curr Sci 93:1296–1300
Schmalhausen I (1983) Pathways and regularities of the evolutionary process (in Russian). Nauka, Moscow
Seckbach J (2002) Symbiosis: mechanisms and model systems. Kluwer Academic Publishers, Dordrecht
Sessitsch A, Howieson JG, Perret X, Antoun H, Martinez-Romero E (2002) Advances in Rhizobium research. Crit Rev Plant Sci 21:323–378
Shtark OY, Borisov AY, Zhukov VA, Provorov NA, Tikhonovich IA (2010) Intimate associations of beneficial soil microbes with host plants. In: Dixon R, Tilston E (eds) Soil microbiology and sustainable crop production. Springer, Berlin, pp 119–196
Souza V, Nguyen TT, Hudson RR, Pinero D, Lenski RE (1992) Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex? Proc Natl Acad Sci U S A 89:8389–8393
Sprent JI (2001) Nodulation in legumes. Cromwell Press Ltd, Kew
Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25
Stougaard J (2001) Genetics and genomics of root symbiosis. Curr Opin Plant Biol 4:328–335
Streeter J (1995) Integration of plant and bacterial metabolism in nitrogen fixing systems. In: Tikhonovich IA, Provorov NA, Romanov VI, Newton WE (eds) Nitrogen fixations: fundamentals and applications. Kluwer Academic Publishers, Dordrecht, pp 67–76
Tikhonovich IA, Provorov NA (2009) From plant–microbe interactions to symbiogenetics: a universal paradigm for the inter-species genetic integration. Ann Appl Biol 154:341–350
Tikhonovich IA, Provorov NA (2012) Development of approaches for symbiogenetics to study the variability and heredity in the super-species systems. Russ J Genet 48 (accepted)
Tort L, Balasch JC, Mackenzie S (2003) Fish immune system. The crossroads between innate and adaptive responses. Immunologia 22:277–286
van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, Satiat-Jeunemaître B, Alunni B, Bourge M, Kucho K, Abe M, Keresz A, Maroti G, Toshiki T, Kondorosi E, Mergaert P (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:122–1126
van Ham RCHJ, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, Fernández JM, Jiménez L, Postigo M, Silva FJ, Tamames J, Viguera E, Latorre A, Valencia A, Morán F, Moya A (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100:581–586
Vieille C, Elmerich C (1990) Characterization of two Azospirillum brasilense Sp7 plasmid genes homologous to Rhizobium meliloti nodPQ. Molec Plant–Microbe Interact 6:389–400
Vieille C, Elmerich C (1992) Characterization of an Azospirillum brasilense Sp7 plasmid gene homologous to Alcaligenes eutrophis phbB and Rhizobium meliloti nodG. Molec Gen Genet 231:375–384
Yakovlev GP (1991) Legumes of the globe (in Russian). Nauka, Leningrad
Young JPW, Crossman LC, Johnston AWB, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson ARJ, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Noebertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7:R34
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Supported by grants from RFBR (12-04-00409a), RFBR-NWO (047.018.001), Scientific School 3440.2010.4, and State Contract (2.740.11.0698).
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Provorov, N.A., Vorobyov, N.I. (2012). Reconstruction of the Adaptively Advantages Macroevolutionary Events in the Mutualistic Symbioses. In: Pontarotti, P. (eds) Evolutionary Biology: Mechanisms and Trends. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30425-5_10
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