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P020120713547028261576.Pdf This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Molecular Phylogenetics and Evolution 64 (2012) 452–470 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Three genome-based phylogeny of Cupressaceae s.l.: Further evidence for the evolution of gymnosperms and Southern Hemisphere biogeography ⇑ Zu-Yu Yang a,b, Jin-Hua Ran a, Xiao-Quan Wang a, a State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China b Graduate University of the Chinese Academy of Sciences, Beijing 100039, China article info abstract Article history: Phylogenetic information is essential to interpret the evolution of species. While DNA sequences from Received 1 April 2011 different genomes have been widely utilized in phylogenetic reconstruction, it is still difficult to use Revised 1 May 2012 nuclear genes to reconstruct phylogenies of plant groups with large genomes and complex gene families, Accepted 2 May 2012 such as gymnosperms. Here, we use two single-copy nuclear genes, together with chloroplast and mito- Available online 18 May 2012 chondrial genes, to reconstruct the phylogeny of the ecologically-important conifer family Cupressaceae s.l., based on a complete sampling of its 32 genera. The different gene trees generated are highly congru- Keywords: ent in topology, supporting the basal position of Cunninghamia and the seven-subfamily classification, LEAFY (LFY) and the estimated divergence times based on different datasets correspond well with each other and with NEEDLY (NLY) Allopolyploid origin the oldest fossil record. These results imply that we have obtained the species phylogeny of Cupressaceae Ancient hybridization s.l. In addition, possible origins of all three polyploid conifers were investigated, and a hybrid origin was Gymnosperm suggested for Cupressus, Fitzroya and Sequoia. Moreover, we found that the biogeographic history of Gondwana Cupressaceae s.l. is associated with the separation between Laurasia and Gondwana and the further break-up of the latter. Our study also provides new evidence for the gymnosperm phylogeny. Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction convincing if divergence time estimates are congruent among different genes and consistent with the fossil record. Reconstructing plant phylogenies using sequences from inde- In the past decade, low-copy nuclear genes have been widely pendent nuclear loci and different genomic compartments has utilized to improve the resolution and robustness of plant phyloge- been increasingly popular due to the growing awareness that rely- netic reconstruction at various taxonomic levels (e.g., Wang et al., ing on a single data set may result in insufficient phylogenetic res- 2000; Sang, 2002; Peng and Wang, 2008). However, this use is lim- olution or misleading inferences (Maddison, 1997; Wendel and ited by the problems associated with the complex evolutionary Doyle, 1998). Phylogenetic congruence among different genomic dynamics of nuclear genes, such as gene paralogy, recombination, compartments could strongly suggest that the gene trees are also lineage sorting, and lateral gene transfer (Small et al., 2004). This congruent with the species phylogeny (Wang et al., 2000). On the limitation is particularly notable for gymnosperms due to the large other hand, molecular dating has proved very efficient in estimat- nuclear genomes and complex gene families (Kinlaw and Neale, ing evolutionary divergence times of diverse taxa (e.g., Wang et al., 1997; Murray, 1998; Leitch et al., 2001; Ahuja and Neale, 2005), 2000; Sanderson, 2002; Knapp et al., 2005; Barker et al., 2007; as well as the unavailability of complete genome sequences so Sauquet et al., 2009), although there are still some controversies far. In contrast to other low-copy nuclear genes with a high rate regarding mainly the appropriateness of the selected model, of birth and death evolution, the use of sister genes from ancient calibration procedure, effect of long branches, and degree of gene duplication could minimize these potential problems when congruence between time estimates and the fossil record (e.g., both copies exist in the studied taxa. Kumar, 2005; Magallón and Sanderson, 2005; Rutschmann et al., Cupressaceae s.l., including Cupressaceae s.s. and traditional 2007; Inoue et al., 2010; Magallón, 2010). It would be more Taxodiaceae without Sciadopitys, is an important component of for- ests, and comprises 32 genera and more than 130 species (Farjón, 2005; Adams et al., 2009; Debreczy et al., 2009). Among them, only four genera, i.e., Callitris, Cupressus, Hesperocyparis (a New World ⇑ Corresponding author. Address: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, 20 genus separated from Cupressus)(Adams et al., 2009) and Juniperus, Nanxincun, Xiangshan, Beijing 100093, China. Fax: +86 10 62590843. have more than 10 species, and as many as 19 genera are monotypic. E-mail address: [email protected] (X.