Journal of Plant Biology

, Volume 56, Issue 5, pp 290–305 | Cite as

Phylogeny of Magnoliaceae based on ten chloroplast DNA regions

  • Sangtae Kim
  • Youngbae SuhEmail author
Original Article


Phylogenetic analyses of ten chloroplast DNA regions, ndhF, rbcL, matK, ORF350, trnL intron, trnL-trnF, trnH-psbA, rbcL-atpB, trnK 5′ intron, and trnK 3′ intron (8,719 bp in aligned sequences) from 48 selected taxa were carried out to address phylogenetic questions in the family Magnoliaceae. The major clades in the molecular tree are considerably different from the currently suggested classification system and from the traditionally recognized subgroups in the family. Eleven major clades were recognized with strong support in the subfamily Magnolioideae: (1) MICHELIA clade: Michelia, Elmerrillia, sect. Maingola, sect. Alcimandra, and sect. Aromadendron, (2) YULANIA clade: subgen. Yulania, (3) GYNOPODIUM clade: Pachylarnax, sect. Manglietiastrum, and sect. Gynopodium, (4) KMERIA clade: Kmeria, (5) THEORHODON clade: sect. Theorhodon sensu stricto (excluding sect. Splendentes, which was recently separated from sect. Theorhodon) and sect. Magnolia, (6) GWILLIMIA clade: sect. Gwillimia, sect. Lirianthe, and sect. Blumiana, (7) TALAUMA clade: sect. Talauma and sect. Splendentes, (8) MANGLIETIA clade: Manglietia, (9) RYTIDOSPERMUM clade: sect. Rytidospermum sensu stricto (excluding Magnolia fraseri, M. macrophylla, and M. dealbata) and sect. Oyama, (10) FRASERI clade: M. fraseri, and (11) MACROPHYLLA clade: M. macrophylla and M. dealbata. The recognition of eleven major clades in the subfamily Magnolioideae in this study is in good agreement with previous molecular studies based on less sampling or fewer DNA regions. All of these eleven clades were highly supported with bootstrap values exceeding 80% in both maximum parsimony and maximum likelihood analyses and with posterior probabilities exceeding 0.98 in a Bayesian analysis. However, detailed relationships among the major clades were weakly supported. The molecular data suggest that the taxonomic circumscription of infrafamilial delimitations and compositions should be reconsidered.


Chloroplast genes Classification system Magnolia Magnoliaceae Molecular phylogeny 


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  1. Azuma HL, Thien B, Kawano S (1999) Molecular phylogeny of Magnolia (Magnoliaceae) inferred from cpDNA sequences and evolutionary divergence of floral scents. J Plant Res 112:291–306CrossRefGoogle Scholar
  2. Azuma H, Garcia-Franco JG, Rico-Gray V, Thien LB (2001) Molecular phylogeny of Magnoliaceae, the biogeography of tropical and temperate disjunctions. Amer J Bot 88:2275–2285CrossRefGoogle Scholar
  3. Barkman TJ, Chenery JG, McNeal JR, Lyons-Weile J, Ellisens WJ, Moore G, Wolfe AD, dePamphilis CW (2000) Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. Proc Natl Acad Sci USA 97:13166–13171PubMedCrossRefGoogle Scholar
  4. Bohs L, Olmstead RG (1997) Phylogenetic relationships in Solanum (Solanaceae) based on ndhF sequences. Syst Bot 22:5–17CrossRefGoogle Scholar
  5. Borsch T, Hilu KW, Quandt D, Wilde V, Neinhuis C, Barthlott W (2003) Non-coding plastid trnT-trnF sequences reveal a highly supported phylogeny of basal angiosperms. J Evol Biol 15:558–567CrossRefGoogle Scholar
