Advertisement

Plant Systematics and Evolution

, Volume 274, Issue 1–2, pp 111–126 | Cite as

Phylogeny of Cleome L. and its close relatives Podandrogyne Ducke and Polanisia Raf. (Cleomoideae, Cleomaceae) based on analysis of nuclear ITS sequences and morphology

  • Luis A. Inda
  • Pedro Torrecilla
  • Pilar Catalán
  • Thirza Ruiz-Zapata
Original Article

Abstract

A phylogenetic survey of representatives from all New World and several Old World supraspecific groupings of Cleome, as well as from the closely related Podandrogyne and Polanisia, was conducted based on separate analysis of nuclear ribosomal ITS sequences and of morphological characters. Parsimony analysis of the molecular data recognized this group of cleomoid taxa as a strongly supported monophyletic lineage. Podandrogyne was imbedded within a highly supported Andinocleome clade, whereas Polanisia was placed as a member of a North American/Old World Cleome s. l. clade but with low support. The ITS data also indicated the sequential divergence of several basal Old World (sects. Cleome, Gymnogonia, Ranmanissa and Rutidosperma) and North American (subg. Physospermon, sect. Peritoma) lineages followed by more recent splittings of Central and South American lineages (the Andinocleome (sects. Pterosperma and Rimosperma) group, and sects. Melidiscus and Tarenaya). The morphological data showed extensive homoplasy and did not resolve the phylogeny of these cleomoids, although the cladistic analysis distinguished two poorly supported (subg. Eucleome and sect. Tarenaya) clades. Despite this, several sets of morphological and chromosomal secondary synapomorphies served to characterize the main sectional clades recovered in the molecular tree. Based on the strong support of the Cleome + Podandrogyne + Polanisia clade and the insufficient resolution and low support of the basal branches of this tree, and on the inherent homoplasy and unsatisfactory resolution of the morphological diagnostic traits used to characterize these taxa, a reunification of the three cleomoid genera under a large genus Cleome s. l. would be advisable. A biogeographical interpretation of our molecular phylogeny indicated and earlier origin of the ancestral Cleome lineages in the Old World, followed by colonization of North America and then a subsequent expansion towards central and South American with more recent secondary radiations in these subcontinents.

Keywords

Cleome Cleomoideae ITS Morphology Phylogenetics Podandrogyne Polanisia 

Notes

Acknowledgments

We want to thank Hugh Iltis, Eric Schranz and Peter Stevens for their valuable comments and useful discussions on our phylogenetic study and for their critical review of our manuscript, Lupita Sánchez-Acebo (MO Bot. Gardens, USA) for providing us DNA accessions of Cleome and Polanisia, and D. Clark (COLO Herbarium, USA) and A. Ortega (University of Extremadura, Spain) for facilitating for us materials of C. serrulata and of C. violacea.

