Plant Syst Evol (2009) 283:57–77 DOI 10.1007/s00606-009-0214-4 ORIGINAL ARTICLE How to get off the mismatch at the generic rank in African Podostemaceae? Mike Thiv Æ Jean-Paul Ghogue Æ Valentin Grob Æ Konrad Huber Æ Evelin Pfeifer Æ Rolf Rutishauser Received: 16 February 2009 / Accepted: 20 August 2009 / Published online: 10 September 2009 Ó Springer-Verlag 2009 Abstract The Podostemaceae are highly enigmatic plants taxa without stem scales but showing pollen as single which are restricted to submerged river-rock habitats. The grains, with Monandriella linearifolia being basal to this availability of new material of nine taxa from continental clade; (3) the Ledermanniella-Dyad clade including Djinga, Africa prompted this new study. Five species belonging to Dicraeanthus, and Ledermanniella species without stem the genera Dicraeanthus, Leiothylax, Letestuella, Macro- scales but with pollen dyads. To reduce the polyphyly of podiella, and Stonesia and another four species of the large Ledermanniella sensu lato (i.e. sensu C. Cusset) we propose genera Inversodicraea sensu stricto and Ledermanniella restricting Ledermanniella to the species of the former sensu stricto have been analysed for the first time. New subgenus Ledermanniella, resurrecting Monandriella as anatomical and developmental data are described and monotypic genus, and accepting the genus name Inverso- illustrated by use of microtome sections and scanning dicraea for members of Ledermanniella subg. Phyllosoma. electron microscopy. In parallel, phylogenetic analyses of all available sequence data of African Podostemaceae have Keywords African Podostemaceae Á Dicraeanthus Á been conducted using three plastid markers (matK, trnD- Inversodicraea Á Ledermanniella Á Leiothylax Á Letestuella Á trnT, rpoB-trnC). Inversodicraea cf. bosii appears basal Monandriella Á Molecular systematics Á Morphology Á within the continental African clade. The remaining taxa are Structural diversity Á Water plants Á matK Á trnD-trnT Á distributed in three, rather poorly supported, major clades rpoB-trnC which are consistent with their morphology: (1) the Inver- sodicraea clade is characterised by stem scales and contains members of the former Ledermanniella subg. Phyllosoma Introduction with either pollen-monads or dyads; (2) the Ledermanni- ella-Monad group consisting of Leiothylax, Letestuella, The Podostemaceae (‘‘river-weeds’’, including Tristicha- Macropodiella, Stonesia, and Ledermanniella species—all ceae of some authors; Malpighiales) are the largest family of strictly aquatic angiosperms (Cook and Rutishauser 2007). Molecular analyses indicate that Podostemaceae belong to Electronic supplementary material The online version of this the Malpighiales clade in the eurosids I group (Gustafsson article (doi:10.1007/s00606-009-0214-4) contains supplementary material, which is available to authorized users. et al. 2002; APG II 2003; Korotkova et al. 2009; Wurdack and Davis 2009) and might date back to the Campanian, M. Thiv (&) about 76 mya (Davis et al. 2005). Three subfamilies can be Staatliches Museum fu¨r Naturkunde, Stuttgart, Germany recognised: Tristichoideae and Weddellinoideae as the two e-mail: [email protected] smaller podostemaceous subfamilies, and as third subfamily J.-P. Ghogue the large and morphologically distinct Podostemoideae with Herbier National du Cameroun, Yaounde´, Cameroun 42 genera and ca. 270 spp. (Engler 1928; Kita and Kato 2001; Cook and Rutishauser 2007). V. Grob Á K. Huber Á E. Pfeifer Á R. Rutishauser Institut fu¨r Systematische Botanik, Universita¨tZu¨rich, In the past few years there has been a study focus on Zurich, Switzerland African, including Madagascan, Podostemoideae (Moline 123 58 M. Thiv et al. et al. 2007; Kita et al. 2008). They are classified in 16 Monandriella linearifolia (syn. L. monandra). Moreover, genera and ca. 82 species. Most of these inconspicuous we extended the number of chloroplast molecular markers, water plants are restricted to a single river or waterfall by sequencing matK, trnD-trnT, and rpoB-trnC for most of (Grob et al. 2007; Ameka et al. 2009). Many of the genera the taxa. and species in Africa occur in Cameroon and Gabon The Podostemaceae show many morphological pecu- (Engler 1928; Cusset 1987; Cook and Rutishauser 2007; liarities making this family a worthwhile, but often prob- Ghogue et al. 2009). lematic study object. Some features may be seen as The genera present in this region are, among others, adaptations to seasonally submerged river rocks with Dicraeanthus, Djinga, Inversodicraea, Ledermanniella, flowering in air possible for only a short period after the Leiothylax, Letestuella, Macropodiella, Monandriella, and rainy period. Many Podostemaceae have a flattened pho- Stonesia. Some of them, however, expand