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Phylotranscriptomic Analysis of the Origin and Early Diversification Of Phylotranscriptomic analysis of the origin and early PNAS PLUS diversification of land plants Norman J. Wicketta,b,1,2, Siavash Mirarabc,1, Nam Nguyenc, Tandy Warnowc, Eric Carpenterd, Naim Matascie,f, Saravanaraj Ayyampalayamg, Michael S. Barkerf, J. Gordon Burleighh, Matthew A. Gitzendannerh,i, Brad R. Ruhfelh,j,k, Eric Wafulal, Joshua P. Derl, Sean W. Grahamm, Sarah Mathewsn, Michael Melkoniano, Douglas E. Soltish,i,k, Pamela S. Soltish,i,k, Nicholas W. Milesk, Carl J. Rothfelsp,q, Lisa Pokornyp,r, A. Jonathan Shawp, Lisa DeGironimos, Dennis W. Stevensons, Barbara Sureko, Juan Carlos Villarrealt,BéatriceRoureu, Hervé Philippeu,v, Claude W. dePamphilisl, Tao Chenw, Michael K. Deyholosd, Regina S. Baucomx, Toni M. Kutchany, Megan M. Augustiny,JunWangz, Yong Zhangv, Zhijian Tianz,ZhixiangYanz,XiaoleiWuz,XiaoSunz, Gane Ka-Shu Wongd,z,aa,2, and James Leebens-Mackg,2 aChicago Botanic Garden, Glencoe, IL 60022; bProgram in Biological Sciences, Northwestern University, Evanston, IL 60208; cDepartment of Computer Science, University of Texas, Austin, TX 78712; dDepartment of Biological Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E9; eiPlant Collaborative, Tucson, AZ 85721; fDepartment of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721; gDepartment of Plant Biology, University of Georgia, Athens, GA 30602; hDepartment of Biology and iGenetics Institute, University of Florida, Gainesville, FL 32611; jDepartment of Biological Sciences, Eastern Kentucky University, Richmond, KY 40475; kFlorida Museum of Natural History, Gainesville, FL 32611; lDepartment of Biology, Pennsylvania State University, University Park, PA 16803; mDepartment of Botany and qDepartment of Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4; nArnold Arboretum of Harvard University, Cambridge, MA 02138; oBotanical Institute, Universität zu Köln, Cologne D-50674, Germany; pDepartment of Biology, Duke University, Durham, NC 27708; rDepartment of Biodiversity and Conservation, Real Jardín Botánico-Consejo Superior de Investigaciones Cientificas, 28014 Madrid, Spain; sNew York Botanical Garden, Bronx, NY 10458; tDepartment fur Biologie, Systematische Botanik und Mykologie, Ludwig-Maximilians-Universitat, 80638 Munich, Germany; uDépartement de Biochimie, Centre Robert-Cedergren, Université de Montréal, Succursale Centre-Ville, Montreal, QC, Canada H3C 3J7; vCNRS, Station d’ Ecologie Expérimentale du CNRS, Moulis, 09200, France; wShenzhen Fairy Lake Botanical Garden, The Chinese Academy of Sciences, Shenzhen, Guangdong 518004, China; xDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109; yDonald Danforth Plant Science Center, St. Louis, MO 63132; zBGI-Shenzhen, Bei shan Industrial Zone, Yantian District, Shenzhen 518083, China; and aaDepartment of Medicine, University of Alberta, Edmonton, AB, Canada T6G 2E1 Edited by Paul O. Lewis, University of Connecticut, Storrs, CT, and accepted by the Editorial Board September 29, 2014 (received for review December 23, 2013) Reconstructing the origin and evolution of land plants and their algal relatives is a fundamental problem in plant phylogenetics, and is essential for understanding how critical adaptations arose, in- Significance cluding the embryo, vascular tissue, seeds, and flowers. Despite advances in molecular systematics, some hypotheses of relationships Early branching events in the diversification of land plants and remain weakly resolved. Inferring deep phylogenies with bouts of closely related algal lineages remain fundamental and un- rapid diversification can be problematic; however, genome-scale resolved questions in plant evolutionary biology. Accurate data should significantly increase the number of informative charac- reconstructions of these relationships are critical for testing hy- ters for analyses. Recent phylogenomic reconstructions focused on potheses of character evolution: for example, the origins of the the major divergences of plants have resulted in promising but in- embryo, vascular tissue, seeds, and flowers. We investigated consistent results. One limitation is sparse taxon sampling, likely relationships among streptophyte algae and land plants using resulting from the difficulty and cost of data generation. To address the largest set of nuclear genes that has been applied to this this limitation, transcriptome data for 92 streptophyte taxa were problem to date. Hypothesized relationships were rigorously generated and analyzed along with 11 published plant genome tested through a series of analyses to assess systematic errors in sequences. Phylogenetic reconstructions were conducted using up phylogenetic inference caused by sampling artifacts and model to 852 nuclear genes and 1,701,170 aligned sites. Sixty-nine analyses misspecification. Results support some generally accepted phy- were performed to test the robustness of phylogenetic inferences to logenetic hypotheses, while rejecting others. This work provides permutations of the data matrix or to phylogenetic method, including a new framework for studies of land plant evolution. supermatrix, supertree, and coalescent-based approaches, maximum- likelihood and Bayesian methods, partitioned and unpartitioned ana- Author contributions: N.J.W., S. Mirarab, T.W., S.W.G., M.M., D.E.S., P.S.S., D.W.S., M.K.D., lyses, and amino acid versus DNA alignments. Among other J.W., G.K.