Journal of Plant Research

, Volume 119, Issue 6, pp 599–616 | Cite as

Phylogenetic analyses of Malpighiales using plastid and nuclear DNA sequences, with particular reference to the embryology of Euphorbiaceae sens. str.

  • Toru TokuokaEmail author
  • Hiroshi Tobe
Regular Paper


We present phylogenetic analyses of Malpighiales, which are poorly understood with respect to relationships within the order, using sequences from rbcL, atpB, matK and 18SrDNA from 103 genera in 23 families. From several independent and variously combined analyses, a four-gene analysis using all sequence data provided the best resolution, resulting in the single most parsimonious tree. In the Malpighiales [bootstrap support (BS) 100%], more than eight major clades comprising a family or group of families successively diverged, but no clade containing more than six families received over 50% BS. Instead, ten terminal clades that supported close relationships between and among families (>50% BS) were obtained, between, for example, Balanopaceae and Chrysobalanaceae; Lacistemataceae and Salicaceae; and Phyllanthaceae and Picrodendraceae. The monophyly of Euphorbiaceae sens. str. were strongly supported (BS 100%), but its sister group was unclear. Euphorbiaceae sens. str. comprised two basally diverging clades (BS 100%): one leading to the Clutia group (Chaetocarpus, Clutia, Pera and Trigonopleura), and the other leading to the rest of the family. The latter shared a palisadal, instead of a tracheoidal exotegmen as a morphological synapomorphy. While both Acalyphoideae (excluding Dicoelia and the Clutia group) and Euphorbioideae are monophyletic, Crotonoideae were paraphyletic, requiring more comprehensive analyses.


atpB Euphorbiaceae Malpighiales matK rbcL 18S rDNA 



We are grateful to Hiroaki Setoguchi, Yukitoshi Kimoto, Kipiro Damas, Jun-ichi Nagasawa and Shigeru Matsutani, as well as to the curators of MO, L and E, for their assistance in obtaining materials used in the study. The study was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (17770069) and a grant for Biodiversity Research of the 21st Century COE (A14).


