Plant and Soil

, Volume 254, Issue 1, pp 207–217

Molecular phylogeny of Alnus (Betulaceae), inferred from nuclear ribosomal DNA ITS sequences

  • Elisabeth Navarro
  • Jean Bousquet
  • André Moiroud
  • Antonio Munive
  • Dominique Piou
  • Philippe Normand


The nuclear ITS region of 19 species of Alnus was amplified and sequenced. The inferred molecular phylogeny shows that all species of the genus Alnus form a monophyletic group close to Betula and that the fundamental dichotomy within the genus lies between the subgenera Alnaster and Gymnothyrsus, sensu Murai (1964). The subgenus Alnaster appears to be basal in the genus, based on archaism of morphological features, and branching close to the root of the trees due to low ITS divergence from genus Betula. The monophyly of the section Clethropsis is not supported by the present data: Alnus nepalensis is positioned in the subgenus Gymnothyrsus, away from A. nitida and A. maritima. Surprisingly, A. formosana sect. Japonicae is closely tied to A. maritima sect. Clethropsis, with which it shares few morphological traits, and is separate from A. japonica sect. Japonicae with which it shares many traits. An increase in substitution rate is noted in the group comprising A. formosana, A. maritima and A. nitida relative to the rest of the genus, which appears to have had, on the average, a very slow mutation rate. Alnusglutinosa, the designated type for the genus, appears to be representative of the genus both for morphological characters and evolutionary rate. North-East Asia is comforted in its position of origin of the genus since not only does it have the highest number of species and representatives in all deep branching lineages, there are also fewer transcontinental migrations when a North-East Asian ancestor is postulated than when a North American ancestor is postulated.