  6. Cai Z, Penaflor C, Kuehl JV, Leebens-Mack J, Carlson J, dePamphilis CW, Boore JL, Jansen RK (2006) Complete chloroplast genome sequences of Drimys, Liriodendron, and Piper: Implications for the phylogeny of magnoliids and the evolution of GC content. BMC Evol Biol 6:77PubMedCrossRefGoogle Scholar
  7. de Candolle AP (1813) Théorie élémentaire de la botanique, Chez Déterville, Paris Chase MW and 31 authors (1993) Phylogenetics of seed plants: An analysis of nucleotide sequences from the plastid gene rbcL. Ann Missouri Bot Gard 80:528–580Google Scholar
  8. Chen BL, Nooteboom HP (1993) Notes on Magnoliaceae III: The Magnoliaceae of China. Ann Missouri Bot Gard 80:999–1104CrossRefGoogle Scholar
  9. Clark LG, Zhang W, Wendel JF (1995) A phylogeny of the grass family (Poaceae) based on ndhF sequence data. Syst Bot 20:436–460CrossRefGoogle Scholar
  10. Clegg MT (1993) Chloroplast gene sequences and the study of plant evolution. Proc Natl Acad Sci USA 90:363–367PubMedCrossRefGoogle Scholar
  11. Dandy JE (1927) The genera of Magnoliaceae. Kew Bulletin 1927:275–264Google Scholar
  12. Dandy JE (1971) The classification of the Magnoliaceae. Newsletter of the American Magnolia Society 8:3–6Google Scholar
  13. Dandy JE (1978) Revised survey of the genus Magnolia together with Manglietia and Michelia, In NG Treseder, Magnolias. Faber and Faber, London, pp 29–37Google Scholar
  14. Dilcher DL, Crane PR (1984) Archaeanthus: An early angiosperm from the Cenomanian of the western interior of North America. Ann Missouri Bot Gard 71:351–383CrossRefGoogle Scholar
  15. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15Google Scholar
  16. Felsenstein J (1978) Case in which parsimony and compatibility methods will be positively misleading. Syst Zool 27:401–410CrossRefGoogle Scholar
  17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  18. Figlar RB (2000) Proleptic branch initiation in Michelia and Magnolia subgenus-Yulania provides basis for combinations in subfamily Magnoliaceae, In Y Liu, H Fan, Z Chen, Q Wu, Q. Zeng, eds, Proceedings of the International Symposium on the Family Magnoliaceae, Science Press, Beijing, pp 14–26Google Scholar
  19. Figlar RB, Nooteboom HP (2004) Notes on Magnoliaceae IV. Blumea 49:87–100CrossRefGoogle Scholar
  20. Flook PK, Klee S Rowell HF (1999) Combined molecular phylogenetic analysis of the Orthoptera (Arthropoda, Insecta) and implications for their higher systematics. Syst Biol 48:233–253PubMedCrossRefGoogle Scholar
  21. Fragan BM, Stedje B, Stabbetorp OE, Jensen ES, Jakobsen KS (1994) A general approach for PCR-amplification and sequencing of chloroplast DNA from crude vascular plant and algal tissue. BioTechniques 16:484–494Google Scholar
  22. Frodin DG, Govaerts R (1996) World checklist and bibliography of Magnoliaceae, Kew Publishing, RichmondGoogle Scholar
  23. Graham SW, Olmstead RG (2000) Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. Amer J Bot 87:1712–1730CrossRefGoogle Scholar
  24. Hilu KW, Borsch T, Muller K, Soltis DE, Soltis PE, Savolainen V, Chase M, Powell M. Alice L, Evans R, Sauquet H, Neinhuis C, Slotta T, Rohwer J, Chatrou L (2003) Inference of angiosperm phylogeny based on matK sequence information. Amer J Bot 90:758–1776CrossRefGoogle Scholar
  25. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  26. Jansen RK, Cai Z, Raubeson LA, Daniell H, dePamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee S-B, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 49:19369–19374CrossRefGoogle Scholar
