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Phylogeny and Biogeography of the Eastern Asian–North American Disjunct Wild-Rice Genus (Zizania L., Poaceae)

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Phylogeny and Biogeography of the Eastern Asian–North American Disjunct Wild-Rice Genus (Zizania L., Poaceae) Molecular Phylogenetics and Evolution 55 (2010) 1008–1017 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny and biogeography of the eastern Asian–North American disjunct wild-rice genus (Zizania L., Poaceae) Xinwei Xu a, Christina Walters b, Michael F. Antolin c, Mara L. Alexander d, Sue Lutz e, Song Ge f, Jun Wen e,f,* a Freshwater Ecological Field Station of Liangzi Lake, Wuhan University, Wuhan 430072, China b USDA/ARS National Center for Genetic Resources Preservation, 1111 South Mason Street, Fort Collins, CO 80521, USA c Department of Biology, Colorado State University, Fort Collins, CO 80523-1878, USA d San Marcos National Fish Hatchery and Technology Center, 500 East McCarty Lane, San Marcos, TX 78666, USA e Department of Botany, National Museum of Natural History, MRC 166, Smithsonian Institution, Washington, DC 20013-7012, USA f State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China article info abstract Article history: The wild-rice genus Zizania includes four species disjunctly distributed in eastern Asia and North Received 3 September 2009 America, with three species (Z. aquatica, Z. palustris, and Z. texana) in North America and one (Z. latifolia) Revised 17 November 2009 in eastern Asia. The phylogeny of Zizania was constructed using sequences of seven DNA fragments Accepted 18 November 2009 (atpB-rbcL, matK, rps16, trnL-F, trnH-psbA, nad1, and Adh1a) from chloroplast, mitochondrial, and nuclear Available online 26 November 2009 genomes. Zizania is shown to be monophyletic with the North American species forming a clade and the eastern Asian Z. latifolia sister to the North American clade. The divergence between the eastern Asian Z. Keywords: latifolia and the North American clade was dated to be 3.74 (95% HPD: 1.04–7.23) million years ago (mya) Adh1a gene using the Bayesian dating method with the combined atpB-rbcL, matK, rps16, trnL-F, and nad1 data. Biogeography Intercontinental disjunction Biogeographic analyses using a likelihood method suggest the North American origin of Zizania and its Wild-rice migration into eastern Asia via the Bering land bridge. Among the three North American species, the Zizania organellar data and the haplotype network of the nuclear Adh1a gene show a close relationship between Z. palustris and the narrowly distributed endangered species Z. texana. Bayesian dating estimated the divergence of North American Zizania to be 0.71 (95% HPD: 0.12–1.54) mya in the Pleistocene. The non-monophyly of Z. palustris and Z. aquatica in the organellar and nuclear data is most likely caused by incomplete lineage sorting, yet low-frequency unidirectional introgression of Z. palustris into Z. aquatica is present in the nuclear data as well. Published by Elsevier Inc. 1. Introduction and evolution of the disjunct taxa in both continents have rarely been examined (Wen, 1999; Xiang et al., 2004; Wen et al., 2009). The intercontinental disjunction between eastern Asia and The wild-rice genus Zizania L. belongs to the rice tribe (Oryzeae, North America is a well-known biogeographic pattern in the north- Poaceae) and is an aquatic/wetland genus with four species dis- ern hemisphere and has attracted considerable attention from junctly distributed between eastern Asia and North America (Ter- plant biologists (Xiang et al., 1998, 2000; Wen, 1999, 2001; Manos rell et al., 1997). In North America, two annual species Z. palustris and Donoghue, 2001). The phylogenetic relationships of disjunct L. (with var. palustris and var. interior (Fassett) Dore) and Z. aquatica lineages, the timing of the disjunctions, and migration pathways L. (with var. aquatica and var. brevis Fassett), are widespread in the of many taxa have been investigated based on molecular data Great Lake region and along the Atlantic coastal plains, respec- (e.g., Xiang et al., 1998; Wen, 2000; Nie et al., 2005, 2006a,b; Peng tively, and have some overlapping ranges (Aiken et al., 1988; Ter- and Wang, 2008). Most of these studies have focused on woody rell et al., 1997). The perennial Z. texana Hitchcock is restricted to a plants or terrestrial herbs, but few studies have examined aqua- 2.4 km area of the upper San Marcos River in southcentral Texas. It tic/wetland plants. At present, investigators have mainly discussed is an endangered species geographically isolated from all other the questions on the processes of the formation of the interconti- Zizania taxa by at least 640 km (Terrell et al., 1978). Zizania latifolia nental disjunct pattern, such as estimating divergence times and (Griseb.) Turcz. ex Stapf is a perennial widely distributed in eastern inferring ancestral areas. Questions on subsequent diversification Asia (Wu et al., 2006). Of the four species, two are economically important as field crops. Zizania palustris has served as a traditional staple for native Americans for centuries (Johnson, 1969) and as a * Corresponding author. Address: Department of Botany, MRC 166, Smithsonian Institution, Washington, DC 20013-7012, USA. Fax: +1 202 786 2563. specialty commercial crop more recently (Hayes et al., 1989; Oelke, E-mail address: [email protected] (J. Wen). 