Alnus Betula ITS sequences phylogeny rRNA 


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  1. Baldwin B G 1992 Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Mol. Phylogenet. Evol. 1, 3–16.PubMedGoogle Scholar
  2. Benson D R and Silvester W B 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57, 293–319.PubMedGoogle Scholar
  3. Bousquet J, Strauss S H and Li P 1992a Complete congruence between morphological and rbcL-based molecular phylogenies in birches and related species (family Betulaceae). Mol. Biol. Evol. 9, 1076–1088.PubMedGoogle Scholar
  4. Bousquet J, Strauss S H, Doerksen A H and Price R A 1992b Extensive variation in evolutionary rate of rbcL gene sequences among seed plants. Proc. Nat. Acad. Sci. USA 89, 7844–7848.PubMedGoogle Scholar
  5. Bremer K 1994 Branch support and tree stability. Cladistics 10, 295–304.Google Scholar
  6. Burkill J H 1899 Cupuliferae: Betuleae. J. Linn. Soc. Bot. 26, 496–500.Google Scholar
  7. Cerbah M, Souza-Chies T, Jubier M F, Lejeune B and Siljak-Yakovlev S 1998 Molecular phylogeny of the genus Hypochaeris using internal transcribed spacers of nuclear rDNA: inference for chromosomal evolution. Mol. Biol. Evol. 15, 345–354.PubMedGoogle Scholar
  8. Chen Z D, Manchester S R and Sun H Y. 1999 Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology, and paleobotany. Am. J. Bot. 86, 1168–1181.PubMedGoogle Scholar
  9. Crane P R 1981 Betulaceous leaves and fruits from the British Upper Paleocene. Bot. J. Linn. Soc. 83, 103–136.Google Scholar
  10. Crane P R 1989 Early fossil history and evolution of the Betulaceae. In Evolution, Systematics, and Fossil History of the Hamamelidae. Vol. 2: 'Higher' Hamamelidae. Eds. P R Crane and S Blackmore. pp. 87–116. Clarendon, Oxford, United Kingdom.Google Scholar
  11. Cronquist A 1988. The evolution and classification of flowering plants. 2nd edn Allen, Lawrence, Kansas.Google Scholar
  12. Francisco-Ortega J, Fuertes-Aguilar J, Gomez-Campo C, Santos-Guerra A and Jansen R K 1999 Internal transcribed spacer sequence phylogeny of Crambe L. (Brassicaceae): molecular data reveal two Old World disjunctions. Mol. Phylogenet. Evol. 11, 361–380.PubMedGoogle Scholar
  13. Felsenstein J 1981 Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17, 368–376.PubMedGoogle Scholar
  14. Felsenstein J 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.Google Scholar
  15. Furlow J J 1979 The systematics of the American species of Alnus (Betulaceae). Rhodora 81, 151–248.Google Scholar
  16. Furlow J J 1990 The genera of Betulaceae in the Southeastern United States. J. Arnold Arboreum 7l, 1–67.Google Scholar
  17. Hsiao C, Chatterton N J, Asay K H and Jensen K B 1995 Phylogenetic relationships of the monogenomic species of the wheat tribe, Triticeae (Poaceae), inferred from nuclear rDNA (internal transcribed spacer) sequences. Genome 38, 211–223.PubMedGoogle Scholar
  18. Jeandroz S, Roy A and Bousquet J 1997 Molecular phylogeny and phylogeography of the circumpolar genus Fraxinus. Mol. Phylogenet. Evol. 7, 241–251.PubMedGoogle Scholar
  19. Kimura M 1980 A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120.PubMedGoogle Scholar
  20. Kluge A G and Fans J 5 1969 Quantitative phyletics and the evolution of anurans. Syst. Zool. 18, 1–32.Google Scholar
  21. Kollipara K P, Singh R J and Hymowitz T 1997 Phylogenetic and genomic relationships in the genus Glycine Willd. based on sequences from the ITS region of nuclear rDNA. Genome 40, 57–68.PubMedGoogle Scholar
  22. Kuhner M K and Felsenstein J 1994 A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Mol. Biol. Evol. 11, 459–68.PubMedGoogle Scholar
  23. Kumar S, Tamura K and Nei M 1993 MEGA - Molecular Evolutionary Genetics Analysis, Version 1.0. Institute of Molecular Evolutionary Genetics, Pennsylvania State University.Google Scholar
  24. Li P and Bousquet J 1992 Relative rate test for nucleotide substitutions between two lineages. Mol. Biol. Evol. 9, 1185–1189.Google Scholar
  25. Linnaeus C 1753 Species Plantarum, tome II Holmia, Laurentii Salvii (Facsimile ed.), W. Junk, 1908.Google Scholar
  26. Muller J 1984 Significance of fossil pollen for angiosperm history. Annals of the Missouri Botanic Gardens 71, 419–443.Google Scholar
  27. Mullin B C, Swensen S M and Goetting-Minesky P 1990 Hypotheses for the evolution of actinorhizal symbioses. In Nitrogen Fixation: Achievements and Objectives. Eds P M Gresshoff, L E Roth, G Stacey and W E Newton. pp. 781–787. Chapman and Hall, New York.Google Scholar
  28. Murai S 1963 Phytotaxonornical and geobotanical studies on socalled genus Alnus in Japan (II). Comparative studies on all species, including shrubby species. Bull. Gov. For. Exp. Sta. (Tokyo, Japan) 154, 20–72.Google Scholar
  29. Murai S 1964 Phytotaxonomical and geobotanical studies on genus Alnus in Japan (III). Taxonomy of whole world species and distribution of each section. Bull. Gov. For. Exp. Sta. (Tokyo, Japan) 171, 1–107.Google Scholar
  30. Otto S P and Whitlock M C 1997 The probability of fixation in populations of changing size. Genetics 146, 723–33.PubMedGoogle Scholar
  31. Perrière G and Gouy M 1996 WWW-Query: An on-line retrieval system for biological sequence banks. Biochimie 78, 364–369.PubMedGoogle Scholar
  32. Relethford J H 1991 Effect of changes in population size on genetic microdifferentiation. Hum. Biol. 63, 629–641.PubMedGoogle Scholar
  33. Saitou N and Nei M 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.PubMedGoogle Scholar
  34. Savard L, Michaud M and Bousquet J 1993 Genetic diversity and phylogenetic relationships between birches and alders using ITS, 18S rRNA and rbcL gene sequences. Mol. Phylogenet. Evol. 2, 112–118.PubMedGoogle Scholar
  35. Shen Y, Ford-Lloyd B V and Newbury H J 1998 Genetic relationships within the genus Beta determined using both PCR-based marker and DNA sequencing techniques. Heredity 80, 624–632.PubMedGoogle Scholar
  36. Smolander A, Ronkko R, Nurmiaho-Lassil E-L and Haahtela K 1990 Growth of Frankia in the rhizosphere of Betula pendula, a nonhost tree species. Can. J. Microbiol. 36, 649–656.Google Scholar
  37. 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. Nat. Acad. Sci. USA 92, 2647–2651.PubMedGoogle Scholar
  38. Sorensen M D 1999 TreeRot, version 2. Boston University, Boston, Massachussetts.Google Scholar
  39. Spach E 1841 Revisio Betulacearum. Annales de Sciences Naturelles 1115, 182–212.Google Scholar
  40. Swofford D L 1999 PAUP. Phylogenetic Analysis Using Parsimony (and OtherMethods). Version 4. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  41. Takhtajan A 1996 Diversity and Classification of the Flowering plants. New York: Columbia University Press.Google Scholar
  42. Thompson J D, Gibson T J, Plewniak F, Jeanmougin F and Higgins D G. 1997 The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882.PubMedGoogle Scholar
  43. Wen J and Zimmer E A 1996 Phylogeny and biogeography of Panax L. (the ginseng genus, araliaceae): inferences from ITS sequences of nuclear ribosomal DNA. Mol. Phylogenet. Evol. 6, 167–177.PubMedGoogle Scholar
  44. White T J, Bruns T, Lee S and Taylor J 1990 Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications. Eds. M A Innis, D H Gelfand, J J Sninsky and T J White. pp. 315–322. Academic Press, San Diego, California.Google Scholar
  45. Wolfe J 1969 Neogene floristic and vegetational history of the Pacific Northwest. Madrono 20, 83–110.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Elisabeth Navarro
    • 1
    • 2
  • Jean Bousquet
    • 3
  • André Moiroud
    • 1
  • Antonio Munive
    • 1
  • Dominique Piou
    • 4
  • Philippe Normand
    • 1
  1. 1.Ecologie Microbienne, UMR CNRS 5557Université Lyon IVilleurbanneFrance
  2. 2.IBIS, UR IRD 83Université Lyon IVilleurbanneFrance
  3. 3.Centre de Recherche en Biologie ForrestièreUniversité LavalQuébecCanada
  4. 4.Arboretum National des Barres, Nogent-sur-VernissonFrance

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