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Phytochemistry Reviews

, 8:519 | Cite as

Host plant as an organizer of microbial evolution in the beneficial symbioses

  • Nikolai A. Provorov
  • Nikolai I. Vorobyov
Article

Abstract

Evolution of beneficial plant–microbe symbioses is presented as a result of selective processes induced by hosts in the associated microbial populations. These processes ensure a success of “genuine mutualists” (which benefit the host, often at the expense of their own fitness) in competition with “symbiotic cheaters” (which consume the resources provided by host without expressing the beneficial traits). Using a mathematical model describing the cyclic microevolution of rhizobia–legume symbiosis, we suggest that the selective pressures in favor of N2-fixing (Fix+) strains operate within the in planta bacterial population due to preferential allocation of C resources into Fix+ nodules (positive partners’ feedbacks). Under the clonal infection of nodules, Fix+ strains (“genuine mutualists”) are supported by the group (inter-deme, kin) selection while under the mixed infections, this selection is ineffective since the Fix+ strains are over-competed by Fix ones (“symbiotic cheaters”) in the nodular habitats. Nevertheless, under mixed infections, Fix+ strains may be supported due to the coevolutionary responses form plant population which induce the mutualism-specific types of natural (group, individual) selection including the frequency dependent selection implemented in rhizobia population during the competition for host infection. Using the model of multi-strain bacterial competition for inoculation of symbiotic (rhizospheric, nodular) habitats, we demonstrate that the individual selection in favor of host-specific mutualist genotypes is more intensive than in favor of non-host-specific genotypes correlating the experimental data on the coordinated increases of symbiotic efficiency and specificity in the rhizobia–legume coevolution. However, an overall efficiency of symbiotic system is maximal when the non-host-specific mutualists are present in rhizobia population, and selection in favor of these mutualists operating at the whole population level is of key importance for improving the symbiosis. Construction of the agronomically valuable plant–microbe systems should provide the optimization of host-specific versus non-host-specific mutualists’ composition in legume inoculants combined with the clonal penetration of these mutualists into the nodules.

Keywords

Biological altruism Darwinian, frequency-dependent and group (inter-deme, kin) selection Positive partners’ feedbacks Rhizobia–legume symbiosis Symbiotic N2 fixation 

Notes

Acknowledgments

Supported by Russian Foundation of Basic Research (grant 09-04-00907a).

