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FULLTEXT01.Pdf http://www.diva-portal.org This is the published version of a paper published in Genome Biology and Evolution. Citation for the original published paper (version of record): Li, Z., De La Torre, A R., Sterck, L., Cánovas, F M., Avila, C. et al. (2017) Single-Copy Genes as Molecular Markers for Phylogenomic Studies in Seed Plants. Genome Biology and Evolution, 9(5): 1130-1147 https://doi.org/10.1093/gbe/evx070 Access to the published version may require subscription. N.B. When citing this work, cite the original published paper. Permanent link to this version: http://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-140245 GBE Single-Copy Genes as Molecular Markers for Phylogenomic Studies in Seed Plants Zhen Li1,2,3,AmandaR.DeLaTorre4,5, Lieven Sterck1,2,3,FranciscoM.Canovas 6, Concepcion Avila6, Irene Merino7,Jose´ Antonio Cabezas8,Marıa Teresa Cervera8,Par€ K. Ingvarsson4,7,and Yves Van de Peer1,2,3,9,* 1Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium 2Center for Plant Systems Biology, VIB, Ghent, Belgium 3Bioinformatics Institute Ghent, Ghent, Belgium 4Department of Ecology and Environmental Science, Umea˚University,Umea˚ , Sweden 5Department of Plant Sciences, University of California-Davis, Davis, CA 6Departamento de Biologıa Molecular y Bioquımica, Facultad de Ciencias, Universidad de Malaga, Campus Universitario de Teatinos s/n, Malaga, Spain 7Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden 8INIA, Center Forest Research (CIFOR), Madrid, Spain 9Genomics Research Institute, University of Pretoria, Hatfield Campus, Pretoria, South Africa *Corresponding author: E-mail: [email protected]. Accepted: April 26, 2017 Abstract Phylogenetic relationships among seed plant taxa, especially within the gymnosperms, remain contested. In contrast to angio- sperms, for which several genomic, transcriptomic and phylogenetic resources are available, there are few, if any, molecular markers that allow broad comparisons among gymnosperm species. With few gymnosperm genomes available, recently obtained tran- scriptomes in gymnosperms are a great addition to identifying single-copy gene families as molecular markers for phylogenomic analysis in seed plants. Taking advantage of an increasing number of available genomes and transcriptomes, we identified single- copy genes in a broad collection of seed plants and used these to infer phylogenetic relationships between major seed plant taxa. This study aims at extending the current phylogenetic toolkit for seed plants, assessing its ability for resolving seed plant phylogeny, and discussing potential factors affecting phylogenetic reconstruction. In total, we identified 3,072 single-copy genes in 31 gym- nosperms and 2,156 single-copy genes in 34 angiosperms. All studied seed plants shared 1,469 single-copy genes, which are generally involved in functions like DNA metabolism, cell cycle, and photosynthesis. A selected set of 106 single-copy genes provided good resolution for the seed plant phylogeny except for gnetophytes. Although some of our analyses support a sister relationship between gnetophytes and other gymnosperms, phylogenetic trees from concatenated alignments without 3rd codon positions and amino acid alignments under the CAT þ GTR model, support gnetophytes as a sister group to Pinaceae. Our phylogenomic analyses demonstrate that, in general, single-copy genes can uncover both recent and deep divergences of seed plant phylogeny. Key words: single-copy genes, gymnosperms, angiosperms, seed plants, phylogenomics. Introduction Gnetidae, and Pinidae (Chase and Reveal 2009). Both mor- Seed plants originated 370 Ma, and probably comprise phological and molecular studies have clearly shown that an- 260,000 to 310,000 extant species (Fiz-Palacios et al. 2011; giosperms and gymnosperms are two monophyletic groups Christenhusz and Byng 2016). Current seed plants consist of (Chaw et al. 2000; Wang and Ran 2014), but the relationship angiosperms (flowering plants) and gymnosperms, the latter between the different clades in gymnosperms is less clear of which are further subdivided into Cycadidae, Ginkgoidae, than in angiosperms (Haston et al. 2009), despite great efforts ß The Author(s) 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 1130 Genome Biol. Evol. 9(4):1130–1147. doi:10.1093/gbe/evx070 Advance Access publication April 27, 2017 Downloaded from https://academic.oup.com/gbe/article-abstract/9/5/1130/3770952/Single-Copy-Genes-as-Molecular-Markers-for by Umea University Library user on 19 October 2017 