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(Mizutaniaceae, Marchantiophyta) Inferred from Molecular Phylogenetic Analyses

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(Mizutaniaceae, Marchantiophyta) Inferred from Molecular Phylogenetic Analyses Systematic position ofthe enigmatic liverwort Mizutania (Mizutaniaceae, Marchantiophyta) inferred from molecular phylogenetic analyses Hiroaki Masuzaki,l Masaki Shimamura,t Tatsuwo Furuki,2 Hiromi Tsubota,3 Tomio Yamaguchi,l 1 Haji Mohamed Abdul Majid 4 & Hironori Deguchi 1 Department 0/Biological Science, Graduate School a/Science, Hiroshima University, Kagamiyama 1-3-1, Higashi-Hiroshima 739-8526, Japan 2 Natural History Museum and Institute, Chiba, Aoba-cho 955-2, Chuo-ku, Chiba-shi, Chiba 260-8682, Japan 3 Miyajima Natural Botanical Garden, Graduate School a/Science, Hiroshima University, Mitsumaruko-yama 1156-2, Miyajima-cho, Hatsukaichi 739-0543, Japan 4 Biology Department, University Brunei Darussalam, Jalan Tungku Link, Gadong, Brunei Darussalam BE1410 Author for correspondence: Hiroaki Masuzaki, [email protected] Masuzaki & al. • Systematic position ofMizutania TAXON 59 (2) • April 2010: 448-458 Systematic position ofthe enigmatic liverwort Mizutania (Mizutaniaceae, Marchantiophyta) inferred from molecular phylogenetic analyses Hiroaki Masuzaki,l Masaki Shimamura,l Tatsuwo Furuki,2 Hiromi Tsubota,3 Tomio Yamaguchi,l 1 Haji Mohamed Abdul Majid 4 & Hironori Deguchi I Department 0/Biological Science, Graduate School o/Science, Hiroshima University, Kagamiyama 1-3-1, Higashi-Hiroshima 739-8526, Japan 2 Natural History Museum and Institute, Chiba, Aoba-cho 955-2, Chuo-ku, Chiba-shi, Chiba 260-8682, Japan 3 Miyajima Natural Botanical Garden, Graduate School o/Science, Hiroshima University, Mitsumaruko-yama 1156-2, Miyajima-cho, Hatsukaichi 739-0543, Japan 4 Biology Department, University Brunei Darussalam, Jalan Tungku Link, Gadong, Brunei Darussalam BE1410 Author for correspondence: Hiroaki Masuzaki, [email protected] Abstract Phylogenetic analyses of liverworts using chloroplast rbeL and rps4 sequences were performed with special refer­ ence to the enigmatic thalloid liverwort, Mizutania rieeardioides. The results showed that Mizutania is nested within leafy liverwort family Calypogeiaceae (subclass Jungermanniidae), thereby refuting the traditional interpretation that Mizutania is a member of the simple thalloid liverworts (subclass Metzgeriidae) related to Aneuraceae. Male plants with three ranked bracts, which are newly discovered in this study, also show a close morphological affinity to those ofleafy liverworts. Parallel evolution ofthe flattened gametophyte seems to have occurred sporadically in the Jungermanniidae in association with adapta­ tion to prostrate growth on the ground or on living leaves. The unistratose thalloid features ofMizutania are interpreted as an extremely reduced or highly specialized form of a creeping leafy liverwort. The rudimentary sexual branches which develop on the margins ofthe thallus are similar in many characteristics to those ofCalypogeiaceae. We reduce the monotypic family Mizutaniaceae to a synonym of Calypogeiaceae. Keywords Mizutania; molecular phylogeny; rbeL; rps4 • INTRODUCTION it has been collected from several other localities in Borneo and also in Malay Peninsular Malaysia (Furuki & Iwatsuki, Based on morphology, liverworts (Marchantiophyta) have 1989). This taxon is characterized by ribbon-like, unistratose traditionally been subdivided into the marchantioid group and thalli. Developing young thalli and regenerant buds on the thal­ jungermannioid group, the latter of which comprises two lus margins have a wedge-shaped apical cell with two cutting subgroups: the simple thalloid liverworts and the leafy ones faces (Inoue & aI., 2008) but apical protective structures such (Schuster, 1966). Recent molecular phylogenetic analyses of as slime papillae or scales are absent. Short female branches, liverworts (e.g., Heinrichs & aI., 2005; Forrest & aI., 2006; He­ rhizoids and exogenous gemmae are often found on the thallus Nygren & aI., 2006; Crandall-Stotler & aI., 2008) have brought margins. The surface ofthe thallus and gemmae are covered unexpected results. For example the Treubiales, previously with massive verrucae. Mizutania plants show a close morpho­ treated as members ofthe simple thalloids, were resolved as the logical affinity with the prothalli of ferns, particularly those earliest diverging group along with the leafy Haplomitriales. belonging to Hymenophyllaceae Mart. and Vittariaceae Ching. The Blasiales, previously treated as simple thalloid liverworts, Mizutania had long been misidentified as a fern prothallius for were resolved in the complex thalloid liverworts. And the Pleu­ over a quarter ofa century and specimens had been neglected roziales, possessing leaves with water sacs, were resolved as and stored away amongst unidentified