The Evolutionary Root of Flowering Plants

Goremykin, Vadim V.; Nikiforova, Svetlana V.; Biggs, Patrick J.; Zhong, Bojian; Delange, Peter; Martin, William; Woetzel, Stefan; Atherton, Robin A.; McLenachan, Patricia A.; Lockhart, Peter J.

doi:10.1093/sysbio/sys070

Cited by 72 publications

(121 citation statements)

References 62 publications

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“…We investigated whether previous studies supporting Ctenophora-sister were conducted using adequately fitting substitution models. Using three exemplar datasets, which we call Ryan-Choano, Moroz-3D, and Whelan-6-Choano (details are provided below and in Methods), we compared the relative fit of site-homogeneous and siteheterogeneous models using Bayesian cross-validation (36, 37), a routine statistical technique used to evaluate the predictive performance of a probabilistic model, which has been commonly used in the context of phylogenetics (23,24,(38)(39)(40)(41). Using 10 cross-validation replicates, we found that in all cases, site-heterogeneous models fit these data significantly better than the site-homogeneous models that previous studies mostly relied upon ( Table 1).…”

Section: Resultsmentioning

confidence: 99%

Genomic data do not support comb jellies as the sister group to all other animals

Pisani

Pett

Dohrmann

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

300

336

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Understanding how complex traits, such as epithelia, nervous systems, muscles, or guts, originated depends on a well-supported hypothesis about the phylogenetic relationships among major animal lineages. Traditionally, sponges (Porifera) have been interpreted as the sister group to the remaining animals, a hypothesis consistent with the conventional view that the last common animal ancestor was relatively simple and more complex body plans arose later in evolution. However, this premise has recently been challenged by analyses of the genomes of comb jellies (Ctenophora), which, instead, found ctenophores as the sister group to the remaining animals (the "Ctenophora-sister" hypothesis). Because ctenophores are morphologically complex predators with true epithelia, nervous systems, muscles, and guts, this scenario implies these traits were either present in the last common ancestor of all animals and were lost secondarily in sponges and placozoans (Trichoplax) or, alternatively, evolved convergently in comb jellies. Here, we analyze representative datasets from recent studies supporting Ctenophora-sister, including genome-scale alignments of concatenated protein sequences, as well as a genomic gene content dataset. We found no support for Ctenophora-sister and conclude it is an artifact resulting from inadequate methodology, especially the use of simplistic evolutionary models and inappropriate choice of species to root the metazoan tree. Our results reinforce a traditional scenario for the evolution of complexity in animals, and indicate that inferences about the evolution of Metazoa based on the Ctenophora-sister hypothesis are not supported by the currently available data.Metazoa | Ctenophora | Porifera | phylogenomics | evolution R esolving the phylogenetic relationships close to the root of the animal tree of life, which encompass the phyla Porifera (sponges), Cnidaria (jellyfish, corals, and their allies), Ctenophora (comb jellies), Placozoa (the "plate animals" of the genus Trichoplax), and Bilateria (the group containing all remaining phyla), is fundamental to understanding early animal evolution and the emergence of complex traits [reviewed by Dohrmann and Wörheide (1)]. Traditionally, sponges have been recognized as the sister group to the remaining animals (the "Porifera-sister" hypothesis). Under this scenario, true epithelia (with belt desmosomes connecting neighboring cells) and extracellular digestion are conventionally thought to have been primitively absent in sponges, having evolved in the common ancestor of Placozoa, Ctenophora, Cnidaria, and Bilateria. Within this group, gap junctions between neighboring cells, ectodermal and endodermal germ layers, sensory cells, nerve cells, and muscle cells evolved only once in the common ancestor of Ctenophora, Cnidaria, and Bilateria. Thus, Porifera-sister is consistent with the view that the last common ancestor of the animals was relatively simple and more complex body plans evolved after sponges had separated from the other animal lineages. However, a s...

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Section: Resultsmentioning

confidence: 99%

Genomic data do not support comb jellies as the sister group to all other animals

Pisani

Pett

Dohrmann

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

300

336

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“…2). This internal branch has been consistently resolved and highly supported by phylogenetic analyses, irrespective of whether they support Amborellales alone or the clade of (Amborellales, Nymphaeales) as sister to the remaining extant angiosperms (e.g., Soltis et al, 2011;Goremykin et al, 2013;Ruhfel et al, 2014;Wickett et al, 2014). So, the debate about the relationship of Amborella and Nuphar relative to each other is strictly in the context of a rooted tree-the alternatives cannot be distinguished in an unrooted context.…”

Section: Potential Bias Caused By Mis-rooting Angiospermsmentioning

confidence: 95%

“…Early phylogenetic analyses produced discordant inferences regarding the sister group of the remaining extant angiosperms (e.g., Magnoliales by Donoghue and Doyle [1989], Calycanthales by Loconte and Stevenson [1991], Ceratophyllaceae by Chase et al [1993], Chloranthaceae by Nixon et al [1994]), but more recent studies have consistently identified Amborellales alone (e.g., Mathews and Donoghue, 1999;Soltis et al, 2000Soltis et al, , 2011 or the clade of (Amborellales, Nymphaeales) (e.g., Barkman et al, 2000;Qiu et al, 2010;Goremykin et al, 2013) as the sister group. Wickett et al (2014) and Xi et al (2014) both addressed the question of whether Amborellales or the clade of (Amborellales, Nymphaeales) are the sister group by performing both concatenation-and coalescent-based phylogenomic analyses on independently derived sets of hundreds of nuclear gene regions (852 by Wickett et al [2014] and 310 by Xi et al [2014]).…”

Section: Et Al's (2014) Coalescent-based Study Of Early-derived Amentioning

confidence: 99%

Coalescence vs. concatenation: Sophisticated analyses vs. first principles applied to rooting the angiosperms

Simmons

Gatesy

2015

Molecular Phylogenetics and Evolution

179

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“…Since publication of a series of landmark papers that identified Amborella trichopoda, Nymphaeales, and Austrobaileyales as successive sister lineages relative to all other extant angiosperms (98)(99)(100)(101), all analyses performed with rich taxon sampling have supported A. trichopoda (7,12,14,(101)(102)(103)(104)(105) or a Nymphaeales+A. trichopoda clade (12,106,107) as sister to all other extant angiosperm lineages. All of our analyses placed A. trichopoda as sister to all other angiosperms ( Figs.…”

Section: Relationships Among Streptophytic Algal Lineages and Land Plmentioning

confidence: 99%

Phylotranscriptomic analysis of the origin and early diversification of land plants

Wickett

Mirarab

Nguyen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

1,159

1,173

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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, maximumlikelihood 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.land plants | Streptophyta | phylogeny | phylogenomics | transcriptome T he origin of embryophytes (land plants) in the Ordovician period roughly 480 Mya (1-4) marks one of the most important events in the evolution of life on Earth. The early evolution of embryophytes in terrestrial environments was facilitated by numerous innovations, including parental protection for the developing embryo, sperm and egg production in multicellular protective structures, and an alternation of phases (often referred to as generations) in which a diploid sporophytic life history stage gives rise to a multicellular haploid gametophytic phase. With 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 er...

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The Evolutionary Root of Flowering Plants

Cited by 72 publications

References 62 publications

Genomic data do not support comb jellies as the sister group to all other animals

Genomic data do not support comb jellies as the sister group to all other animals

Coalescence vs. concatenation: Sophisticated analyses vs. first principles applied to rooting the angiosperms

Phylotranscriptomic analysis of the origin and early diversification of land plants

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