  1. APG II (2003) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants. APG II. Bot J Linn Soc 141:399–436Google Scholar
  2. Boesewinkel FD (1980) Development of ovule and testa of Linum usitatissimum L. Acta Bot Neerl 29:17–32Google Scholar
  3. Boesewinkel FD (1985) The ovule and seed of Humiria balsamifera (Aubl.) St.Hil. Acta Bot Neerl 34:183–191Google Scholar
  4. Boesewinkel FD, Bouman F (1980) Development of ovule and seed-coat of Dichapetalum mombuttense Engl. with notes on other species. Acta Bot Neerl 29:103–115Google Scholar
  5. Boesewinkel FD, Geenen J (1980) Development of ovule and seed-coat of Erythroxylum coca Lamk. Acta Bot Neerl 29:231–241Google Scholar
  6. Chase MW, Zmarzty S, Lledó MD, Wurdack KJ, Swensen SM, Fay MF (2002) When in doubt, put it in Flacourtiaceae: a molecular phylogenetic analysis based on plastid rbcL DNA sequences. Kew Bull 57:141–181Google Scholar
  7. Corner EJH (1976) The seeds of dicotyledons. Cambridge University Press, CambridgeGoogle Scholar
  8. Dathan ASR, Singh D (1971) Embrylogy and seed-development in Bergia L. J Indian Bot Soc 50:362–370Google Scholar
  9. Dathan ASR, Singh D (1973a) Structure and development of ovule and seed in Flacourtia indica (Burn.F) Merrill. Proc Indian Natl Sci Acad Part B Biol Sci 39:172–179Google Scholar
  10. Dathan ASR, Singh D (1973b) Structure and development of seed coat in Viola spp. J Indian Bot Soc 52:119–126Google Scholar
  11. Dathan ASR, Singh D (1973c) Development and structure of seed in Tacsonia Juss. and Passiflora L. Proc Indian Acad Sci Sect B 77:5–18Google Scholar
  12. Davis CC, Chase MW (2004) Elatinaceae are sister to Malpighiaceae; Peridiscaceae belong to Saxifragales. Am J Bot 91:262–273Google Scholar
  13. Davis CC, Wurdack KJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–678PubMedCrossRefGoogle Scholar
  14. Davis CC, Webb CO, Wurdack KJ, Jaramillo CA, Donoghue MJ (2005) Explosive radiation of Malpighiales supports a Mid-Cretaceous origin of modern tropical rain forests. Am Nat 165:E36–E65PubMedCrossRefGoogle Scholar
  15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  16. Hasebe M, Omori T, Nakazawa M, Sano T, Kato M, Iwatsuki K (1994) rbcL sequences provide evidence for the evolutionary lineages of leptosporangiate ferns. Proc Natl Acad Sci USA 91:5730–5734PubMedCrossRefGoogle Scholar
  17. van Heel WA (1973) Flowers and fruits in Flacourtiaceae I Scaphocalyx spathacea Ridl. Blumea 21:259–279Google Scholar
  18. van Heel WA (1979) Flowers and fruits in Flacourtiaceae IV Hydnocarpus spp. Kiggelaria africana L., Casearia spp., Berberidopsis corallina Hook.f. Blumea 25:513–529Google Scholar
  19. Hilu KW, Borsch T, Müller K, Soltis DE, Soltis PS, Savolainen V, Chase MW, Powell MP, Alice LA, Evans R, Sauquet H, Neinhuis C, Slotta TAB, Rohwer JG, Campbell CS, Chatrou LW (2003) Angiosperm phylogeny based on matK sequence information. Am J Bot 90:1758–1776Google Scholar
  20. Kathriarachchi H, Hoffmann P, Samuel R, Wurdack KJ, Chase MW (2005) Molecular phylogenetics of Phyllanthaceae inferred from five genes (plastid atpB, matK, 3’ ndhF, rbcL, and nuclear PHYC). Mol Phylogenet Evol 36:112–134PubMedCrossRefGoogle Scholar
  21. Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst Biol 45(4):524–545CrossRefGoogle Scholar
  22. Mauritzon J (1936) Zur embrylgie einiger Parietales-Familien Svensk bot Tidskr 30:79–113Google Scholar
  23. Netolitzky F (1926) Anatomie der Angiospermen-Samen. BerlinGoogle Scholar
  24. Nickrent DL, Starr EM (1994) High rates of nucleotide substitution in nuclear small-subunit (18S) rDNA from holoparasitic flowering plants. J Mol Evol 39:62–70PubMedCrossRefGoogle Scholar
  25. Ooi K, Endo Y, Yokoyama J, Murakami N (1995) Useful primer designs to amplify DNA fragments of the plastid gene matK from angiosperm plants. J Jap Bot 70:328–331Google Scholar
  26. Pax F, Hoffmann K (1931) Euphorbiaceae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien, 2nd edn, vol 19c, pp 11–233Google Scholar
  27. Raju MVS (1936) Development of embryo and seed coat in Turnera ulmifolia L. var. angustifolia Willd. Bot Not 1936:308–312Google Scholar
  28. Raju MVS (1952) Embryology of the Passifloraceae. Curr Sci 10:288–289Google Scholar
  29. Raju MVS (1956) Embryology of the Passifloraceae I Gametogenesis and seed development of Passiflora calcarata Mast. J Indian Bot Soc 35:126–138Google Scholar