-S.W., and J.L.-M. designed research; N.J.W., S. Mirarab, N.N., T.W., E.C., N.M., S.A., results, we find robust support for a sister-group relationship M.S.B., J.G.B., M.A.G., B.R.R., E.W., J.P.D., S.W.G., S. Mathews, M.M., D.E.S., P.S.S., N.W.M., between land plants and one group of streptophyte green al- C.J.R., L.P., A.J.S., L.D., D.W.S., B.S., J.C.V., B.R., H.P., C.W.d., T.C., M.K.D., M.M.A., J.W., Y.Z., Z.T., Z.Y., X.W., X.S., G.K.-S.W., and J.L.-M. performed research; S. Mirarab, N.N., T.W., N.M., gae, the Zygnematophyceae. Strong and robust support for a S.A., M.S.B., J.G.B., M.A.G., E.W., J.P.D., S.W.G., S. Mathews, M.M., D.E.S., P.S.S., N.W.M., C.J.R., clade comprising liverworts and mosses is inconsistent with a L.P., A.J.S., L.D., D.W.S., B.S., J.C.V., H.P., C.W.d., T.C., M.K.D., R.S.B., T.M.K., M.M.A., J.W., Y.Z., widely accepted view of early land plant evolution, and suggests G.K.-S.W., and J.L.-M. contributed new reagents/analytic tools; N.J.W., S. Mirarab, N.N., E.C., that phylogenetic hypotheses used to understand the evolution of N.M., S.A., M.S.B., J.G.B., M.A.G., B.R.R., E.W., B.R., H.P., and J.L.-M. analyzed data; N.J.W., S. Mirarab, T.W., S.W.G., M.M., D.E.S., D.W.S., H.P., G.K.-S.W., and J.L.-M. wrote the paper; fundamental plant traits should be reevaluated. and N.M. archived data. The authors declare no conflict of interest. land plants | Streptophyta | phylogeny | phylogenomics | transcriptome This article is a PNAS Direct Submission. P.O.L. is a guest editor invited by the Editorial Board. EVOLUTION he origin of embryophytes (land plants) in the Ordovician Freely available online through the PNAS open access option. – Tperiod roughly 480 Mya (1 4) marks one of the most im- Data deposition: The sequences reported in this paper have been deposited in the portant events in the evolution of life on Earth. The early evo- iplant datastore database, mirrors.iplantcollaborative.org/onekp_pilot,andtheNa- tional Center for Biotechnology Information Sequence Read Archive, www.ncbi.nlm. lution of embryophytes in terrestrial environments was facilitated nih.gov/sra [accession no. PRJEB4921 (ERP004258)]. by numerous innovations, including parental protection for the 1N.J.W. and S. Mirarab contributed equally to this work. developing embryo, sperm and egg production in multicellular 2To whom correspondence may be addressed. Email: [email protected], protective structures, and an alternation of phases (often referred to [email protected], or [email protected]. as generations) in which a diploid sporophytic life history stage This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. gives rise to a multicellular haploid gametophytic phase. With 1073/pnas.1323926111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1323926111 PNAS | Published online October 29, 2014 | E4859–E4868 Downloaded by guest on September 26, 2021 these and subsequent innovations, embryophytes diversified and ancestor and were subsequently lost in most lineages within the lineage ultimately came to dominate and significantly alter the Zygnematophyceae. terrestrial environments (1–4). The origin of embryophytes was Early events in the diversification of embryophytes gave rise to a pivotal event in evolutionary history that spawned the tremen- mosses, liverworts, and hornworts (collectively bryophytes) (25, dous diversity of morphological, physiological, reproductive, and 39–44). Virtually every possible hypothesis of branching order ecological traits we see in both the extant and fossil terrestrial involving these groups has been proposed and supported by flora. Moreover, colonization of land by plants greatly changed the various data. Resolving this uncertainty has implications for global carbon cycle, drawing down atmospheric CO2 concen- understanding evolution of the heteromorphic alternation of life trations (5) and forming the foundation of the vast majority of history phases shared by all embryophytes. Whereas all bryo- terrestrial ecosystems. phyte lineages share a life history in which the haploid phase Subsequent innovations in embryophyte evolution greatly ex- (gametophyte) is dominant, with a diploid phase (sporophyte) panded the diversity of the terrestrial flora. The origin of vascular that is dependent on the maternal gametophyte, vascular plants tissue and antidesiccation features in tracheophytes (vascular instead have a dominant sporophytic phase. A grade of bryo- plants) established a more efficient system for the transport and phytes would support the hypothesis that the gametophyte- retention of water, photosynthate, and other nutrients, as well as dominant life cycle is plesiomorphic in embryophytes (45).
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