The Linderniaceae and Gratiolaceae Are Further Lineages Distinct from the Scrophulariaceae (Lamiales)
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Research Paper 1 The Linderniaceae and Gratiolaceae are further Lineages Distinct from the Scrophulariaceae (Lamiales) R. Rahmanzadeh1, K. Müller2, E. Fischer3, D. Bartels1, and T. Borsch2 1 Institut für Molekulare Physiologie und Biotechnologie der Pflanzen, Universität Bonn, Kirschallee 1, 53115 Bonn, Germany 2 Nees-Institut für Biodiversität der Pflanzen, Universität Bonn, Meckenheimer Allee 170, 53115 Bonn, Germany 3 Institut für Integrierte Naturwissenschaften ± Biologie, Universität Koblenz-Landau, Universitätsstraûe 1, 56070 Koblenz, Germany Received: July 14, 2004; Accepted: September 22, 2004 Abstract: The Lamiales are one of the largest orders of angio- Traditionally, Craterostigma, Lindernia and their relatives have sperms, with about 22000 species. The Scrophulariaceae, as been treated as members of the family Scrophulariaceae in the one of their most important families, has recently been shown order Lamiales (e.g., Takhtajan,1997). Although it is well estab- to be polyphyletic. As a consequence, this family was re-classi- lished that the Plocospermataceae and Oleaceae are their first fied and several groups of former scrophulariaceous genera branching families (Bremer et al., 2002; Hilu et al., 2003; Soltis now belong to different families, such as the Calceolariaceae, et al., 2000), little is known about the evolutionary diversifica- Plantaginaceae, or Phrymaceae. In the present study, relation- tion of most of the orders diversity. The Lamiales branching ships of the genera Craterostigma, Lindernia and its allies, hith- above the Plocospermataceae and Oleaceae are called ªcore erto classified within the Scrophulariaceae, were analyzed. Se- Lamialesº in the following text. The most recent classification quences of the chloroplast trnK intron and the matK gene by the Angiosperm Phylogeny Group (APG2, 2003) recognizes (~ 2.5 kb) were generated for representatives of all major line- 20 families. However, the recent literature (e.g., Olmstead et ages of the Lamiales and the former Scrophulariaceae. Bayesian al., 2001; Fischer, 2004) shows that concepts of several fami- and parsimony analyses revealed two isolated lineages, one of lies are in flux, as the number of genera increases that are in- which consists of Lindernia and its allies, the other of Gratiola cluded in phylogenetic analyses and as the addition of molec- and allies. Gratiola was previously assumed to be related to Lin- ular characters continues to produce new results. The genera dernia and was therefore included here. It is proposed to treat Craterostigma and Lindernia have so far not been included in the two clades as separate families, Linderniaceae and Gratiola- any phylogenetic analysis. ceae. For the Linderniaceae, several morphological synapomor- phies exist in addition to molecular data, such as conspicuous Wettstein (1891) included Craterostigma and Lindernia into a club-shaped stamen appendages. tribe Gratioleae, and this was also followed by other authors (e.g., Takhtajan, 1997). However, the Lindernieae were already Key words: Lamiales, Scrophulariaceae, poikilohydric plants, recognized as a separate tribe of the Scrophulariaceae (Rei- Linderniaceae, Gratiolaceae, phylogeny. chenbach, 1831) and as a subtribe of the Gratioloeae (Bentham, 1846). These two authors based their entity on corolla shape and geniculate stamens to originally comprise the genera Arta- nema D. Don, Curanga Juss (= Picria Lour.), Torenia L. (incl. Cra- Introduction terostigma Hochst. as a section), Vandellia L., Lindernia All., Ily- santhes Rafin., Bonnaya Link et Otto, Peplidium Del., Micran- With more than 22000 species, the Lamiales are one of the themum Rich., and Hemianthus Nutt. Urban (1884) lumped most diverse orders of angiosperms and include widely known Ilysanthes and Bonnaya, with two fertile stamens, on the one plants such as mints, foxgloves, and snapdragons. The Lam- hand, and Lindernia and Vandellia, with four fertile stamens, iales are monophyletic and comprise important families such on the other. This concept with two genera, Lindernia and Ily- as the Acanthaceae, Gesneriaceae, Lamiaceae, Lentibularia- santhes, was also presented by v. Wettstein (1891). Principally ceae, and Scrophulariaceae. Moreover, they are of scientific due to arguments giving weight to particular characters, the interest because desiccation-tolerant plants, such as Cratero- classification system within the Lindernieae continued to be stigma (Gaff, 1971), occur within this lineage. The present modified. The genera Torenia and Craterostigma were separat- analyses were in part motivated in order to provide a phyloge- ed out by Engler (1897), now using the winged calyx of Torenia netic context