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A Combined Morphological and Molecular Phylogenetic Analysis of Parthenocissus (Vitaceae) and Taxonomic Implications

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A Combined Morphological and Molecular Phylogenetic Analysis of Parthenocissus (Vitaceae) and Taxonomic Implications Botanical Journal of the Linnean Society, 2012, 168, 43–63. With 9 figures A combined morphological and molecular phylogenetic analysis of Parthenocissus (Vitaceae) and taxonomic implications LIMIN LU1,2, JUN WEN1,3* and ZHIDUAN CHEN1* 1State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, China 2Graduate School of Chinese Academy of Sciences, Beijing 100039, China 3Department of Botany, National Museum of Natural History, MRC166, Smithsonian Institution, Washington, D.C. 20013-7012, USA Received 21 June 2010; revised 11 March 2011; accepted for publication 18 August 2011 Parthenocissus (the Virginia creeper genus, Vitaceae) consists of 13 species and shows a disjunct distribution between Asia and North America. We investigated the inflorescence structure, calyx morphology, appendages on the inner side of petals, leaf epidermis, pollen and seed characters throughout the genus. A combined phylogenetic analysis with 27 morphological and 4137 molecular characters was conducted and the result was largely congruent with that of the previous molecular work, but with higher resolution. The combined analysis identified two clades corresponding to the Asian and North American taxa. Parthenocissus feddei was resolved as closely related to the clade containing P. cuspidifera, P. heterophylla and P. semicordata. The four species share synapomorphies of having conspicuously raised veinlets, an obscurely five- (to eight-) lobed calyx, appendages on the inner side of petals covering the entire length of anthers and foveolate pollen exine ornamentation. Within the Old World clade, the pentafoliolate species were weakly supported as more closely related to species with both simple and trifoliolate leaves. Furthermore, the ancestral states of tendril apices, inflorescence structure, appendages on the inner side of petals and exine ornamentation of pollen grains were reconstructed on the molecular strict consensus tree. The appendages on the inner side of petals and exine ornamentation of pollen grains were suggested to be important characters in the taxonomy of Parthenocissus, especially for species with trifoliolate leaves. Finally, the previous classifications of Parthenocissus were evaluated within the phylogenetic framework. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168, 43–63. ADDITIONAL KEYWORDS: morphology – phylogeny – seed morphology. INTRODUCTION Java to northern Thailand and three in North America (Soejima & Wen, 2006; Wen, 2007; Chen, Parthenocissus Planch. (the Virginia creeper genus, Ren & Wen, 2007). Vitaceae) consists of c. 13 species and shows a dis- Parthenocissus can be easily distinguished from junct distribution between Asia and North America the other genera of Vitaceae by its highly branched (extending to Mexico and the Caribbean region). tendrils, adhesive discs at tendril apices, inconspicu- There are approximately ten Old World species dis- ous floral discs and two long ventral infolds extending tributed primarily in eastern Asia, with one species in from the apex to the base of the seed (Brizicky, 1965; the western Ghats of India and Sri Lanka, one in Li, 1998; Chen et al., 2007; Wen, 2007). Li (1990) segregated Parthenocissus thomsoni (M.Lawson) Planch. and P. austro-orientalis Metcalf from Par- *Corresponding authors. E-mail: Jun Wen, [email protected]; thenocissus and established the new genus Yua Zhiduan Chen, [email protected] C.L.Li based on their bifurcate tendrils, leaf-opposed © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168, 43–63 43 44 L. LU ET AL. Table 1. Comparison of two classification systems of Parthenocissus by Galet (1967) and Li (1996). Names in parentheses indicate synonyms Galet (1967) Li (1996) Ser. Trifoliolae Galet Sect. Parthenocissus Ser. Trifoliolae Galet P. cuspidifera P. chinensis P. dalzielii P. cuspidifera P. heterophylla (P. neilgherriensis) P. feddei P. semicordata (P. anamallayana, P. himalayana) P. heterophylla Ser. Tricuspidatae Galet P. semicordata (P. cuspidifera var. pubifolia) Ser. Parthenocissus P. suberosa P. quinquefolia P. tricuspidata Sect. Margaritaceae C.L.Li Ser. Heterophyllae C.L.Li Ser. Quinquefoliolae Galet P. dalzielii Ser. Tricuspidatae Galet P. henryana P. suberosa P. heptaphylla P. tricuspidata P. laetevirens Sect. Tuberculiformes C.L.Li P. quinquefolia P. henryana P. vitacea P. laetevirens compound dichasium and ventral infolds extending recognized nine species and one variety of Partheno- upward two-thirds from the base of the seed. The cissus in China: P. chinensis C.L.Li, P. cuspidifera generic status of Yua has been supported by recent (Miq.) Planch. var. pubifolia C.L.Li, P. dalzielii molecular phylogenetic analyses (Wen et al., 2007; Gagnep., P. feddei (H.Lév.) C.L.Li, P. henryana Nie et al., 2010). (Hemsl.) Diels & Gilg, P. laetevirens Rehd., P. quin- Parthenocissus was established as a genus by Plan- quefolia (L.) Planch. (as an introduced species native chon (1887). Two infrageneric classification systems to North America), P. semicordata (Wall.) Planch., have been proposed since then (Table 1). Galet (1967) P. suberosa Hand.