bryophyte specimens sister to the Metzgeriales, comprising typical simple thalloid in herbaria. However, the presence ofperichaetialleaves sur­ liverworts. Only in a single decade, the analyses led to sig­ rounding the archegonia proved that Mizutania belongs to the nificant alteration ofthe conventionalliverwort classification bryophytes, because fern archegonia are always embedded in (compare Crandall-Stotler & Stotler, 2000; Crandall-Stotler & the prothallus and have no protective leafy structures (Furuki aI., 2008). However, several taxonomically enigmatic taxa still & Iwatsuki, 1989). In addition, branching ofthe thallus ofMizu­ remain to be studied by modern analysis, in order to resolve tania originates from an apical cell, which is characteristic of their classification. The family Mizutaniaceae Furuki & Z. a typical bryophyte. Furthermore, marginal meristems offern Iwats. is one ofthese enigmatic taxa. prothalli typically develop into branch thalli, a character not Mizutania riccardioides Furuki & Z. Iwats. was described found in Mizutania (Inoue & aI., 2008). Finally, the unicellular as a new species ofliverwort based on specimens collected by rhizoids and presence ofoil bodies in the cells strongly support M. Mizutani from Mt. Kinabalu, Borneo in 1963. Since then, the genus as a member ofthe liverworts. Therefore, the thalli 448 TAXON 59 (2)· April 2010: 448-458 Masuzaki & al. • Systematic position ofMizutania ofMizutania are not similar to fern prothalli. The chromosome genera in 22 families. Six exemplars with partial sequences number, n = 9, is also an additional character suggesting that were newly obtained, and 50 were downloaded from GenBank. the taxon is a member ofthe liverworts (Inoue & Furuki, 1992); Sequences for Marchantia polymorpha L. and Riccardia cap­ in liverworts, n = 9 is the most common number. ensis Arnell were added to the dataset as outgroups based on With a strong emphasis on the morphological characters the result ofphylogenetic analyses ofrbcL sequences. For ac­ mentioned above, Mizutania has been placed in its own fam­ cession numbers and voucher information ofthe datasets, see ily Mizutaniaceae (Furuki & Iwatsuki, 1989). Schuster (1992) Appendices SI and S2 in the Electronic Supplement to this and Crandall-Stotler & aI. (1994) considered Mizutania to be a article. Liverwort taxonomy and nomenclature basically fol­ member ofthe simple thalloid liverworts and placed the Mizu­ lows that of Crandall-Stotler & aI. (2008). Fresh materials of taniaceae in the suborder Metzgeriineae. Recent classification Mizutania were collected from three localities in West Malaysia studies have treated the families Mizutaniaceae, Aneuraceae, (Peninsular Malaya); Cameron Highlands (Aug. 2000, 2000 Metzgeriaceae and Vandiemeniaceae as closely related to each malt., T Yamaguchi 18890, T Furuki 16385, 16391; March other and have retained these families in the Metzgeriales 1989, 1440 malt, T Furuki & T Matsui 7659), Fraser's Hill (Crandall-Stotler & aI., 2008). Although Mizutania superfi­ (Sep.2005, 1200 malt., H Masuzaki 147, 170, T Furuki 20448, cially resembles members of Aneuraceae, particularly Ric­ T Yamaguchi 25802) and Genting Highlands (July 2007, 1600 cardia, there are many morphological differences. The thallus malt., H Masuzaki 894). Voucher specimens are deposited in of Riccardia, one of the simplest forms in the Metzgeriales, HIRO with duplicates in CBM. is composed of multiple cell layers in cross-section, whereas DNA extraction and peR amplification. - The protocol Mizutania is consistently unistratose. Riccardia may form en­ ofthe DNA-glass binding interaction method for extraction of dogenous gemmae (Furuki, 1991; Schuster, 1992) and ventral total DNA and direct sequencing by PCR was following the or occasionally dorsal rhizoids on the thallus, while Mizutania method ofTsubota & aI. (2005). For the denaturation of pro­ produces exogenous gemmae and marginal rhizoids, and pe­ teins in the DNA extraction, a halfvolume ofchloroform was richaetia originating from marginal cells (Furuki & Iwatsuki, added to the tube and mixed by vigorous shaking for 5 min. 1989). The chromosome number ofMizutania ofn = 9 (Inoue The design ofthe PCR and DNA sequencing primers follows & Furuki, 1992) is also in contrast to the basic number ofn = Tsubota & aI. (1999). The list of the newly designed primers 10 in Riccardia (Hewson, 1970). in this study is shown in Table 1. The systematic position of Mizutania is still enigmatic, Phylogenetic analysis. - Homology searches ofthe DNA because fertile plants with sporophytes have not yet been col­ databases using BLAST (Altschul & aI., 1997) were carried lected. In the present study, the ribulose bisphosphate carbox­ out based on the rbcL and rps4 sequences ofMarchantiapoly­ ylase large subunit (rbcL) and small ribosomal protein 4 (rps4) morpha (Ohyama & aI.,
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