their range tosynthetic body which adheres to a hard substrate. It has outside of Cameroon and Gabon (Table 1). Identification been called a ‘‘thallus’’ because the conventional demar- keys, drawings and short descriptions of all African cation into stem, leaf, and root is often not obvious. Var- Podostemaceae are provided in Rutishauser et al. (2007), in ious botanists (Schnell 1998; Sehgal et al. 2002, 2007) addition to photographs of selected specimens. Molecular regard this vegetative body as a unique architectural type. data of African Podostemaceae have been analysed by, In contrast, we here adopt the classical root–shoot model e.g., Kita et al. (2005), Moline et al. (2007), and Pfeifer (CRS model) with its structural categories roots, shoots et al. (2009). (including stems and leaves), as already proposed by, e.g., Moline et al. (2007) used matK sequence and morpho- Warming (1881, 1891, 1899), Ja¨ger-Zu¨rn (2000), and Cook logical data for eight African Podostemaceae species of the and Rutishauser (2007). The term ‘‘stem’’ is applied to a genera Dicraeanthus, Djinga, and Ledermanniella sensu cylindrical or slightly flattened photosynthetic body that lato (incl. Inversodicraea). Accordingly, all podostemoids develops exogenous leaves. We use the term ‘‘root’’ for a studied from continental Africa form a clade that is sister to slightly or strongly flattened photosynthetic body when the Madagascan genera Endocaulos and Thelethylax. adhesive hairs and endogenous shoot buds are developed Moline et al. (2007) have already tentatively suggested but no exogenous leaves. revisions of the generic delimitations in the African taxa. The objectives of this study were: For example, Ledermanniella sensu lato (incl. Inversodic- 1 To perform a molecular phylogenetic analysis of raea and Monandriella), as described by Cusset (1974, African podostemoids and to include morphological 1984a, b), the largest podostemoid genus in Africa with ca. data across nine genera and 17 species. 46 spp., turned out to be an artificial and somewhat 2 To describe morphological idiosyncrasies of African awkward genus. Its two subgenera Ledermanniella and Podostemoideae and to plot them on to the molecular Phyllosoma (as proposed by Cusset 1984a, b) were distin- tree in order to describe their evolutionary history. guishable by the absence versus presence of stem scales in Special emphasis will be given to the infraspecific addition to the usually compound foliage leaves (Moline variability of stem scale morphology because this et al. 2007; Rutishauser et al. 2007). Before Cusset’s revi- feature is traditionally taken as very important for sion (1974, 1984a, b) most Ledermanniella spp. belonged to species delimitation in Inversodicraea (syn. Lederman- the genus Inversodicraea Engler ex R.E. Fries. Among the niella subg. Phyllosoma). To better visualise morpho- species known before Cusset and included in this study logical differences, members of four genera (Tables 1, 4), Ledermanniella bifurcata, L. bowlingii, (Dicraeanthus, Inversodicraea, Leiothylax, and Letes- L. cristata, L. ledermannii, and L. pusilla were members of tuella) will be described and illustrated using micro- Inversodicraea, whereas Ledermanniella (with L. lineari- tome sections and scanning electron microscopy. folia), and Monandriella (with M. linearifolia, syn. Leder- 3 To solve the mismatch at the generic rank in African manniella monandra) were monotypic genera. Podostemaceae–Podostemoideae. The availability of new material of these rarely collected plants prompted our new analysis. Since the study by Moline et al. (2007), material of five additional species from small genera such as Dicraeanthus zehnderi, Leio- Methods thylax quangensis, Letestuella tisserantii, Macropodiella heteromorpha, and Stonesia ghoguei became available to Taxon sampling us and has been analysed here. Four species from the large genus Ledermanniella sensu lato (incl. Inversodicraea, The objective of the sampling was to include representa- Monandriella) were also added: Inversodicraea cf. anni- tives of important groups of African Podostemaceae to thomae and I. cristata, Ledermanniella pusilla, and infer their infrageneric relationships. Information on the 123 African Podostemaceae Table 1 Vouchers, distribution and EMBL numbers of the selected taxa Voucher Origin Distribution EMBL acc. no. EMBL acc. no. EMBL acc. no. Ref. matK trnD-trnT rpoB-trnC Dicraeanthus africanus Engler Ghogue GHO-1413 (YA, Z/ZT) Cameroon Cameroon DQ168442 FM877851 FM877824 Moline et al. (2007) Dicraeanthus zehnderi H. Hess Ghogue GHO-1650 (YA, Z/ZT) Cameroon Cameroon (S) FM877834 FM877843 FM877812 This study (accession 1) Dicraeanthus zehnderi H. Hess Ghogue GHO-1651 (YA, Z/ZT) Cameroon idem FM877836 – FM877816