The Linderniaceae and Gratiolaceae are further Lineages Distinct from the Scrophulariaceae (Lamiales)

 

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Abstract

The Lamiales are one of the largest orders of angiosperms, with about 22 000 species. The Scrophulariaceae, as one of their most important families, has recently been shown to be polyphyletic. As a consequence, this family was re-classified and several groups of former scrophulariaceous genera now belong to different families, such as the Calceolariaceae, Plantaginaceae, or Phrymaceae. In the present study, relationships of the genera Craterostigma, Lindernia and its allies, hitherto classified within the Scrophulariaceae, were analyzed. Sequences of the chloroplast trnK intron and the matK gene (∼ 2.5 kb) were generated for representatives of all major lineages of the Lamiales and the former Scrophulariaceae. Bayesian and parsimony analyses revealed two isolated lineages, one of which consists of Lindernia and its allies, the other of Gratiola and allies. Gratiola was previously assumed to be related to Lindernia and was therefore included here. It is proposed to treat the two clades as separate families, Linderniaceae and Gratiolaceae. For the Linderniaceae, several morphological synapomorphies exist in addition to molecular data, such as conspicuous club-shaped stamen appendages.

References

• 1 Akaike H.. A new look at the statistic model identification.  IEEE Transactions on Automatic Control. (1974);  19 716-723
  CrossrefPubMedGoogle Scholar
• 2 Albach D. C., Chase M.. Paraphyly of Veronica (Veroniceae, Scrophulariaceae): Evidence from Internal Transcribed Spacer (ITS) Sequences of Nuclear Ribosomal DNA.  Journal of Plant Research. (2001);  114 9-18
  PubMedGoogle Scholar
• 3 APG2 . An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II.  Botanical Journal of the Linnean Society. (2003);  141 399-436
  CrossrefPubMedGoogle Scholar
• 4 Beardsley P. M., Olmstead R. G.. Redefining Phrymaceae: The placement of Mimulus, tribe Mimuleae, and Phryma.  American Journal of Botany. (2002);  89 1093-1102
  PubMedGoogle Scholar
• 5 Bentham G.. Scrophulariaceae. De Candolle, A. P., ed. Prodromus Systematis Naturalis 10. Paris; Lovell, Reeve & Co. (1846): 186-586
  Google Scholar
• 6 Bentham G.. Scrophulariaceae. Bentham, G. and Hooker, J. D., eds. Genera Plantarum 2. London; Lovell, Reeve & Co. (1876): 913-980
  Google Scholar
• 7 Borsch T., Hilu W., Quandt D., Wilde V., Neinhuis C., Barthlott W.. Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms.  Journal of Evolutionary Biology. (2003);  16 558-576
  CrossrefPubMedGoogle Scholar
• 8 Bremer B., Bremer K., Heidari N., Erixon P., Olmstead R. G.. Phylogenetics of asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higher taxonomic levels.  Molecular Phylogenetics and Evolution. (2002);  24 274-301
  CrossrefPubMedGoogle Scholar
• 9 Chiba T., Harada T., Goto S., Ishikawa R., Niizeki M.. Transcription of tRNA genes from large-scale plastid DNA deletion clearly reveals the action of nuclear-encoded RNA polymerase in the plastid.  Journal of Plant Physiology. (1996);  148 652-656
  PubMedGoogle Scholar
• 10 Doyle J. J., Doyle J. L.. Isolation of plant DNA from fresh tissue.  Focus. (1990);  12 13-15
  PubMedGoogle Scholar
• 11 Engler A.. Scrophulariaceae africanae II.  Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie. (1897);  23 500-5002
  PubMedGoogle Scholar
• 50 Fischer E.. Crepidorhopalon, a new genus with the relationship of Craterostigma, Torenia and Lindernia (Scrophulariaceae) with two new or note-worthy species from Central and South Central Africa (Zaire, Zambia).  Feddes Repertorium. (1989);  100 439-450
  PubMedGoogle Scholar
• 12 Fischer E.. Systematik der afrikanischen Lindernieae (Scrophulariaceae).  Tropische und subtropische Pflanzenwelt. (1992);  82 1-365
  PubMedGoogle Scholar
• 13 Fischer E.. Scrophulariaceae. Kubitzki, K., ed. The Families and Genera of Vascular Plants. Berlin; Springer (2004): 333-432
  Google Scholar
