Plant and Soil

, Volume 194, Issue 1–2, pp 185–192 | Cite as

The impact of molecular systematics on hypotheses for the evolution of root nodule symbioses and implications for expanding symbioses to new host plant genera

  • Susan M. Swensen
  • Beth C. Mullin


Current taxonomic schemes place plants that can participate in root nodule symbioses among disparate groups of angiosperms. According to the classification scheme of Cronquist (1981) which is based primarily on the analysis of morphological characters, host plants of rhizobial symbionts are placed in subclasses Rosidae and Hamamelidae, and those of Frankia are distributed among subclasses Rosidae, Hamamelidae, Magnoliidae and Dilleniidae. This broad phylogenetic distribution of nodulated plants has engendered the notion that nitrogen fixing endosymbionts, particularly those of actinorhizal plants, can interact with a very broad range of unrelated host plant genotypes. New angiosperm phylogenies based on DNA sequence comparisons reveal a markedly different relationship among nodulated plants and indicate that they form a more coherent group than has previously been thought (Chase et al., 1993; Swensen et al., 1994; Soltis et al., 1995). Molecular data support a single origin of the predisposition for root nodule symbiosis (Soltis et al., 1995) and at the same time support the occurrence of multiple origins of symbiosis within this group (Doyle, 1994; Swensen, 1996; Swensen and Mullin, In Press).