  27. Johnson LA, Soltis DE (1994) matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19:143–156CrossRefGoogle Scholar
  28. Johnson LA, Soltis DE (1995) Phylogenetic inference in Saxifragaceae sensu stricto and Gilia (Polemoniaceae) using matK sequences. Ann Missouri Bot Gard 82:149–175CrossRefGoogle Scholar
  29. Johnson LA, Schultz JL, Soltis DE, Soltis PS (1996) Monophyly and generic relationships of Polemoniaceae based on matK sequences. Amer J Bot 83:1207–1224CrossRefGoogle Scholar
  30. Judd WD, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2008) Plant systematics: a phylogenetic approach. Sinauer, SunderlandGoogle Scholar
  31. Kim JH, Hart HT, Mes HM (1996) The phylogenetic position of East Asian Sedum species (Crassulaceae) based on chloroplast DNA trnL (UAA)-trnF (GAA) intergenic spacer sequence variation. Acta Botanica Neerlandica 45:309–321Google Scholar
  32. Kim K-J, Jansen RK (1995) ndhF sequence evolution and the major clades in the sunflower family. Proc Natl Acad Sci USA 92:10379–10383PubMedCrossRefGoogle Scholar
  33. Kim S, Park J-W, Kim Y-D, Suh Y (2001) Phylogenetic relationships in family Magnoliaceae inferred from ndhF sequences. Amer J Bot 91:2101–2004Google Scholar
  34. Kim S, Yoo M-J, Albert VA, Farris JS, Soltis PS, Soltis DE (2004) Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolution and functional implications of a 260-million-year-old duplication. Amer J Bot 91:2102–2118CrossRefGoogle Scholar
  35. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparable studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  36. Law YW (1984) A preliminary study on the taxonomy of the family Magnoliaceae. Acta Phytotax Sinica 22:80–109Google Scholar
  37. Law YW (1996) Magnoliaceae, In Flora Reipublicae Popularis Sinicae. 30(1). Science Press, Beijing, ChinaGoogle Scholar
  38. Li HL (1952) Floristic relationships between eastern Asia and eastern North America. Transactions of the American Philosophical Society 42:371–429CrossRefGoogle Scholar
  39. Li HL (1972) Eastern Asia-eastern North America species-pairs in wide ranging genera, In A Graham ed, Floristics and paleofloristics of Asia and eastern North America, Elsevier, Amsterdam, pp 65–78Google Scholar
  40. Maddison DR (1991) The discovery and importance of multiple islands of most-parsimonious trees. Syst Zoo 40:315–328CrossRefGoogle Scholar
  41. Magallón S, Sanderson MJ (2001) Absolute diversification rates in angiosperm clades. Evolution 55:1762–1780PubMedGoogle Scholar
  42. Mathews S, Donoghue MJ (1999) The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 268:947–950CrossRefGoogle Scholar
  43. Mishler BD (1994) Cladistic analysis of molecular and morphological data. American Journal of Physical Anthropology 94:143–156PubMedCrossRefGoogle Scholar
  44. Mishler BD, Soltis PS, Soltis DE (1998) Compartmentalization in phylogeny reconstruction: philosophy and practice, DIMACS Report, PrincetonGoogle Scholar
  45. Moore MJ, Bell CD, Soltis PS, Soltis DE (2007) Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci USA 104:19363–19368PubMedCrossRefGoogle Scholar
  46. Morgan D, Soltis DE (1993) Phylogenetic relationships among members of Saxifragaceae sensu lato based on rbcL sequence data. Ann Missouri Bot Gard 80:631–660CrossRefGoogle Scholar
  47. Nickerson J, Drouin G (2004) The sequence of the largest subunit of RNA polymerase II is a useful marker for inferring seed plant phylogeny. Mol Phylogenet Evol 31:403–415PubMedCrossRefGoogle Scholar