• 14 Gaff D.. Desiccation tolerant flowering plants in Southern Africa.  Science. (1971);  174 1033-1034
  PubMedGoogle Scholar
• 51 Graham S. W., Reeves P. A., Burns A. C. E., Olmstead R. G.. Microstructural changes ion noncoding chloroplast DNA: Interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference.  International Journal of Plant Science. (2000);  161 S83-S96
  CrossrefPubMedGoogle Scholar
• 15 Hallier H.. Ueber die Abgrenzung und Verwandtschaft der einzelnen Sippen bei den Scrophularineen.  Bulletin de la Herbarium Boissier, 2me série. (1903);  3 181-207
  PubMedGoogle Scholar
• 16 Hartl D.. Das Vorkommen rhinanthoider Knospendeckung bei Lindenbergia Lehm., einer Gattung der Scrophulariaceae-Antirrhinoideae.  Österreichische Botanische Zeitschrift. (1955);  102 80-83
  CrossrefPubMedGoogle Scholar
• 17 Hartl D.. Das alveolierte Endosperm bei Scrophulariaceen, seine Entstehung, Anatomie und taxonomische Bedeutung.  Beiträge zur Biologie der Pflanzen. (1959);  35 95-110
  PubMedGoogle Scholar
• 18 Hepper F. N.. Two new species of East African Craterostigma (Scrophulariaceae).  Kew Bulletin. (1987 a);  42 945-946
  PubMedGoogle Scholar
• 19 Hepper F. N.. Transfer of three tropical African species of Craterostigma to Torenia (Scrophulariaceae).  Boletim da Sociedade Broteriana, Série 2. (1987 b);  2 271-272
  PubMedGoogle Scholar
• 20 Hilu K. W., Borsch T., Müller K., Soltis D. E., Soltis P. S., Savolainen V., Chase M., Powell M., Alice L. A., Evans R., Sauquet H., Neinhuis C., Slotta T. A., Rohwer J. G., Campbell C. S., Chatrou L.. Angiosperm phylogeny based on matK sequence information.  American Journal of Botany. (2003);  90 1758-1776
  PubMedGoogle Scholar
• 21 Hjertson M.. Taxonomy, phylogeny and biogeography of Lindenbergia (Scrophulariaceae).  Botanical Journal of the Linnean Society. (1995);  119 265-321
  CrossrefPubMedGoogle Scholar
• 22 Huelsenbeck J. P., Ronquist F.. MrBayes: Bayesian inference of phylogenetic trees.  Bioinformatics. (2001);  17 754-755
  CrossrefPubMedGoogle Scholar
• 23 Huelsenbeck J. P., Ronquist F., Nielsen R., Bollback J. P.. Bayesian inference of phylogeny and its impact on evolutionary biology.  Science. (2001);  294 2310-2314
  CrossrefPubMedGoogle Scholar
• 24 Huelsenbeck J. P., Larget B., Miller R. E., Ronquist F.. Potential Applications and Pitfalls of Bayesian Inference of Phylogeny.  Systematic Biology. (2002);  51 673-688
  CrossrefPubMedGoogle Scholar
• 52 Kelchner S. A.. The evolution of non-coding chloroplast DNA and its application in plant systematics.  Annals of the Missouri Botanical Garden. (2000);  87 482-498
  PubMedGoogle Scholar
• 25 Löhne C., Borsch T.. Phylogenetic utility and molecular evolution of the petD group II intron in basal angiosperms.  Molecular and Biological Evolution. (in press); 
  PubMedGoogle Scholar
• 26 Magallon S., Crane P. R., Herendeen P. S.. Phylogenetic pattern, diversity, and diversification of eudicots.  Annals of the Missouri Botanical Garden. (1999);  86 297-372
  PubMedGoogle Scholar
• 27 Magin N., Classen R., Gack C.. The morphology of false anthers in Craterostigma plantagineum and Torenia polygonioides (Scrophulariaceae).  Canadian Journal of Botany. (1989);  67 1931-1937
  PubMedGoogle Scholar
• 28 Müller J., Müller K.. QuickAlign: A New Alignment Editor.  Plant Molecular Biology Reporter. (2003);  21 5
  PubMedGoogle Scholar
• 29 Müller K.. PRAP - computation of Bremer support for large data sets.  Molecular Phylogenetics and Evolution. (2004);  31 780-782
  CrossrefPubMedGoogle Scholar
• 53 Müller K., Borsch T.. Phylogenetics of Utricularia (Lentibulariaceae) and molecular evolution of the trnK intron in a lineage with high substitutional rates.  Plant Systematics and Evolution. (in press); 
  PubMedGoogle Scholar
• 30 Müller K., Borsch T., Legendre L., Porembski S., Theisen I., Barthlott W.. Evolution of carnivory in Lentibulariaceae and the Lamiales.  Plant Biology. (2004);  6 477-490
  Article in Thieme ConnectPubMedGoogle Scholar