1993). Zizania latifolia was once used as an important grain in 1055-7903/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.ympev.2009.11.018 X. Xu et al. / Molecular Phylogenetics and Evolution 55 (2010) 1008–1017 1009 ancient China and has been cultivated as an aquatic vegetable be- and 0.6 U GoTaq DNA polymerase (Promega) in a volume of cause the young shoots become swollen, soft and edible after being 25 lL under the following conditions: 3 min at 95 °C, followed by infected by the fungus Ustilago esculenta P. Henn. (Thrower and 35 cycles of 30 s at 94 °C, 30 s at 50–55 °C, and 90 s at 72 °C, and Chan, 1980; Zhai et al., 2001; Guo et al., 2007). then a final 5 min extension at 72 °C. Amplifications were carried Previous phylogenetic studies of the rice tribe have supported out in a PTC-225 Peltier Thermal Cycler. the placement of Zizania in Oryzeae (Zhang and Second, 1989; Duv- The amplification and sequencing primers of the organellar re- all et al., 1993; Ge et al., 2002; Guo and Ge, 2005; Tang et al., 2010). gions were from the following sources: (1) the atpB-rbcL spacer Zizania is most closely related to the South American genus (Manen et al., 1994); (2) the trnH-psbA spacer (Hamilton, 1999); Rhynchoryza Baill. At the infrageneric level, the Asian Z. latifolia is (3) the trnL-F spacer (primers ‘‘c” and ‘‘f” of Taberlet et al., 1991); well differentiated from the North American species by its chromo- (4) the rps16 intron (Oxelman et al., 1997); (5) the matK gene some number and morphology (Duvall, 1987; Terrell et al., 1997), (Ge et al., 1999); and (6) the nad1 intron 2 (Demesure et al., whereas the relationships among three North American species are 1995; Guo and Ge, 2005). Two individuals from each population not fully resolved. Because of the overlap in distributional ranges were sequenced for the organellar regions and additional individ- and the existence of morphological intermediates, the two annual uals from sympatric populations and the Texas population were species, Z. palustris and Z. aquatica, were once treated as a single used. The nuclear Adh1a gene was amplified and sequenced with species (Fassett, 1924; Hitchcock and Chase, 1951). Later studies the Zizania-specific primers (Adh1aF1: 50-CTGACAGAGGTG- based on spikelet anatomy (Duvall and Biesboer, 1988a), artificial TAATGCTTA-30, Adh1aF2: 50-TCGGGACTTCGACCTTCAGT-30, and hybridization (Duvall and Biesboer, 1988b), and isozyme patterns Adh1aR, Xu et al., 2008) from six individuals of each population (Warwick and Aiken, 1986) supported the recognition of two an- of the annual species and 30 individuals of Zizania texana. The re- nual species. A close relationship between Z. texana and Z. aquatica gion of the outgroups was amplified and sequenced with primers is supported by the isoelectric focusing (IEF) profiles of seed pro- Adh1F6 and Adh1R7 (Zhang and Ge, 2007). tein (Duvall and Biesboer, 1989), whereas crossing behaviors sug- All PCR products were purified using the polyethylene glycol gest that Z. texana is more closely related to Z. palustris (Duvall, (PEG)/NaCl method of Kusukawa et al. (1990). Purified PCR prod- 1987). The latter relationship is supported by Horne and Kahn ucts were sequenced using the BigDye Terminator Cycle Sequenc- (1997) based on isozyme and nuclear ribosomal ITS sequence anal- ing Ready Reaction kit (Applied Biosystems). Sequencing reactions ysis. Nevertheless the hypothesis needs to be further tested be- were purified by gel filtration chromatography using Sephadex col- cause Horne and Kahn (1997) sampled only 3–4 individuals from umns (Amersham Pharmacia Biotech) and run on an ABI 3730xl a single population of each species and they used the distantly re- DNA analyzer (Applied Biosystems). The program Sequencher 4.5 lated Oryza sativa L. as the outgroup. The studies by Horne and (GeneCodes Corporation) was used to evaluate chromatograms Kahn (1997) and Xu et al. (2008) only examined the North Ameri- for base confirmation and to edit contiguous sequences. Individu- can or the eastern Asian species of Zizania, respectively. als in Zizania can be either homozygous or heterozygous at the The objectives of this study are to (1) construct the phylogeny Adh1a locus. For a heterozygote, sequences of two alleles can not to resolve the interspecific relationships in Zizania, (2) estimate be separated in the chromatogram when multi-point mutations the divergence times between intercontinental species and among or length differences caused by insertions or deletions exist be- intracontinental species, and (3) reconstruct the biogeographic his- tween the two alleles. In such cases, purified PCR products were tory of Zizania between eastern Asia and North America.
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