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Phylotranscriptomic analysis of the origin and early diversification of land plants

Wickett, N. J., S. Mirarab, N. Nguyen, T. Warnow, E. Carpenter, N. Matasci, S. Ayyampalayam, M. S. Barker, J. G. Burleigh, M. A. Gitzendanner, B. R. Ruhfel, E. Wafula, J. P. Der, S. W. Graham, S. Mathews, M. Melkonian, D. E. Soltis, P. S. Soltis, N. W. Miles, C. J. Rothfels, L. Pokorny, A. J. Shaw, L. DeGironimo, D. W. Stevenson, B. Surek, J. C. Villarreal, B. Roure, H. Philippe, C. W. dePamphilis, T. Chen, M. K. Deyholos, R. S. Baucom, T. M. Kutchan, M. M. Augustin, J. Wang, Y. Zhang, Z. Tian, Z. Yan, X. Wu, X. Sun, G. K.-S. Wong, and J. Leebens-Mack. 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. PNAS 111:E4859–E4868.

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.

Abstract

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 a widely accepted view of early land plant evolution, and suggests that phylogenetic hypotheses used to understand the evolution of fundamental plant traits should be reevaluated.

Related to this article is the following data article:

Matasci, N., L.-H. Hung, Z. Yan, E. J. Carpenter, N. J. Wickett, S. Mirarab, N. Nguyen, T. Warnow, S. Ayyampalayam, M. Barker, J. G. Burleigh, M. A. Gitzendanner, E. Wafula, J. P. Der, C. W. dePamphilis, B. Roure, H. Philippe, B. R. Ruhfel, N. W. Miles, S. W. Graham, S. Mathews, B. Surek, M. Melkonian, D. E. Soltis, P. S. Soltis, C. Rothfels, L. Pokorny, J. A. Shaw, L. DeGironimo, D. W. Stevenson, J. C. Villarreal, T. Chen, T. M. Kutchan, M. Rolf, R. S. Baucom, M. K. Deyholos, R. Samudrala, Z. Tian, X. Wu, X. Sun, Y. Zhang, J. Wang, J. Leebens-Mack, and G. K.-S. Wong. 2014. Data access for the 1,000 Plants (1KP) project. GigaScience 3:17.

Abstract

The 1,000 plants (1KP) project is an international multi-disciplinary consortium that has generated transcriptome data from over 1,000 plant species, with exemplars for all of the major lineages across the Viridiplantae (green plants) clade. Here, we describe how to access the data used in a phylogenomics analysis of the first 85 species, and how to visualize our gene and species trees. Users can develop computational pipelines to analyse these data, in conjunction with data of their own that they can upload. Computationally estimated protein-protein interactions and biochemical pathways can be visualized at another site. Finally, we comment on our future plans and how they fit within this scalable system for the dissemination, visualization, and analysis of large multi-species data sets.