  30. Raju MVS (1958) Seed development and fruit dehiscence in Ionidium suffruticosum Ging. Phytomorphology 8:218–224Google Scholar
  31. Rao AN (1957) The embryology of Hypericum patulum Thunb. and H. mysorense Hyene. Phytomorphology 7:139–149Google Scholar
  32. Savolainen V, Fay MF, Albach DC, Backlund A, van der Bank M, Cameron KM, Johnson SA, Lledó MD, Pintaud JC, Powell M, Sheahan MC, Soltis DE, Soltis PS, Weston P, Whitten WM, Wurdack KJ, Chase MW (2000a) Phylogeny of the eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bull 55:257–309Google Scholar
  33. Savolainen V, Chase MW, Hoot SB, Morton CM, Soltis DE, Bayer C, Fay MF, Bruijn AY de, Sullivan S, Qiu YL (2000b) Phylogenetics of flowering plants based on combined analysis of plastid atpB and rbcL gene sequences. Syst Biol 49:306–362PubMedCrossRefGoogle Scholar
  34. Setoguchi H, Tobe H, Ohba H (1992) Seed coat anatomy of Crossostylis (Rhizophoraceae): its evolutionary and systematic implications. Bot Mag Tokyo 105:625–638CrossRefGoogle Scholar
  35. Setoguchi H, Kosuge K, Tobe H (1999) Molecular phylogeny of Rhizophoraceae based on rbcL gene sequences. J Plant Res 112:443–455CrossRefGoogle Scholar
  36. Singh D (1963) Structure and development of ovule and seed of Viola tricolor L. and Ionidium suffruticosum Ging. J Indian Bot Soc 42:448–462Google Scholar
  37. Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Prince LM, Kress WJ, Nixon KC, Farris JS (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381–461CrossRefGoogle Scholar
  38. Stevens PF (2005) Angiosperm Phylogeny Website. Version 6, May 2005.
  39. Stuppy W (1996) Systematische Morphologie und Anatomie der Samen der biovulaten Euphorbiaceen. Diss KaiserslauternGoogle Scholar
  40. Swofford DL (2001) PAUP: Phylogenetic analysis using parsimony, ver 4.0b10. Sinauer, Sunderland, MAGoogle Scholar
  41. Tobe H, Raven PH (1984) An embryological contribution to systematics of the Chrysobalanaceae I Tribe Chrysobalaneae. Bot Mag Tokyo 97:397–411CrossRefGoogle Scholar
  42. Tobe H, Raven PH (1987) The embryology and relationships of Cassipourea and Sterigmapetalum (Rhizophoraceae-Macarisieae). Opera Bot 92:253–264Google Scholar
  43. Tokuoka T, Tobe H (1995) Embryology and systematics of Euphorbiaceae sens. lat.: a review and perspective. J Plant Res 108:97–96CrossRefGoogle Scholar
  44. Tokuoka T, Tobe H (1998) Ovules and seeds in Crotonoideae (Euphorbiaceae): structure and systematic implications. Bot Jahrb Syst 120:165–186Google Scholar
  45. Tokuoka T, Tobe H (1999) Embryology of tribe Drypeteae, an enigmatic taxon of Euphorbiaceae. Plant Syst Evol 215:189–208CrossRefGoogle Scholar
  46. Tokuoka T, Tobe H (2001) Ovules and seeds in subfamily Phyllanthoideae (Euphorbiaceae): structure and systematic implications. J Plant Res 114:75–92CrossRefGoogle Scholar
  47. Tokuoka T, Tobe H (2002) Ovules and seeds in Euphorbioideae (Euphorbiaceae): structure and systematic implications. J Plant Res 115:361–374PubMedCrossRefGoogle Scholar
  48. Tokuoka T, Tobe H (2003) Ovules and seeds in Acalyphoideae (Euphorbiaceae): structure and systematic implications. J Plant Res 116:355–380PubMedCrossRefGoogle Scholar
  49. Webster GL (1987) The saga of the spurges: a review of classification and relationships in the Euphorbiales. Bot J Linn Soc 94:3–46Google Scholar
  50. Webster GL (1994a) Classification of the Euphorbiaceae. Ann Mo Bot Gard 81:3–32CrossRefGoogle Scholar
  51. Webster GL (1994b) Synopsis of the genera and suprageneric taxa of Euphorbiaceae. Ann Mo Bot Gard 81:33–144CrossRefGoogle Scholar
  52. Wurdack KJ (2002) The molecular systematics and evolution of Euphorbiaceae sensu lato. Ph.D. dissertation, University of North Carolina, Chapel Hill, NCGoogle Scholar
  53. Wurdack KJ, Hoffman P, Chase MW (2005) Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) using plastid rbcL and trnL-F sequences. Am J Bot 92:1397–1420Google Scholar

Copyright information

© The Botanical Society of Japan and Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Natural Environmental Sciences, Faculty of Integrated Human StudiesKyoto UniversityKyotoJapan
  2. 2.Department of Botany, Graduate School of ScienceKyoto UniversityKyotoJapan

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