-Q. Wang). Cupressaceae s.s. was first separated from Taxodiaceae by Pilger 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.05.004 Author's personal copy Z.-Y. Yang et al. / Molecular Phylogenetics and Evolution 64 (2012) 452–470 453 (1926), but afterwards the morphological, anatomical, embryologi- The LEAFY (LFY) gene that encodes a transcription factor in- cal, immunological, and cladistic studies (Eckenwalder, 1976; Hart, volved in regulating cell division and arrangement or floral meri- 1987; Price and Lowenstein, 1989; Farjón, 2005; Schulz and Stutzel, stem identity occurs in all land plants (Frohlich and Meyerowitz, 2007) as well as molecular investigations (Brunsfeld et al., 1994; 1997; Maizel et al., 2005; Tanahashi et al., 2005; Moyroud et al., Tsumura et al., 1995; Chaw et al., 1997, 2000; Stefanovic et al., 2010). Although this gene exists as a single-copy in most diploid 1998; Gadek et al., 2000; Kusumi et al., 2000; Quinn et al., 2002; angiosperms, its sister gene NEEDLY (NLY) that originated from a Rydin et al., 2002; Schmidt and Schneider-Poetsch, 2002; Rai duplication event in the common ancestor of seed plants still re- et al., 2008) consistently support a merger of the two families. For mains in gymnosperms (Frohlich and Meyerowitz, 1997; Moura- the infra-familial classification of Cupressaceae s.l., Gadek et al. dov et al., 1998; Maizel et al., 2005; Vazquez-Lobo et al., 2007; (2000) divided the family into seven subfamilies based on morpho- Shiokawa et al., 2008). Thus, the duplicated sister genes LFY and logical and cpDNA evidence, which include Cunninghamioideae, NLY are very suitable to be used as nuclear gene markers for the Taiwanioideae, Athrotaxidoideae, Sequoioideae, Taxodioideae, phylogenetic reconstruction of Cupressaceae s.l. Callitroideae and Cupressoideae. However, Farjón (2005) did not Recently, the LFY gene, especially its second intron, has been recognize the subfamily Callitroideae that occurs in the Southern widely used to reconstruct the phylogeny of many angiosperm Hemisphere, and treated Cupressaceae s.s. as a subfamily (Cupres- groups (e.g., Oh and Potter, 2003; Grob et al., 2004; Kim et al., soideae) rather than two subfamilies. 2008), and several genera of gymnosperms such as Gnetum (Won All previous molecular phylogenies of Cupressaceae (s.l. or s.s.) and Renner, 2006), Thuja (Peng and Wang, 2008), and Pseudotsuga were reconstructed based on chloroplast DNA (cpDNA) markers (Wei et al., 2010). Also, the NLY gene has been used to resolve the (Tsumura et al., 1995; Gadek and Quinn, 1993; Brunsfeld et al., interspecific relationships of Cupressus (Little, 2006). Moreover, 1994; Gadek et al., 2000; Kusumi et al., 2000), although 4–10 genera there is a rich fossil record of Cupressaceae s.l. (as summarized in Florin, of the family were sampled in several other studies using nuclear 1963; Miller, 1977; Farjón, 2005), which is very helpful for estimat- genes (Chaw et al., 1997; Stefanovic et al., 1998; Kusumi et al., ing the divergence times of different lineages within the family. 2002; Rydin et al., 2002). In addition, the published cpDNA phylog- In the present study, we use the two nuclear genes LFY and NLY, enies comprise only 12–22 genera of Cupressaceae s.l. (Gadek and coupled with the chloroplast matK and mitochondrial rps3 genes, Quinn, 1993; Brunsfeld et al., 1994; Tsumura et al., 1995; Kusumi to reconstruct the phylogeny of Cupressaceae s.l. based on a com- et al., 2000; Quinn et al., 2002) except that 31 genera were sampled plete sampling of its 32 genera. Then, we discuss the evolution of by Gadek et al. (2000), and the intergeneric relationships, especially LFY and NLY in gymnosperms, and possible hybrid origins of Cupres- within Cupressaceae s.s., were poorly resolved in the rbcL gene trees sus, Fitzroya and Sequoia. In addition, the biogeographical history of (Gadek and Quinn, 1993; Brunsfeld et al., 1994; Gadek et al., 2000). Cupressaceae s.l., in particular Cupressaceae s.s. in the Southern In the study of Gadek et al. (2000), five genera occurring in the Hemisphere, is investigated with the help of molecular dating, the Southern Hemisphere (Actinostrobus, Austrocedrus, Fitzroya, Pilgero- fossil record and geological evidence for the break-up of Gondwana. dendron and Papuacedrus) and two genera in the Northern Hemi- sphere [Cupressus s.s. and Xanthocyparis, a new genus from 2.
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