Phylotranscriptomic analysis of the origin and early diversification of land plants

• Published in: Proceedings of the National Academy of Sciences - PNAS 2014-11, Vol.111 (45), p.E4859-E4868
• Main Authors: Wickett, Norman J, Mirarab, Siavash, Nguyen, Nam, Warnow, Tandy, Carpenter, Eric, Matasci, Naim, Ayyampalayam, Saravanaraj, Barker, Michael S, Burleigh, J Gordon, Gitzendanner, Matthew A, Ruhfel, Brad R, Wafula, Eric, Der, Joshua P, Graham, Sean W, Mathews, Sarah, Melkonian, Michael, Soltis, Douglas E, Soltis, Pamela S, Miles, Nicholas W, Rothfels, Carl J, Pokorny, Lisa, Shaw, A Jonathan, DeGironimo, Lisa, Stevenson, Dennis W, Surek, Barbara, Villarreal, Juan Carlos, Roure, Béatrice, Philippe, Hervé, dePamphilis, Claude W, Chen, Tao, Deyholos, Michael K, Baucom, Regina S, Kutchan, Toni M, Augustin, Megan M, Wang, Jun, Zhang, Yong, Tian, Zhijian, Yan, Zhixiang, Wu, Xiaolei, Sun, Xiao, Wong, Gane Ka-Shu, Leebens-Mack, James
• Format: Article
• Language: English
• Subjects: Algae; Biological Sciences; Botanics; DNA, Plant - genetics; DNA, Plant - metabolism; Evolution; Evolution, Molecular; Flowers & plants; Gene Expression Profiling; Genome, Plant - physiology; Life Sciences; Maximum likelihood method; Phylogenetics; Phylogeny; PNAS Plus; Quantitative Trait, Heritable; Sequence Alignment; Streptophyta - classification; Streptophyta - physiology; Transcriptome - physiology; Vegetal Biology; Zygnematophyceae
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1323926111

Significance Early branching events in the diversification of land plants and closely related algal lineages remain fundamental and unresolved questions in plant evolutionary biology. Accurate reconstructions of these relationships are critical for testing hypotheses of character evolution: for example, the origins of the embryo, vascular tissue, seeds, and flowers. We investigated relationships among streptophyte algae and land plants using the largest set of nuclear genes that has been applied to this problem to date. Hypothesized relationships were rigorously tested through a series of analyses to assess systematic errors in phylogenetic inference caused by sampling artifacts and model misspecification. Results support some generally accepted phylogenetic hypotheses, while rejecting others. This work provides a new framework for studies of land plant evolution. 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, including the embryo, vascular tissue, seeds, and flowers. Despite advances in molecular systematics, some hypotheses of relationships remain weakly resolved. Inferring deep phylogenies with bouts of rapid diversification can be problematic; however, genome-scale data should significantly increase the number of informative characters for analyses. Recent phylogenomic reconstructions focused on the major divergences of plants have resulted in promising but inconsistent results. One limitation is sparse taxon sampling, likely resulting from the difficulty and cost of data generation. To address this limitation, transcriptome data for 92 streptophyte taxa were generated and analyzed along with 11 published plant genome sequences. Phylogenetic reconstructions were conducted using up to 852 nuclear genes and 1,701,170 aligned sites. Sixty-nine analyses were performed to test the robustness of phylogenetic inferences to permutations of the data matrix or to phylogenetic method, including supermatrix, supertree, and coalescent-based approaches, maximum-likelihood and Bayesian methods, partitioned and unpartitioned analyses, and amino acid versus DNA alignments. Among other results, we find robust support for a sister-group relationship between land plants and one group of streptophyte green algae, the Zygnematophyceae. Strong and robust support for a clade comprising liverworts and mosses is inconsistent with