References

  1. Amarger N, Lobreau JP (1982) Quantitative study of nodulation competitiveness in Rhizobium strains. Appl Environ Microbiol 44:583–588PubMedGoogle Scholar
  2. Balachandar D, Raja P, Kumar K et al (2007) Non-rhizobial nodulation in legumes. Biotechnol Mol Biol Rev 2:49–57Google Scholar
  3. Bassam BJ, Mahanty HK, Gresshoff PM (1987) Symbiotic interaction of auxotrophic mutants of Rhizobium trifolii with white clover (Trifolium repens). Endocyt C Res 4:331–347Google Scholar
  4. Beattie GA, Clayton MK, Handelsman J (1989) Quantitative comparison of the laboratory and field competitiveness of Rhizobium leguminosarum biovar phaseoli. Appl Environ Microbiol 55:2755–2761PubMedGoogle Scholar
  5. Berg G, Müller H, Zachow C et al (2008) Endophytes: structural and functional diversity and biotechnological applications in control of plant pathogens. Ecol Genet 6:17–26Google Scholar
  6. Bethlenfalvay GI, Abu-Shakra SS, Phillips DA (1978) Interdependence of nitrogen nutrition and photosynthesis in Pisum sativum L. II. Host plant response to nitrogen fixation by Rhizobium strains. Plant Physiol 62:131–133PubMedCrossRefGoogle Scholar
  7. Beveridge CA, Mathesius U, Rose RJ et al (2007) Common regulatory themes in meristem development and whole-plant homeostasis. Curr Opin Plant Biol 10:44–51PubMedCrossRefGoogle Scholar
  8. Bosworth AH, Williams MK, Albrecht KA et al (1992) Alfalfa yield response to inoculation with recombinant strains of Rhizobium meliloti with an extra copy of dctABD and/or modified nifA expression. Appl Environ Microbiol 60:3815–3822Google Scholar
  9. Brewin NJ (1998) Tissue and cell invasion by Rhizobium: the structure and development of infection threads and symbiosomes. In: Spaink H, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Molecular biology of model plant-associated bacteria. Kluwer, DordrechtGoogle Scholar
  10. Brewin NJ (2004) Plant cell wall remodeling in the Rhizobium–legume symbiosis. Crit Rev Plant Sci 23:1–24CrossRefGoogle Scholar
  11. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304CrossRefGoogle Scholar
  12. Bryan JA, Berlyn GP, Gordon JC (1996) Towards a new concept of the evolution of symbiotic nitrogen fixation in the Leguminosae. Plant Soil 186:151–159CrossRefGoogle Scholar
  13. Darlington PJ (1978) Altruism: its characteristics and evolution. Proc Natl Acad Sci USA 75:385–389PubMedCrossRefGoogle Scholar
  14. Denison RF (2000) Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am Nat 156:567–576CrossRefGoogle Scholar
  15. Dorosinsky LM, Lazareva NM (1968) On the specificity of soybean and lupine nodule bacteria. Mikrobiologia 37:115–121 (in Russian)Google Scholar
  16. Douglas AE (1994) Symbiotic interactions. Oxford University Press, OxfordGoogle Scholar
  17. Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81:599–603CrossRefGoogle Scholar
  18. Dyakov YT, Dzhavakhiya V, Korpela T (2007) Comprehensive and molecular phytopathology. Elsevier, AmsterdamGoogle Scholar
  19. Foster KR, Kokko H (2006) Cheating can stabilize cooperation in mutualisms. Proc Roy Soc B 273:2233–2239CrossRefGoogle Scholar
  20. Frank SA (1992) Models of plant–pathogen co-evolution. Trends Genet 8:213–219PubMedGoogle Scholar
  21. Frank SA (1994) Genetics of mutualism: the evolution of altruism between species. Theor Biol 170:393–400CrossRefGoogle Scholar
  22. Frank SA (1996) Host-symbiont conflict over the mixing of symbiotic lineages. Proc Roy Soc Lond B 263:339–344CrossRefGoogle Scholar
  23. Graften A (2007) Detecting kin selection at work using inclusive fitness. Proc Roy Soc Lond B 274:713–719CrossRefGoogle Scholar
  24. Guinel FC, Geil RD (2002) A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment of these two symbioses. Can J Bot 80:695–720CrossRefGoogle Scholar
  25. Gundel PE, Batista WB, Texeira M et al (2008) Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency. Proc Roy Soc B 275:897–905CrossRefGoogle Scholar
  26. Haldane JBS (1932) The causes of evolution. Longmans, Green & Co, New YorkGoogle Scholar
  27. Hamilton WDJ (1964) The genetical evolution of social behavior. J Theor Biol 7:1–16PubMedCrossRefGoogle Scholar
  28. Herre EA, Knowlton N, Mueller UG et al (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53PubMedCrossRefGoogle Scholar
  29. Jones KM, Kobayashi H, Davies BW et al (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev 5:619–633CrossRefGoogle Scholar
  30. Kaminski PA, Batut J, Boistard P (1998) A survey of symbiotic nitrogen fixation by rhizobia. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Molecular biology of model plant-associated bacteria. Kluwer, DordrechtGoogle Scholar
  31. Kiers ET, Rousseau RA, West SA et al (2003) Host sanctions and the legume-Rhizobium mutualism. Nature 425:78–81PubMedCrossRefGoogle Scholar
  32. Kinkema M, Scott PL, Gresshoff PM (2006) Legume nodulation: successful symbiosis through short- and long-distance signaling. Funct Plant Biol 33:707–721CrossRefGoogle Scholar
  33. Kistner C, Parniske M (2002) Evolution of signal transduction in intercellular symbiosis. Trends Plant Sci 7:511–518PubMedCrossRefGoogle Scholar
  34. Kneip C, Lockhart P, Voß C et al (2007) Nitrogen fixation in eukaryotes—new models for symbiosis. BMC Evol Biol 7:55PubMedCrossRefGoogle Scholar
  35. Kurchak ON, Provorov NA, Simarov BV (2001) Plasmid pSym1-32 of Rhizobium leguminosarum bv. viceae controlling nitrogen fixing activity, effectiveness of symbiosis, competitiveness and acid tolerance. Russ J Genet 37:1025–1031CrossRefGoogle Scholar