References

  1. Ainouche A-K, Bayer RJ (1999) Phylogenetic relationships in Lupinus (Fabaceae: Papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. Amer J Bot 86:590–607CrossRefGoogle Scholar
  2. Airy-Shaw HK (1965) Diagnoses of new families, new names, etc., for the seventh edition of Willis’s ‘Dictionary’. Kew Bull 18(2):256 [Cleomaceae]Google Scholar
  3. Al Shehbaz IA (1973) The biosystematics of the genus Thelypodium (Cruciferae). Contrib Gray Herbarium 204:3–148Google Scholar
  4. Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann Missouri Bot Gard 82:247–277CrossRefGoogle Scholar
  5. Bell CD, Donoghue MJ (2005) Phylogeny and biogeography of Valerianaceae (Dipsacales) with special reference to the South American valerians. Org Divers Evol 5:147–159CrossRefGoogle Scholar
  6. Blattner FR (2006) Multiple intercontinental dispersals shaped the distribution area of Hordeum (Poaceae). New Phytol 169:603–614PubMedCrossRefGoogle Scholar
  7. Catalán P (2006) Phylogeny and evolution of Festuca L. and related genera of subtribe Loliinae (Poeae, Poaceae). In: Sharma AK, Sharma A (eds) Plant genome: biodiversity and evolution. vol 1D. Chap. 10. Enfield, New Hampshire, pp 255–303Google Scholar
  8. Cochrane TS (1978) Podandrogyne formosa (Capparidaceae) a new species from Central America. Brittonia 30:405–410CrossRefGoogle Scholar
  9. De Candolle AP (1824) Prodromus Systematis Naturalis Regni Vegetabilis 1:241–242Google Scholar
  10. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  11. Ducke A (1930) Plantes nouvelles ou peu connues de la région amazonienne. Archiv Jard Bot Rio de Janeiro 5:115–116 pl. 7Google Scholar
  12. Eichler A (1865) Capparidaceae. In: Martius (ed) Flora Brasiliensis 13(1):238–292, Tables 51–65Google Scholar
  13. Felsenstein J (1985) Phylogenies and the comparative method. Amer Naturalist 125:1–15CrossRefGoogle Scholar
  14. Hall JC, Sytsma KJ, Iltis HH (2002) Phylogeny of Capparaceae and Brassicaceae based on chloroplast sequence data: solving the riddle of the Californian cuisine. Amer J Bot 89:1826–1842CrossRefGoogle Scholar
  15. Hall JC, Iltis HH, Sytsma KJ (2004) Molecular phylogenetics of core Brassicales, placement of orphan genera Emblingia, Forchhammeria, Tirania, and character evolution. Syst Bot 29:654–669CrossRefGoogle Scholar
  16. Heilborn O (1931) Section Fruticosae Eichl. of the genus Cleome L. Arkiv For Botanik 23(10):1–19Google Scholar
  17. Hsiao C, Chatterton NJ, Asay KH, Jensen KB (1995) Molecular phylogeny of the Pooideae (Poaceae) based on nuclear rDNA (ITS) sequences. Theor Appl Genet 90:389–398CrossRefGoogle Scholar
  18. Hutchinson J (1967) The genera of flowering plants 2. (Capparidaceae). Clarendon Press, Oxford, pp 303–317Google Scholar
  19. Hutchinson J (1969) Evolution and phylogeny of flowering plants. Academic Press, LondonGoogle Scholar
  20. Iltis HH (1952) A revision of the New World species of Cleome. Ph. D. thesis, Washington University, St Louis, 335 pGoogle Scholar
  21. Iltis HH (1957) Studies in the Capparidaceae. III. Evolution and phylogeny of the western of North American Cleomoideae. Ann Missouri Bot Gard 44:77–119CrossRefGoogle Scholar
  22. Iltis HH (1958) Studies in the Capparidaceae. IV. Polanisia Raf. Brittonia 10:33–58CrossRefGoogle Scholar
  23. Iltis HH (1959) Studies in the Capparidaceae. IV. Cleome sect. Physostemon: taxonomy, geography and evolution. Brittonia 11:123–162CrossRefGoogle Scholar
  24. Iltis HH (1960) Studies in the Capparidaceae. VII. Old World Cleomes adventive in the New World. Brittonia 12:279–294CrossRefGoogle Scholar
  25. Iltis HH (1992) Capparaceae. In: Families and genera of Spermatophytes recognized by the Agricultural Research Service. Department of Agriculture, USA. Technical Bulletin, no. 1796, pp 127–128Google Scholar
  26. Iltis HH, Cochrane TS (1989) Studies in the Capparidaceae- XVI. Podandrogyne a new species and three new combinations. Rev Acad Colomb Cienc 17(65):265–270Google Scholar
  27. Judd W, Sanders R, Donoghue M (1994) Angiosperm family pairs: preliminary phylogenetic analysis. Harvard Pap Bot 5:1–51Google Scholar
  28. Keller S (1979) A revision of the genus Wislizenia (Capparaceae) based on populations studies. Brittonia 31:333–351CrossRefGoogle Scholar
  29. Kers LE (2003) Capparaceae. In: Kubitzki K, Bayer C (eds) Flowering plants. Dicotyledons. Malvales, Capparales and Non-betalain Caryophyllales. In: Kubitzki K (ed) The families and genera of vascular plants, vol 5. Springer, Heidelberg, pp 36–56Google Scholar
  30. Koshy JK, Mathew PM (1985) Cytology of the genus Cleome Linn. Cytologia 50(2):283–287Google Scholar