actinorhizal plants evolution nitrogen fixation phylogenetic hypotheses 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akkermans A D L, Hafeez F, Roelofsen W, Chaudhary A H and Baas R 1983 Ultrastructure and nitrogenase activity of Frankia grown in pure culture and in actinorhizae of Alnus, Colletia and Datisca. In Advances in Nitrogen Fixation Research. Eds. C Veeger and W E Newton. pp 311–319. Nijhoff/Junk, The Hague.Google Scholar
  2. Al-Mallah M K, Davey M R, Cocking E C 1989 Formation of nodular structures on rice seedlings by rhizobia. J. Exp. Bot. 40, 473–478.Google Scholar
  3. Bennett J and Ladha J K 1992 Introduction: feasibility of nodulation and nitrogen fixation in rice–potential and prospects. In Nodulation and Nitrogen Fixation in Rice. Eds. G S Khush and J Bennett. pp 1–11. International Rice Research Institute, Manila, Philippines.Google Scholar
  4. Benson D R and Silvester W B 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57, 293–319.Google Scholar
  5. Benson D R, Stephens D W, Clawson M L and Silvester W B 1996 Amplification of 16S rRNA genes from Frankia strains in root nodules of Ceanothus griseus, Coriaria arborea, Coriaria plumosa, Discaria toumatou, and Purshia tridentata. Appl. Environ. Micro. 62, 2904–2909.Google Scholar
  6. Calvert H E, Chaudhary A H, and Lalonde M 1979 Structure of an unusual nodule root symbiosis in a non-leguminous herbaceous dicotyledon. In Symbiotic Nitrogen Fixation in the Management of Temperate Forests. Eds. J C Gorden, C T Wheeler and D A Perry. p 474 Forest Research Laboratory, Oregon State University, Corvallis, OR.Google Scholar
  7. Chase M, Soltis D E, Olmstead R G, Morgan D, Les D H, Mishler B D, Duvall M R, Price R, Hills H G, Qiu Y, Kron K A, Rettig J H, Conti E, Palmer J D, Manhart J R, Sytsma K J, Michaels H J, Kress W J, Donoghue J D, Clark W D, Hedr´en M, Gaut B S, Jansen R K, Kim K-J, Wimpee C F, Smith J F, Furnier G R, Straus S H, Xiang Q, Plunkett G M, Soltis P S, Swensen S M, Eguiarte L E, Learn G H Jr, Barrett S C, Graham S and Albert V A 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80, 528–580.Google Scholar
  8. Cournoyer B, Gouy M and Normand P 1993 Molecular phylogeny of the symbiotic actinomycetes of the genus Frankia matches host-plant infection processes. Mol. Biol. Evol. 10, 1303–1316.Google Scholar
  9. Cronquist A 1981 An integrated system of classification of flowering plants. Columbia University Press, New York, NY.Google Scholar
  10. Cronquist A 1988 The evolution and classification of flowering plants. New York Botanical Garden, Bronx, NY.Google Scholar
  11. Dahlgren R M T 1980 A revised system of classification of the angiosperms. Botanical Journal of the Linnean Society 80, 91– 124.Google Scholar
  12. Darwin C 1859 On the origin of species by natural selection.Google Scholar
  13. Doyle J J 1994 Phylogeny of the legume family: An approach to understanding the origins of nodulation. Ann. Rev. Ecol. Syst. 25, 325–349.Google Scholar
  14. Linneaus C 1753 Species Plantarum. Lumini E and Bosco M 1996 PCR-restriction fragment length polymorphismidentification and host range of single-spore isolates of the flexible Frankia sp. Strain UFI 132715. Appl. Environ. Micro. 62, 3026–3029.Google Scholar
  15. Miller I M and Baker D D 1986 Nodulation of actinorhizal plants by Frankia strains capable of both root hair infection and intercellular penetration. Protoplasma 131, 82–91.Google Scholar
  16. Mirza M S, Hahn D, Dobritsa S V, Akkermans A D L 1994a Phylogenetic studies on uncultured Frankia populations in nodules of Datisca cannabina. Can. J. Microbiol. 40, 313–318.Google Scholar
  17. Mirza M S, Hameed S and Akkermans A D L 1994b Genetic diversity of Datisca cannabina-compatible Frankia strains as determined by sequence analysis of the PCR-amplified 16S RNA gene. Appl. Environ. Microbiol. 60, 2371–2376.Google Scholar
  18. Mirza M S, Akkermans W M and Akkermans A D L 1994c PCR-amplified 16S rRNA sequence analysis to confirm nodulation of Datisca cannabina L. by the endophyte of Coriaria nepalensis Wall. Plant and Soil 160, 147–152.Google Scholar
  19. Müller J 1981 Fossil pollen records of extant angiosperms. The Botanical Review 47, 1 1–142.Google Scholar
  20. Newcomb W and Pankhurst C E 1982 Fine structure of actinorhizal nodules of Coriaria arborea (Coriariaceae). New Zealand Journal of Botany 20, 93–103.Google Scholar
  21. Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L and Misra A K 1996 Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. International Journal of Systematic Bacteriology 46, 1–9.Google Scholar
  22. Silvester W B and Harris S L 1989 Nodule structure and nitrogenase activity of Coriaria arborea in response to varying pO2. Plant and Soil 78, 245–258.Google Scholar
  23. Silvester W B, Harris S L and Tjepkema J D 1990 Oxygen regulation and hemoglobin. In The Biology of Frankia and actinorhizal plants. Eds. C R Schwintzer and J D Tjepkema. pp 157–176. Academic Press, Inc., New York, NY.Google Scholar
  24. Soltis D E, Soltis P S, Morgan D R, Swensen S M, Mullin B C, Dowd J M and Martin P G 1995 Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl. Acad. Sci. 92, 2646–2651.Google Scholar
  25. Sprent J I 1994 Evolution and diversity in the legume-rhizobium symbiosis: Chaos theory? Plant and Soil 161, 1–10.Google Scholar
  26. Swensen S M, Mullin B C, and Chase M W 1994 Phylogenetic affinities of the Datiscaceae based on an analysis of nucleotide sequences from the plastid rbcL gene. Systematic Botany 19(1), 157–168.Google Scholar
  27. Swensen S M 1996 The evolution of actinorhizal symbioses: Evidence for multiple origins of the symbiotic association. Am. J. Bot. 83(11), 1503–1512.Google Scholar
  28. Swensen S M and Mullin B C In Press Phylogenetic relationships among actinorhizal plants: The impact of molecular systematics and implications for the evolution of actinorhizal symbioses. Physiologia Plantarum.Google Scholar
  29. Takhtajan A 1980 Outline of the classification of flowering plants (Magnoliophyta). The Botanical Review (Lancaster) 46, 225– 359.Google Scholar
  30. Thorne R T 1992 Classification and geography of the flowering plants. The Botanical Review (Lancaster) 58, 225–348.Google Scholar
  31. Tjepkema J D, Schwintzer C R and Monz C A 1988 Time course of acetylene reduction in nodules of five actinorhizal genera. Plant Physiology 86, 581–583.Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Susan M. Swensen
    • 1
  • Beth C. Mullin
    • 2
  1. 1.Department of BiologyIthaca CollegeIthacaUSA
  2. 2.The Department of Botany and the Center for Legume ResearchThe University of TennesseeKnoxvilleUSA

Personalised recommendations