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Poaceae: Bambusoideae) Reveals Ten Major Lineages and Low Rate of Molecular Divergence

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Poaceae: Bambusoideae) Reveals Ten Major Lineages and Low Rate of Molecular Divergence Molecular Phylogenetics and Evolution 56 (2010) 821–839 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Large multi-locus plastid phylogeny of the tribe Arundinarieae (Poaceae: Bambusoideae) reveals ten major lineages and low rate of molecular divergence Chun-Xia Zeng a,b,c,1, Yu-Xiao Zhang a,b,c,1, Jimmy K. Triplett d, Jun-Bo Yang a,c, De-Zhu Li a,c,* a Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650204, PR China b Graduate University of Chinese Academy of Sciences, Beijing 100049, PR China c Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming, Yunnan 650204, PR China d Department of Biology, National Museum of Natural History, MRC 166, Smithsonian Institution, Washington, DC 20013-7012, USA article info abstract Article history: The temperate bamboos (tribe Arundinarieae) are notorious for being taxonomically extremely difficult. Received 30 December 2009 China contains some of the world’s greatest diversity of the tribe Arundinarieae, with most genera and Revised 31 March 2010 species endemic. Previous investigation into phylogenetic relationships of the temperate bamboos Accepted 31 March 2010 revealed several major clades, but emphasis on the species-level relationships among taxa in North Available online 8 April 2010 America and Japan. To further elucidate relationships among the temperate bamboos, a very broad sam- pling of Chinese representatives was examined. We produced 9463 bp of sequences from eight non-cod- Keywords: ing chloroplast regions for 146 species in 26 genera and 5 outgroups. The loci sequenced were atpI/H, Arundinarieae psaA-ORF170, rpl32-trnL, rpoB-trnC, rps16-trnQ, trnD/T, trnS/G, and trnT/L. Phylogenetic analyses using China Chloroplast DNA regions maximum parsimony and Bayesian inference supported the monophyly of Arundinarieae. The two major Large sample size subtribes, Arundinariinae and Shibataeinae, defined on the basis of different synflorescence types, were Phylogenetic analysis indicated to be polyphyletic. Most genera in this tribe were confirmed to be paraphyletic or polyphyletic. The cladograms suggest that Arundinarieae is divided into ten major lineages. In addition to six lineages suggested in a previous molecular study (Bergbamboes, the African alpine bamboos, Chimonocalamus, the Shibataea clade, the Phyllostachys clade, and the Arundinaria clade), four additional lineages were recov- ered in our results, each represented by a single species: Gaoligongshania megalothyrsa, Indocalamus sini- cus, Indocalamus wilsonii, Thamnocalamus spathiflorus. Our analyses also indicate that (1) even more than 9000 bp of fast-evolving plastid sequence data cannot resolve the inter- and infra-relationships among and within the ten lineages of the tribe Arundinarieae; (2) an extensive sampling is indispensable for phylogeny reconstruction in this tribe, especially given that many genera appear to be paraphyletic or polyphyletic. Perhaps the ideal way to further illuminate relationships among the temperate bamboos is to sample multiple nuclear loci or whole chloroplast sequences in order to obtain sufficient variation. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction Graebner, and their herbaceous allies in tribe Olyreae Kunth ex Spen- ner (Clark et al., 1995; GPWG, 2001; Bouchenak-Khelladi et al., 2008; The grass subfamily Bambusoideae (true bamboos) as currently Sungkaew et al., 2009). circumscribed encompasses ca. 80–90 genera and 1000–1500 spe- The temperate bamboo tribe Arundinarieae is primarily distrib- cies distributed in temperate regions to mountains of the tropics uted in the North Temperate Zone or at high elevations in the Old worldwide, with the highest species richness in Asia Pacific and World tropics. There are approximately 32 genera and 600 temper- South America and the least in Africa (Bystriakova et al., 2003a,b). ate bamboo species, most of which are distributed in China and Ja- The subfamily has been resolved as monophyletic (GPWG, 2001), pan (Li, 1999; Ohrnberger, 1999). Arundinarieae is a highly consisting of members from the woody bamboo tribes Bambuseae diversified group with different habits (e.g., erect, arching, scan- s.s (Kunth ex Dumort.) and Arundinarieae Nees ex Ascherson and dent, twining, and decumbent) and complex features of morphol- ogy, including pachymorph or leptomorph rhizomes, solitary to many branches, semelauctant or iterauctant synflorescences, 3–6 * Corresponding author at: Key Laboratory of Biodiversity and Biogeography, stamens, and bacoid, nucoid or basic caryopsis (Keng and Wang, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 1996; Li et al., 2006; Yang et al., 2008; Yi et al., 2008). Based on 650204, PR China. Fax: +86 871 5217791. morphological and anatomical characters, the temperate bamboos E-mail addresses: [email protected], [email protected] (D.