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A molecular phylogeny of the wild onions

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A molecular phylogeny of the wild onions (Allium; Alliaceae) with a focus on the western North American center of diversityIntroductionMaterial and methodsTaxon samplingDNA extraction, PCR amplification, and sequencingSequence alignment and indel codingPhylogenetic analysesCharacter state reconstructionResultsSamplingMolecular datasetsPhylogenetic reconstructionCharacter state reconstructionDiscussionGlobal phylogenyTaxonomic considerationsSubgenus AmeralliumSection LophioprasonSections Amerallium, Caulorhizideum, and RhopetoprasonNatural History of Amerallium section LophiprasonSerpentine soils and Allium evolutionConclusionAcknowledgmentsReferencesA molecular phylogeny of the wild onions (Allium; Alliaceae)with a focus on the western North American center of diversityNhu H. Nguyen, Heather E. Driscoll, Chelsea D. Specht*Department of Plant and Microbial Biology, University of California, Berkeley, 111 Koshland Hall, MC 3102, Berkeley, CA 94720, USAReceived 20 September 2007; revised 4 December 2007; accepted 4 December 2007Available online 15 December 2007AbstractNuclear ribosomal DNA (ITS and ETS) sequences from 39 native Californian (USA) Allium species and congeners were combinedwith 154 ITS sequences available on GenBank to develop a global Allium phylogeny with the simultaneous goals of investigating theevolutionary history (monophyly) of Allium in the Californian center of diversity and exploring patterns of adaptation to serpentine soils.Phylogenies constructed with ITS alone or ITS in combination with ETS provided sufficient resolution for investigating evolutionaryrelationships among species. The ITS region alone was sufficient to resolve the deeper relationships in North American species. Additionof a second marker (ETS) further supports the phylogenetic placements of the North American species and adds resolution within sub-genus Amerallium, a clade containing many Californian endemics. Within the global phylogeny, the native North American species werefound to be monophyletic, with the exception of Allium tricoccum and Allium schoenoprasum. All native Californian species included inthe analysis fell into a monophyletic subgenus Amerallium section Lophioprason, although endemic Californian species were not mono-phyletic due to the inclusion of species with ranges extending beyond the California Floristic Province. The molecular phylogeny stronglysupports previous morphology-based taxonomic groupings. Based on our results, serpentine adaptation appears to have occurred multi-ple times within section Lophioprason, while the ancestor of the Californian center of diversity may not have been serpentine-adapted.Ó 2007 Elsevier Inc. All rights reserved.Keywords: Wild onion; Allium; ETS; ITS; Molecular phylogeny; Ecological reconstruction; Amerallium; Lophioprason; Serpentine; Californian endemic1. IntroductionThe California Floristic Province (CFP) is a Mediterra-nean-type ecosystem in western North America that isextremely varied in topography, microclimate, geologyand soils resulting in a high percentage of endemism ofits plants and animals. As one of only five Mediterraneanclimate areas in the world, the CFP has been classified asa Biodiversity Hotspot (Conservation International, 2007)and is the center of diversity in North America for manygroups of plants, including the genus Allium L.Allium comprises a major taxonomic portion of themonocot family All iaceae and consists of a diverse groupof perennial herbs characterized by rhizomatous or, morecommonly, bulbous stems (Fig. 1; M, N), narrow basalleaves, flowers with six free tepal s (Fig. 1; A, C, G–I) andsuperior ovaries with 0–6 crests (Fig. 1; C, H), inflorescenc-es of scapose umbels (Fig. 1; A–L), mucilaginous latex, anda distinctive onion-like odor and taste due to the presenceof cystine sulf oxides. Allium contains many economicallyimportant crop and ornamental species, including onion(Allium cepa), garlic (A. sativum), leek (A. ampeloprasum ),and chive (A. schoenoprasum). Allium is naturally distrib-uted throughout the Northern Hemisphere and is repre-sented by ca. 750 species worldwide (Stern, 1992)withca.100 species in North America (McNeal and Jacobsen,2002) and ca. 50 species and 20 varieties native to Califor-nia (McNeal, 1992; Hickm an, 1993). The genus is mainlyrestricted to regions that are seasonally dry, with centersof diversity in southwest/central Asia, eastern Asia, and1055-7903/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved.doi:10.1016/j.ympev.2007.12.006*Corresponding author. Fax: +1 510 642 4995.E-mail address: [email protected] (C.D. Specht).www.elsevier.com/locate/ympevAvailable online at www.sciencedirect.comMolecular Phylogenetics and Evolution 47 (2008) 1157–1172Fig. 1. Selected images of Allium (section Lophioprason) species used in this study. (A) A. falcifolium inflorescence and falcate leaves, (B) A. lemmonii, a speciesin subsection Falcifolia, (C) A. campanulatum showing the dark ovary crests in the center, (D) A. sanbornii, a representative of subsection Sanborniana, (E) A.sharsmithiae, a serpentine endemic species showing the umbel inflorescence, (F) A. diabolense, a species in subsection Sanborniana, (G) A. shevockii, a species insubsection Sanborniana, (H) A. haematochiton (serpentine form), (I) A. haematochiton (non-serpentine form) highlighting the pink ovary crests in the center,(J) A. amplectens (non-serpentine form), (K) A. unifolium, a representative in subsection Acuminata, (L) A. bolanderi, a species in subsection Bolanderiana,(M)A. bolanderi bulbs and rhizomes, (N) A. serra (‘‘herringbone” pattern in bulb scale), (O) A. fimbriatum var. purdyi growing on serpentine soil.1158 N.H. Nguyen et al. / Molecular Phylogenetics and Evolution 47 (2008) 1157–1172in North America. The two North American centers ofdiversity occur in Texas (ca. 15 species + 5 varieties) andthe California Floristic Province.Characters including nectary morphology, leaf numberand shape/size, ovary crest and seed morphology, inflores-cence structure, vegetative anatomy, basic chromosomenumber, and bulb/rhizome morphology in combinationwith biogeographic patterns have been used to place spe-cies into subgenera and sections. Many of these groupingshave been supported and refined with recent studies usingchloroplast and nuclear (ITS) genomic data (Samoylovet al., 1995; Linne von Berg et al., 1996; Dubouzet and Shi-noda, 1998, 1999; Mes et al., 1999; Samoylov


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