that can be used to reconstruct the evolution of as a main character. As a consequence, most species were in- characters involved in desiccation tolerance. cluded in a large genus Craterostigma. Pennell (1935) united Lindernia and Ilysanthes and argued that a reduction of sta- mens cannot be used as a generic character. Yamazaki (1954) tried to adopt characters such as seed anatomy and suggested Plant Biol. 7 (2005): 1 ±12 division of Lindernia into Lindernia s.str., with non-alveolated Georg Thieme Verlag KG Stuttgart ´ New York seeds, and Vandellia, with bothrospermous seeds. However, DOI 10.1055/s-2004-830444 this concept was ignored by most subsequent authors. More- ISSN 1435-8603 over, the monotypic Chamaegigas was included in Lindernia 2 Plant Biology 7 (2005) R. Rahmanzadeh et al. by Obermeyer (1967). The genus Crepidorhopalon Eb. Fisch. solving the backbone of core Lamiales, even when combining was described as including former members of Craterostigma, six different genomic regions (Bremer et al., 2002) or employ- Lindernia, and Torenia which share aulacospermous seeds and ing Bayesian approaches for tree inference (Müller et al., characteristic hairs on the lower corolla lip (Fischer, 1989). A 2004). However, the Gesneriaceae and Plantaginaceae appear further genus, Hartliella, was described during a revision of to be the first branching in both studies, although their relative the Lindernieae in Africa (Fischer, 1992). positions are unsupported. The fossil record of the Lamiales only dates back to the Tertiary (Magallon et al., 1999). There- The Scrophulariaceae in the circumscription of Bentham fore, the Lamiales represents a young angiosperm lineage, (1846, 1876) and Wettstein (1891) was traditionally treated as which possibly underwent rapid radiation in the Tertiary. This the largest family in the Lamiales. Other families, like the Oro- would imply that during early branching of the main lineages banchaceae, Lentibulariaceae, Globulariaceae, or Plantagina- few mutations were fixed, which may also be one of the rea- ceae, were recognized based on morphological differences, sons for the difficulty to infer Lamiales relationships. but were considered to be derived from an ancestral stock of the Scrophulariaceae. Only Hallier (1903) included the latter This study builds upon a set of complete sequences of the trnK families into the Scrophulariaceae, whereas most authors fol- intron (including the matK gene) that was originally generated lowed Wettstein in the circumscription and division of the to infer relationships of the Lentibulariaceae (Müller et al., Scrophulariaceae by dividing the family into the three sub- 2004). The matK gene (approx. 1600 bp) codes for a maturase families the Pseudosolaneae, Antirrhinoideae, and Rhinanthoi- and is located within domain IV of the trnK group II intron deae. Nevertheless, the Scrophulariaceae sensu Wettstein ap- (approx. 700 bp), upstream of psbA in the chloroplast genome peared as a heterogeneous and perhaps not natural group in large single copy region (Chiba et al., 1996; Neuhaus and Link, detailed morphological studies (e.g., Fischer, 1992). The first 1987). The aims of this contribution are to infer the phyloge- molecular phylogenetic analysis (Olmstead and Reeves, 1995) netic relationships of Lindernia and its allies, in particular, test- was based on rbcL and ndhF sequences and indicated that the ing their affinities to the Scrophulariaceae s.str. and the Planta- Scrophulariaceae are polyphyletic. Using a broader sampling ginaceae. Of particular relevance are those genera included and three genes, Olmstead et al. (2001) divided the Scrophu- into the Gratioleae (Wettstein, 1891). Molecular-based phylo- lariaceae into several distinct families: (I) Scrophulariaceae genetic hypotheses are then discussed in relation to morpho- s.str., comprising the Hemimerideae, Aptosimeae, Verbasceae, logical characters in the context of an updated classification Manuleae, Selagineae, and also Buddleja (Buddlejaceae) and system. Myoporum (Myoporaceae); and (II) the Veronicaceae, includ- ing the Gratioleae (without Mimulus), Antirrhineae, Cheloneae Materials and Methods (without Halleria) Hemimerideae, Digitalideae, and also Calli- triche (Callitrichaceae), Hippuris (Hippuridaceae), Globularia Plant material (Globulariaceae), and Plantago (Plantaginaceae). This latter clade is now referred to as the Plantaginaceae (APGII, 2003). Most plants sequenced for this study were either cultivated in Olmstead et al. (2001) included a core of the Gratioleae (Gra- the Botanical Gardens of Bonn University or collected in the tiola, Amphianthus and Bacopa) plus Angelonia (Hemimeridae) field by E. F. For detailed information see Table 1. into the Plantaginaceae because it appears as sistergroup to the remaining Plantaginaceae in their analysis, although lack-