  31. Linden J, Planchon JE (1863) Troisiéme Voyage de J. Linden, dans les parties intertropicales de l’Amerique. Plantae Columbianae 1:17–20 [Capparidaceae]Google Scholar
  32. Maddison WP, Maddison DR (1992) Mac Clade. Analysis of phylogeny and character evolution. Version 3. Sinauer Ass, SunderlandGoogle Scholar
  33. Mitchell AD, Heenan PB (2000) Systematic relationshipsof New Zealand endemic Brassicaceae inferred from nrDNA ITS sequence data. Syst Bot 25:98–105CrossRefGoogle Scholar
  34. Ondurff R (ed) (1967) Index to plant chromosome numbers for 1965. Regnum Vegetabile 50Google Scholar
  35. Pax F, Hoffmann K (1936) Capparidaceae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien. 2nd edn. 17 b: Leipzig, pp 146–223Google Scholar
  36. Rambaud A (1996) Sequence Alignment Editor (Se-Al). Ver 1.0 alpha 1. Oxford University, OxfordGoogle Scholar
  37. Reid G, Sidwell K (2002) Overlapping variables in botanical systematics. In: McLeod N, Forey PL (eds) Morphology, shape and phylogeny. Systematics Association Special Volume Series 64, Taylor & Francis, London, pp 53–66Google Scholar
  38. Rodman JE (1991) A taxonomic analysis of glucosinolate-producing plants, part 2: cladistics. Syst Bot 16(4):619–629CrossRefGoogle Scholar
  39. Rodman JE, Price RA, Karol K, Conti E, Sytsma KJ, Palmer JD (1993) Nucleotide sequences of the rbcL gene indicate monophyly of mustard oil plants. Ann Missouri Bot Gard 80:686–699CrossRefGoogle Scholar
  40. Rodman JE, Karol K, Price RA, Sytsma KJ (1996) Molecules, morphology, and Dahlgren´s expanded order Capparales. Syst Bot 21(3):289–307CrossRefGoogle Scholar
  41. Rodman JE, Soltis PS, Soltis DE, Sytsma KJ, Karol K (1998) Parallel evolution of glucosinolate biosynthesis inferred from congruent nuclear and plastid gene phylogenies. Amer J Bot 85(7):997–1006CrossRefGoogle Scholar
  42. Ruiz-Zapata T, Escala M (1995) La ultramicromorfología de semillas de Cleome L. (Capparidaceae) en relación con su taxonomía y síndromes de dispersión. Ernstia 5:139–160Google Scholar
  43. Ruiz-Zapata T, Xena de Enrech N (1997) La morfología del polen de Cleome L. (Capparidaceae) en relación con su taxonomía y síndromes de polinización. Acta Bot Venez 20:67–80Google Scholar
  44. Ruiz-Zapata T, Huérfano AA, Xena de Enrech N (1996) Contribución al estudio citotaxonómico del género Cleome L. (Capparidaceae). Fyton 59:85–94Google Scholar
  45. Sánchez-Acebo L (2002) A phylogenetic study of the genus Cleome L. (Brassicaceae-Cleomoideae) based on chloroplast sequence data. M.S. Thesis. University of Missouri-St Louis, USAGoogle Scholar
  46. Sánchez-Acebo L (2005) A phylogenetic study of the New World Cleome (Brassicaceae-Cleomoideae). Ann Missouri Bot Gard 92:179–201Google Scholar
  47. Schranz ME, Mitchell-Olds T (2006) Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Pl Cell 18:1152–1165CrossRefGoogle Scholar
  48. Soreng RJ (1990) Chloroplast-DNA phylogenetics and biogeography in a reticulating group: study in Poa (Poaceae). Amer J Bot 77:1383–1400CrossRefGoogle Scholar
  49. Swofford DL (2002) PAUP: Phylogenetic analysis using parsimony and other methods. Ver 4.0 beta 10 Sinauer. SunderlandGoogle Scholar
  50. 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. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  51. Torrecilla P, López-Rodríguez JA, Catalán P (2004) Phylogenetic relationships of Vulpia and related genera (Poeaae; Poaceae) based on analysis of ITS and trnL-F sequences. Ann Missouri Bot Gard 91:124–158Google Scholar
  52. Triana J, Planchon JE (1862) Prodromus Florae novo Granatensis. Ann Sc Nat Bot Ser 4 17(2):65–128Google Scholar
  53. Turczaninov N (1854) Animadversiones ad primam partem herbaria turczaninowiam, nunc universitatis Caesareae Charkowiensis. Bull Soc Imp Nat Mosc 27(2):313–329 [Capparidaceae]Google Scholar
  54. Unfried I, Gruendler P (1990) Nucleotide sequence of the 5.8S and 25S rRNA genes and of the internal transcribed spacers from Arabidopsis thaliana. Nucleic Acids Res 18:4011PubMedCrossRefGoogle Scholar
  55. Warwick SI, Al-Shehbaz IA, Price RA, Sauder C (2002) Phylogeny of Sisymbrium (Brassicaceae) based on ITS sequences of nuclear ribosomal DNA. Canad J Bot 80:1002–1017CrossRefGoogle Scholar
  56. Woodson RE (1948) Gynandropsis, Cleome and Podandrogyne. Ann Missouri Bot Gard 35:139–147CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Luis A. Inda
    • 1
  • Pedro Torrecilla
    • 2
  • Pilar Catalán
    • 1
  • Thirza Ruiz-Zapata
    • 2
  1. 1.Departamento de Agricultura y Economía Agraria, Escuela Politécnica Superior de HuescaUniversidad de ZaragozaHuescaSpain
  2. 2.Instituto de Botánica AgrícolaUniversidad Central de VenezuelaMaracayVenezuela

Personalised recommendations