  48. Nie Z-L, Wen J, Zauma H, Qiu Y-L, Sun H, Meng, Y, Sun W-B, Zimmer EA (2008) Phylogenetic and biogeographic complexity of Magnoliaceae in the Northern Hemisphere inferred from three nuclear data sets. Mol Phylogenet Evol 48:1027–1040PubMedCrossRefGoogle Scholar
  49. Nooteboom HP (1985) Notes on Magnoliaceae, with a revision of Pachylarnax and Elmerrillia and the Malesian species of Manglietia and Michelia. Blumea 31:65–12Google Scholar
  50. Nooteboom HP (1993) Magnoliaceae, In K Kubitzki, JG Rohwer, V Bittrich, eds, The families and genera of vascular plants, vol. II, Springer-Verlag, New York, pp 391–401Google Scholar
  51. Nooteboom HP (2000) Different looks at the classification of the Magnoliaceae. In Y Liu, H Fan, Z Chen, Q Wu, Q Zeng eds, Proceedings of the International Symposium on the Family Magnoliaceae. Science Press, Beijing, pp 26–38Google Scholar
  52. Olmstead RG, Sweere JA (1994) Combining data in phylogenetic systematics: An empirical approach using three molecular data sets in the Solanaceae. Syst Biol 43:467–481CrossRefGoogle Scholar
  53. Olmstead RG, Palmer JD (1994) Chloroplast DNA systematics: A review of method and data analysis. Amer J Bot 81:1205–1224CrossRefGoogle Scholar
  54. Olmstead RG, Reeves PA (1995) Evidence for the polyphyly of the Scrophulariaceae based in chloroplast rbcL and ndhF sequences. Annals of the Missouri Botanical Garden 82:176–193CrossRefGoogle Scholar
  55. Osako T, Ohnishi O (2000) Intra- and interspecific phylogeny of wild Fagopyrum (Polygonaceae) species based on nucleotide sequences of noncoding regions in chloroplast DNA. Amer J Bot 87:573–582CrossRefGoogle Scholar
  56. Oxelman B, Backlund BM, Bremer B (1999) Relationships of Buddlejaceae s. l. Investigated using parsimony jackknife and branch support analysis of chloroplast ndhF and rbcL sequence data. Syst Bot 24:164–182CrossRefGoogle Scholar
  57. Palmer JD, Jansen RK, Michaels HJ, Chase MW, Manhart JR (1988) Chloroplast DNA variation and plant phylogeny. Ann Missouri Bot Gard 75:1180–1206CrossRefGoogle Scholar
  58. Parkinson CL, Adams KL, Palmer JD (1999) Multigene analyses identify the three earliest lineages of extant flowering plants. Curr Biol 9:1485–1488PubMedCrossRefGoogle Scholar
  59. Plunkett GM, Soltis DE, Soltis PS (1996) Evolutionary pattern in Apiaceae: inferences based on matK sequence data. Syst Bot 21:477–495CrossRefGoogle Scholar
  60. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  61. Qiu YL, Parks CR, Chase MW (1995a) Molecular divergence in the eastern Asian-eastern North America disjunct section Rytidospermum of Magnolia (Magnoliaceae). Amer J Bot 82:1589–1598CrossRefGoogle Scholar
  62. Qiu YL, Chase MW, Parks CR (1995b) A chloroplast DNA phylogenetic study of the eastern Asia-eastern North America disjunct section Rytidospermum of Magnolia (Magnoliaceae). Amer J Bot 82:1582–1588CrossRefGoogle Scholar
  63. Qiu YL, Lee J, Lu Y-L, Bernasconi-q F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW (1999) The earliest angiosperms: Evidence from mitochondrial, plastid and nuclear genomes. Nature 402:404–407PubMedCrossRefGoogle Scholar
  64. Qiu YL, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW (2000) Phylogeny of basal angiosperms: analyses of five genes from three genomes. Int J Plant Sci 161:S3–S27CrossRefGoogle Scholar