  36. Laguerre G, Mavingui P, Allard MR et al (1996) Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction lengths polymorphism analysis of chromosomal and symbiotic gene regions: application to Rhizobium leguminosarum and its different biovars. Appl Environ Microbiol 62:2029–2036PubMedGoogle Scholar
  37. Lugtenberg BJJ, Dekkers L, Bloemberg G (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490PubMedCrossRefGoogle Scholar
  38. Maynard Smith J (1964) Group selection and kin selection. Nature 201:1145–1147CrossRefGoogle Scholar
  39. Mettler LE, Gregg TG (1969) Population genetics and evolution. Prentice-Hall, Inc, Englewood CliffsGoogle Scholar
  40. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection on a birth-and-death process. Genome Res 8:1113–1130PubMedGoogle Scholar
  41. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  42. Nester E, Wood D, Pantoja M, Liu P (2004) Agrobacterium–plant interactions: unfinished business and continuing surprises. In: Tikhonovich IA, Lugtenberg BJJ, Provorov NA (eds) Biology of plant–microbe interactions. Biont, St.-PetersburgGoogle Scholar
  43. Pankhurst CE, MacDonald PE, Reeves JM (1986) Enhanced nitrogen fixation and competitiveness for nodulation of Lotus pedunculatus by a plasmid-cured derivative of Rhizobium loti. J Gen Microbiol 132:2321–2328Google Scholar
  44. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedCrossRefGoogle Scholar
  45. Parsons R (2002) Nodule infection and regulation in the GunneraNostoc symbiosis. Proc Roy Irish Acad 102B(1):41–43CrossRefGoogle Scholar
  46. Person C, Samborski DJ, Rohringer R (1962) The gene-for-gene concept. Nature 194:561–562PubMedCrossRefGoogle Scholar
  47. Plazinski J (1981) Isolation of ineffective and high-effective mutant strains of Rhizobium species using translocatable drug-resistance elements as mutagens. Acta Microbiol Polon 30:89–95Google Scholar
  48. Provorov NA (1994) The interdependence between taxonomy of legumes and specificity of their interaction with rhizobia in relation to evolution of the symbiosis. Symbiosis 17:183–200Google Scholar
  49. Provorov NA (1998) Coevolution of rhizobia with legumes: facts and hypotheses. Symbiosis 24:337–367Google Scholar
  50. Provorov NA, Tikhonovich IA (2003) Genetic resources for improving nitrogen fixation in legume–rhizobia symbiosis. Genet Res Crop Evol 50:89–99CrossRefGoogle Scholar
  51. Provorov NA, Vorobyov NI (2000) Population genetics of rhizobia: construction and analysis of an “infection and release” model. J Theor Biol 205:105–119PubMedCrossRefGoogle Scholar
  52. Provorov NA, Vorobyov NI (2006) Interplay of Darwinian and frequency-dependent selection in the host-associated microbial populations. Theor Popul Biol 70:262–272PubMedCrossRefGoogle Scholar
  53. Provorov NA, Vorobyov NI (2008a) Evolution of symbiotic bacteria in “plant–soil” systems: interplay of molecular and population mechanisms. In: Kim MB (ed) Progress in environmental microbiology. Nova Sci Publ Inc, New YorkGoogle Scholar
  54. Provorov NA, Vorobyov NI (2008b) Simulation of plant–bacteria co-evolution in the mutually beneficial symbiosis. Ecol Genet 6:34–47Google Scholar
  55. Provorov NA, Borisov AY, Tikhonovich IA (2002) Developmental genetics and evolution of symbiotic structures in nitrogen-fixing nodules and arbuscular mycorrhiza. J Theor Biol 214:215–232PubMedCrossRefGoogle Scholar
  56. Ruse M (2000) Limits to our knowledge of evolution. In: Clegg MT, Hecht MK, Macinryre RJ (eds) Evolutionary biology. Kluwer, New York, pp 3–33Google Scholar
  57. Schardl CL, Leuchtmann A, Chung KR et al (1997) Coevolution by common descent of fungal symbionts (Epichloe spp.) and grass hosts. Mol Biol Evol 14:133–143Google Scholar
  58. Selander RK, Caugant DA, Ochman H et al (1986) Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol 51:873–884PubMedGoogle Scholar
  59. Sharypova LA, Yurgel SN, Keller M et al (1998) The eff-482 locus of Sinorhizobium meliloti CXM1–105 that influences symbiotic effectiveness consists of three genes encoding an endoglucanase, a transcriptional regulator and an adenylate cyclase. Mol Gen Genet 261:1032–1044Google Scholar
  60. Simms EL, Taylor DL (2002) Partner choice in nitrogen-fixing mutualisms of legumes and rhizobia. Integr Comp Biol 42:369–380CrossRefGoogle Scholar
  61. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San DiegoGoogle Scholar
  62. Sprent JI (2001) Nodulation in legumes. Cromwell Press Ltd, KewGoogle Scholar
  63. Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25PubMedCrossRefGoogle Scholar
  64. Streeter J (1995) Integration of plant and bacterial metabolism in nitrogen fixing systems. In: Tikhonovich IA, Provorov NA, Romanov VI, Newton WE (eds) Nitrogen fixation: fundamentals and applications. Kluwer, DordrechtGoogle Scholar
  65. Tikhonovich IA, Provorov NA (2007) Beneficial plant–microbe interactions. In: Dyakov YT, Dzhavakhiya V, Korpela T (eds) Comprehensive and molecular phytopathology. Elsevier, AmsterdamGoogle Scholar
  66. Tikhonovich IA, Provorov NA (2009) From plant–microbe interactions to symbiogenetics: a universal paradigm for the inter-species genetic integration. Ann Appl Biol 154:341–350CrossRefGoogle Scholar
  67. Vorobyov NI, Provorov NA (2008) Simulation of evolution of legume–rhizobia symbiosis under the multi-strain bacterial competition for inoculation of symbiotic habitats. Ecol Genet 6:3–11 (in Russian)Google Scholar
  68. West SA, Murray MG, Machado CA et al (2001) Testing Hamilton’s rule with competition between relatives. Nature 409:510–513PubMedCrossRefGoogle Scholar
  69. Williams GS (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.All-Russia Research Institute for Agricultural MicrobiologySt.-Petersburg, Pushkin-8Russia

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