-Mazz. and P. tricuspidata (Sieb. & recognized three series in Parthenocissus: series Zucc.) Planch. The treatment by Chen et al. (2007) Tricuspidatae Galet mainly with simple leaves, series was largely congruent with that of Li (1998), except Trifoliolae Galet mainly with trifoliolate leaves and that P. cuspidifera var. pubifolia was treated as a series Quinquefoliolae Galet mainly with palmate synonym of P. semicordata in Chen et al. (2007). penta- (to hepta-) foliolate leaves. Based on tendril Species delimitation in south-eastern Asia and the morphology, Li (1996) divided the Chinese species of Himalayan region, however, has been highly contro- Parthenocissus into three sections: (1) section Par- versial. More than six names of species and infra- thenocissus with young tendril apices slender, curving specific taxa have been proposed in these regions and slightly expanded as fist-shaped adhesive discs; (e.g. P. anamallayana Planch., P. cuspidifera (Miq.) (2) section Margaritaceae C.L.Li with young tendril Planch., P. heterophylla (Blume) Merr., P. himalayana apices expanded into ball-like structures; and (3) (Royle) Planch., P. neilgherriensis (Wight) Planch. and section Tuberculiformes C.L.Li with palmate, pentafo- P. semicordata (Wall.) Planch.). The circumscrip- liolate leaves and young tendril apices expanded into tions of these species and their distribution require tubercles. investigation. Parthenocissus has a long and complex taxonomic Family level phylogenetic analyses have not history. Rehder (1905) recognized three species of resolved the relationships within Parthenocissus. Parthenocissus from North America: P. quinquefolia Ingrouille et al. (2002), using plastid rbcL sequences, (L.) Planch., P. vitacea (Knerr) Hitchc. and P. hepta- demonstrated the monophyly of Vitaceae and, on the phylla (Buckl.) Britton ex Small. His treatment has basis of two species, Parthenocissus. The plastid data been widely accepted by later workers (e.g. Brizicky, by Soejima & Wen (2006) supported the close rela- 1965; Soejima & Wen, 2006; Wen et al., 2007). The tionship between Parthenocissus and Yua, with three classification of Chinese Parthenocissus mainly species of Parthenocissus forming a clade with Yua follows Li (1998) and Chen et al. (2007). Li (1998) austro-orientalis. The GAI1 data, with more species of © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168, 43–63 PHYLOGENETIC ANALYSIS OF PARTHENOCISSUS 45 Parthenocissus sampled, resolved Parthenocissus Parthenocissus (Li, 1996). We also investigated char- as monophyletic with moderate support. Recently, acters such as veinlets, calyx morphology and append- Nie et al. (2010) presented a molecular phylogenetic ages on the inner side of petals, because these analysis of Parthenocissus based on the plastid (atpB- characters have never been systematically evaluated rbcL, rps16 and trnL-F) and nuclear GAI1 sequences. for this genus (e.g. Li, 1996). Calyx morphology and The monophyly of Parthenocissus was confirmed with appendages on the inner side of petals were observed strong support. Within Parthenocissus, two major and photographed with a stereomicroscope (a Nikon clades corresponding to their distribution in Asia and SMZ1000 with a Nikon DXM 1200F digital camera). North America were recognized. Within the Asian Under light microscopy (LM), the leaf epidermis of clade, three subgroups congruent with their leaflet all 13 Parthenocissus spp. and one species of Yua was numbers were recognized. The Asian pentafoliolate examined. Samples were taken from mature leaves of P. henryana and P. laetevirens were supported as c.1¥ 1cm2 in size, boiled in water for approximately being closely related to each other. Three taxa with 10 min and then macerated in Jeffery’s solution simple and trifoliolate leaves (P. dalzielii, P. tricuspi- (Stace, 1965). Pieces of leaf epidermis were stained in data and P. suberosa) formed a well-supported clade. a solution of 1% safranin (in 50% ethanol) and then Taxa with exclusively trifoliolate leaves (P. hetero- dehydrated in an ethanol series (50, 75, 85, 95 and phylla, P. semicordata, P. feddei and P. chinensis) 100%) before being mounted in Canada balsam. To formed a clade. Relationships within the three Asian check the consistency of epidermal characters, we clades, however,
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