Single-Copy Genes as Molecular Markers for Phylogenomic Studies in Seed Plants GBE in resolving the phylogeny with diverse sets of molecular genes is more likely to reflect true species relationships and markers (Zhong et al. 2010; Lee et al. 2011; Xi et al. 2013; may solve incongruences between organelle genes (Zhang Lu et al. 2014). Particularly, the exact phylogenetic position of et al. 2012; Lu et al. 2014; Zeng et al. 2014). gnetophytes, a morphologically unique clade with accelerated Although widely applied to angiosperms (Wu et al. 2006; molecular evolution rates, remains elusive (Wang and Ran Zhang et al. 2012; Zeng et al. 2014), only a few single-copy 2014). Morphological studies, historically, agree that gneto- genes have been used to resolve gymnosperm relationships (Xi phytes are a sister group of angiosperms (anthophyte hypoth- et al. 2013; Lu et al. 2014; Salas-Leiva et al. 2014). In addition, esis) (reviewed in Doyle 1998), because of obviously similar current single-copy genes in gymnosperms were identified on characteristics, such as, the existence of vessel elements and the basis of those in angiosperms (Salas-Leiva et al. 2014; the simple, unisexual, flower-like reproductive organs. Wickett et al. 2014). Whole genome sequencing can facilitate However, this hypothesis was later questioned on the basis the identification of single-copy genes (De Smet et al. 2013; Li of a flood of molecular data, with some providing support for et al. 2016) but the huge genome sizes of gymnosperms (20– gnetophytes as sister to the other seed plants (Gnetales— 30 Gb) have greatly complicated their de novo sequencing (De other seed plant hypothesis) (Burleigh and Mathews 2004) La Torre et al. 2014). As a consequence, only a few gymno- and others providing support for a sister group relationship sperm species have been sequenced so far (Birol et al. 2013; with the other gymnosperms (Gnetales—other gymnosperms Nystedtetal.2013; Neale et al. 2014; Warren et al. 2015). hypothesis) (Cibrian-Jaramillo et al. 2010; Lee et al. 2011). Still However, since single-copy genes are often more broadly ex- others provided support, usually based on mitochondrial or pressed and at higher levels than nonsingle-copy genes (De plastid genes, for gnetophytes as a sister group to conifers Smet et al. 2013; De La Torre et al. 2015), single-copy genes (Gnetifer hypothesis) (Ran et al. 2010), to one clade of coni- can be relatively easily detected by transcriptome sequencing, fers, that is cupressophytes (Gnecup hypothesis) (Xi et al. thereby simplifying the procedure to identify suitable molecu- 2013; Lu et al. 2014), or to the other conifer clade, that is lar markers. In this study, using previously and newly devel- Pinaceae (Gnepine hypothesis) (Zhong et al. 2010, 2011; Wu oped genomic and transcriptomic data in 31 gymnosperms et al. 2011; Burleigh et al. 2012). Also different approaches and 34 angiosperms, we identified single-copy gene families and data treatments yielded different phylogenetic place- to increase the number of phylogenetic markers shared be- ments of gnetophytes within the gymnosperms (Zhong tween gymnosperms (and between gymnosperms and angio- et al. 2010, 2011; Wickett et al. 2014). Besides the contro- sperms) that could be used for phylogenetic and comparative versial systematic position of gnetophytes, Ginkgo,whichisa studies in seed plants (De La Torre et al. 2017). monotypic genus of an ancient lineage that originated at least 270 Ma, also has an ambiguous placement among the gym- Materials and Methods nosperms (Wang and Ran 2014). Some studies suggest Ginkgo as a sister group to a clade comprising conifers and Plant Material and cDNA Libraries Construction gnetophytes (Mathews 2009; Ran et al. 2010; Lu et al. 2014); Pinus pinaster seeds from the Oria provenance (Southern whereas several recent phylogenomic analyses support a sister Spain) were germinated and grown at 20/24 C with a 16/ relationship between Ginkgo and cycads (Cibrian-Jaramillo 8 h photoperiod. Germinating seeds were watered twice a et al. 2010; Wu et al. 2013; Xi et al. 2013; Wickettetal. week with distilled water. One-month-old seedlings were 2014). used for cryosectioning and 0.5-cm tissue sections were pro- Increased species sampling could help resolving the evolu- cessed for laser capture microdissection (Canas~ et al. 2014). tionary relationships within seed plants (Zwickl and Hillis Tissues of P. pinaster were collected from cortex of hypocotyl, 2002), but molecular markers for gymnosperms are still lack- cortex
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