• 31 Müller K.. SeqState - primer design and sequence statistics for phylogenetic DNA data sets.  Applied Bioinformatics. (in press); 
  PubMedGoogle Scholar
• 54 Nakai T.. Classes, ordinae, familiae, subfamilieae, tribus, genera nova quae attinent ad plantas Koreanas.  Journal of Japanese Botany. (1949);  24 8-14
  PubMedGoogle Scholar
• 32 Neuhaus H., Link G.. The chloroplast tRNALys(UUU) gene from mustard (Sinapis alba) contains a class II intron potentially coding for a maturase related polypeptide.  Current Genetics. (1987);  11 251-257
  CrossrefPubMedGoogle Scholar
• 33 Obermeyer A. A.. Lindernia intrepidus, South West Africa. The Flowering Plants of Africa, Vol. 38, pl. 1503. Pretoria; Dept. of Agricultural Technical Services (1967)
  Google Scholar
• 34 Olmstead R. G., Reeves P. A.. Evidence for the polyphyly of the Scrophulariaceae based on chloroplast rbcL and ndhF sequences.  Annals of the Missouri Botanical Garden. (1995);  82 176-193
  PubMedGoogle Scholar
• 35 Olmstead R. G., DePamphilis C. W., Wolfe A. D., Young N. D., Elisons W. J., Reeves P. A.. Disintegration of the Scrophulariaceae.  American Journal of Botany. (2001);  88 348-361
  PubMedGoogle Scholar
• 36 Pennell F. W.. The Scrophulariaceae of Eastern Temperate North America.  Academy of Natural Sciences of Philadelphia Monograph. (1935);  1 1-650
  PubMedGoogle Scholar
• 37 Philippi G.. Scrophulariaceae. Sebald, O. et al., eds. Die Farn- und Blütenpflanzen Baden-Württembergs. Stuttgart; Eugen Ulmer (1996)
  Google Scholar
• 38 Posada D., Crandall K. A.. Modeltest: testing the model of DNA substitution.  Bioinformatics. (1998);  14 817-818
  CrossrefPubMedGoogle Scholar
• 39 Reichenbach H. G.. Scrophulariaceae.  Flora Germanica Excursoria. (1831);  1 385ff
  PubMedGoogle Scholar
• 40 Rodriguez F. J., Oliver J. L., Marín A., Medina J. R.. The general stochastic model of nucleotide substitution.  Journal of Theoretical Biology. (1990);  142 485-501
  PubMedGoogle Scholar
• 41 Ronquist F., Huelsenbeck J. P.. MrBayes 3: Bayesian phylogenetic inference under mixed models.  Bioinformatics. (2003);  19 1572-1574
  CrossrefPubMedGoogle Scholar
• 42 Simmons M. P., Ochoterena H.. Gaps as characters in sequence-based phylogenetic analyses.  Systematic Biology. (2000);  49 369-381
  CrossrefPubMedGoogle Scholar
• 43 Soltis D. E., Soltis P. S., Chase M. W., Mort M. E., Albach D. C., Zanis M., Savolainen V., Hahn W. H., Hoot S. B., Fay M. F., Axtell M., Swensen S. M., Prince L. M., Kress W. J., Nixon K. C., Farris J. S.. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences.  Botanical Journal of the Linnean Society. (2000);  133 381-461
  PubMedGoogle Scholar
• 44 Swofford D. L., Olsen G., Waddell P. J., Hillis D. M.. Phylogenetic inference. Hillis, D. M. et al., eds. Molecular Systematics. Sunderland; Sinauer (1996)
  Google Scholar
• 45 Swofford D. L.. PAUP*. Phylogenetic Analysis Using Parsimony (*and other Methods). Sunderland; Sinauer Associates (1998)
  Google Scholar
• 46 Takhtajan A.. Diversity and Classification of Flowering Plants. New York; Columbia University Press (1997)
  Google Scholar
• 47 Urban I.. Studien über die Scrophulariaceen-Gattungen Ilysanthes, Bonnaya, Vandellia und Lindernia.  Bericht der Deutschen Botanischen Gesellschaft. (1884);  2 429-442
  PubMedGoogle Scholar
• 48 Wettstein  v. R.. Scrophulariaceae. Engler, A. and Prantl, K., eds. Die natürlichen Pflanzenfamilien 4. Leipzig; Engelmann (1891)
  Google Scholar
• 49 Yamazaki T.. Notes on Lindernia, Vandellia, Torenia and their allied genera in Eastern Asia I.  Journal of Japanese Botany. (1954);  29 299-306
  PubMedGoogle Scholar
• 55 Young N. D., Steiner K. E., DePamphilis C. W.. The evolution of parasitism in Scrophulariaceae/Orobanchaceae: Plastid gene sequences refute an evolutionary transition series.  Annals of the Missouri Botanical Garden. (1999);  86 876-893
  PubMedGoogle Scholar

T. Borsch

Nees-Institut für Biodiversität der Pflanzen
Universität Bonn

Meckenheimer Allee 170

53115 Bonn

Germany

Email: borsch@uni-bonn.de

Editor: F. Salamini