  65. Richardson JE, Fay MF, Cronk QCB, Bowman D, Chase MW (2000) A phylogenetic analysis of Rhamnaceae using rbcL and trnL-F plastid DNA sequences. Amer J Bot 87:1309–1324CrossRefGoogle Scholar
  66. Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Amer J Bot 84:1120–1136CrossRefGoogle Scholar
  67. Scotland RW, Sweere JA, Reeves PA, Olmstead RG (1995) Higherlevel systematics of Acanthaceae determined by chloroplast DNA sequences. Amer J Bot 82:266–275CrossRefGoogle Scholar
  68. Soltis DE, Soltis PS (1997) Phylogenetic relationships in Saxifragaceae sensu lato: a comparison of topologies based on 18S rDNA and rbcL sequences. Amer J Bot 84:504–522CrossRefGoogle Scholar
  69. Soltis DE, Kuzoff RK, Conti E, Gornall R, Ferguson K (1996) matK and rbcL gene sequence data indicate that Saxifraga (Saxifragaceae) is polyphyletic. Amer J Bot 83:371–382CrossRefGoogle Scholar
  70. Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Brockington SF, Refulio-Rodriguez NF, Walker JB, Moore MJ, Carlsward BS, Bell CD, Latvis M, Crawley S, Black C, Diouf D, Zi Z, Rushworth CA, Gitzendanner MA, Sytsma, KJ, Qiu Y-L, Hilu KW, Davis CC, Sanderson MJ, Beaman, RS, Olmstead RG, Judd WS, Donoghue MJ, Soltis PS (2011) Angiosperm phylogeny: 17 genes, 640 taxa. Amer J Bot 98:704–730.CrossRefGoogle Scholar
  71. Soltis PS, Soltis DE, Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402–404PubMedCrossRefGoogle Scholar
  72. Soltis PS, Soltis DE, Zanis M, Kim S (2000) Basal lineages of angiosperms: relationships and implications for floral evolution. Int J Plant Sci 161:97–107CrossRefGoogle Scholar
  73. Spongberg SA (1998) Magnoliaceae hardy in cooler temperate regions, In D Hunt ed, Magnolias and their allies, David Hunt, Milborne Port, pp 81–144Google Scholar
  74. Spjut RW (1994) A systematic treatment of fruit types, Memoirs of the New York botanical garden vol. 70, The New York botanical garden, New YorkGoogle Scholar
  75. Steel KP, Vilgalys R (1994) Phylogenetic analyses of Polemoniaceae using nucleotide sequences of the plastid gene matK. Syst Bot 19:126–142CrossRefGoogle Scholar
  76. Swofford DL (2001) PAUP* 4.0b10: Phylogenetic analysis using parsimony (*and other methods), version 4, Sinauer, SunderlandGoogle Scholar
  77. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109PubMedCrossRefGoogle Scholar
  78. Takhtajan A (1969) Diversity and classification of flowering plants, Columbia University Press, New YorkGoogle Scholar
  79. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  80. Thorne RF (1993) Magnoliaceae, In VH Heywood, ed, Flowering plants of the world, Oxford University Press, New York, pp 27–28Google Scholar
  81. Vázquez-Garcia JA (1994) Magnolia (Magnoliaceae) in Mexico and Central America: a synopsis. Brittonia 46:1–23CrossRefGoogle Scholar
  82. Xia N-H, Liu Y-H, Nooteboom HP (2008) Magnoliaceae, In Flora of China, Vol 7, Science Press & Missouri Botanical Garden Press, Beijing and St. LouisGoogle Scholar
  83. Zanis MJ, Soltis DE, Soltis PE, Mathews S, and Donoghue MJ (2002) The root of the angiosperms revisited. Proc Natl Acad Sci USA 99:6848–6853PubMedCrossRefGoogle Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.School of Biological Sciences and ChemistrySungshin UniversitySeoulKorea
  2. 2.Natural Products Research Institute, College of PharmacySeoul National UniversitySeoulKorea

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