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      Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics.

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          Abstract

          Dinoflagellates are key species in marine environments, but they remain poorly understood in part because of their large, complex genomes, unique molecular biology, and unresolved in-group relationships. We created a taxonomically representative dataset of dinoflagellate transcriptomes and used this to infer a strongly supported phylogeny to map major morphological and molecular transitions in dinoflagellate evolution. Our results show an early-branching position of Noctiluca, monophyly of thecate (plate-bearing) dinoflagellates, and paraphyly of athecate ones. This represents unambiguous phylogenetic evidence for a single origin of the group's cellulosic theca, which we show coincided with a radiation of cellulases implicated in cell division. By integrating dinoflagellate molecular, fossil, and biogeochemical evidence, we propose a revised model for the evolution of thecal tabulations and suggest that the late acquisition of dinosterol in the group is inconsistent with dinoflagellates being the source of this biomarker in pre-Mesozoic strata. Three distantly related, fundamentally nonphotosynthetic dinoflagellates, Noctiluca, Oxyrrhis, and Dinophysis, contain cryptic plastidial metabolisms and lack alternative cytosolic pathways, suggesting that all free-living dinoflagellates are metabolically dependent on plastids. This finding led us to propose general mechanisms of dependency on plastid organelles in eukaryotes that have lost photosynthesis; it also suggests that the evolutionary origin of bioluminescence in nonphotosynthetic dinoflagellates may be linked to plastidic tetrapyrrole biosynthesis. Finally, we use our phylogenetic framework to show that dinoflagellate nuclei have recruited DNA-binding proteins in three distinct evolutionary waves, which included two independent acquisitions of bacterial histone-like proteins.

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          Author and article information

          Journal
          Proc. Natl. Acad. Sci. U.S.A.
          Proceedings of the National Academy of Sciences of the United States of America
          Proceedings of the National Academy of Sciences
          1091-6490
          0027-8424
          Jan 10 2017
          : 114
          : 2
          Affiliations
          [1 ] Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom; janjan.cz@gmail.com.
          [2 ] Biology Department, San Diego State University, San Diego, CA 92182.
          [3 ] Botany Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
          [4 ] Program in Integrated Microbial Diversity, Canadian Institute for Advanced Research, Toronto, ON M5G 1Z8, Canada.
          [5 ] Zoology Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
          [6 ] Institute for Marine and Environmental Technology, University of Maryland Center for Environmental Sciences, Baltimore, MD 21202.
          [7 ] Centre for Chromosome Biology, School of Natural Sciences, National University of Ireland, Galway, Ireland.
          [8 ] Shannon Point Marine Center, Western Washington University, Anacortes, WA 98221.
          [9 ] Department of Cell Biology and Molecular Genetics and Agricultural Experiment Station, University of Maryland, College Park, MD 20742.
          [10 ] Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, United Kingdom.
          [11 ] Bedford Institute of Oceanography, Geological Survey of Canada (Atlantic), Dartmouth, NS B2Y 4A2, Canada.
          Article
          1614842114
          10.1073/pnas.1614842114
          5240707
          28028238

          theca, plastids, phylogeny, dinosterol, dinoflagellates

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