-Z. Li). are usually divided into two subtribes, Arundinariinae and 1 These authors contributed equally to this work. 1055-7903/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2010.03.041 822 C.-X. Zeng et al. / Molecular Phylogenetics and Evolution 56 (2010) 821–839 Table 1 Classification system of temperate bamboos by Li (1997). Tribe Bambuseae Subtribe Arundinariinae Acidosasa (Metasasa), Ampelocalamus, Arundinaria (incl. Bashania, Pleioblastus), Chimonocalamus, Drepanostachyum (incl. Himalayacalamus), Ferrocalamus, Gaoligongshania, Gelidocalamus, Indocalamus, Oligostachyum, Pseudosasa, Sasa, Sinarundinaria (incl. Borinda, Yushania), Thamnocalamus (Fargesia) Subtribe Shibatainae Chimonobambusa, Indosasa, Phyllostachys, Qiongzhuea, Semiarundinaria (Brachystachyum), Shibataea, Sinobambusa Shibataeinae, but with different treatments of genera within these amus jinpingensis (Yi et al., 2007b), and Indosasa jinpingensis (Yi, subtribes (Soderstrom and Ellis, 1987; Dransfield and Widjaja, 2001). Subtribal assignments in the classification of Li (1997; Table 1995; Li, 1997). 1) were adopted for this study. Various molecular data sets, including sequence data from the chloroplast genome (Ní Chonghaile, 2002; Triplett, 2008; 2.2. Taxon sampling Sungkaew et al., 2009) and nuclear GBSSI and ITS regions (Guo et al., 2001, 2002; Guo and Li, 2004; Zhuge et al., 2004; Peng Based on prior studies (Clark et al., 1995; GPWG, 2001; et al., 2008), as well as amplified fragment length (AFLP) data Bouchenak-Khelladi et al., 2008; Triplett, 2008; Sungkaew et al., (Triplett, 2008; Triplett et al., 2010) have been utilized to analyze 2009), Bonia amplexicaulis, Bonia levigata, Neomicrocalamus prainii, the temperate bamboos. These molecular phylogenetic studies Bambusa ventricosa, and Dendrocalamus farinosus of the tribe Bam- support Arundinarieae as a natural group, but relationships within buseae were chosen as outgroups. The ingroup taxa were chosen in the tribe remain unclear. Most recently, phylogenetic analyses order to include representatives for as many taxonomic groups as based on chloroplast DNA regions (including rpoB-trnC, rps16- possible within the tribe Arundinarieae. Type species for genera trnQ, trnD/T, and trnT/L intergenic spacers) provided additional in- and other subdivisions were included whenever material was avail- sights into the relationships within Arundinarieae (Triplett, 2008; able. DNA sequences from a total of 160 taxa in 30 genera were gen- Triplett and Clark, 2010). The tribe was resolved to include six ma- erated for this study from herbarium specimens or silica-dried plant jor lineages: Bergbamboes, the African alpine bamboos, Chimono- material. In addition, sequences of Yushania alpina (K. Schumann) calamus, the Shibataea clade, the Phyllostachys clade, and the Lin were retrieved from GenBank (Triplett and Clark, 2010). Table Arundinaria clade. That study also emphasized species-level 2 lists all species sequenced for this study and their sources. relationships among taxa in Japan and North America, but had relatively limited sampling of Chinese species. 2.3. Choice of markers In total, about 25 genera and 380 species of Arundinarieae occur in China (Keng and Wang, 1996; Li et al., 2006), representing In order to obtain phylogenetic resolution at species and generic approximatively 4/5 and 2/3 of the total number of genera and spe- levels within the ingroup, fast-evolving markers are needed. Triplett cies in the tribe, respectively. Of these taxa, most genera and spe- (2008) and Triplett and Clark (2010) identified twelve chloroplast re- cies are endemic to China. Therefore, the inclusion of these Chinese gions that were useful for the study of the temperate bamboos, taxa in molecular systematic studies of Arundinarieae is indispens- including the intergenic spacers atpI/H, ndhF(30 end), psaA- able for producing a comprehensive, phylogeny-based classifica- ORF170, rpl32-trnL, rpoB-trnC, rps16-trnQ, trnD/T, trnG intron, tion of the tribe. To date, no phylogenetic analysis has been trnH-psbA, trnK-rps16, trnT/L, and trnV-ndhC. After several pilot performed utilizing a comprehensive sampling of these species. studies, we also identified atpI/H, psaA-ORF170, rpl32-trnL, rpoB- In this paper, representatives from all subtribes and most genera trnC, rps16-trnQ, trnD/T, and trnT/L as being especially useful for of Arundinarieae in China according to Li (1997; Table 1) were se- our target group, plus the region trnS/G. Because of the low apparent quenced for
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