Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Susan H Brawley; Nicolas A Blouin; Elizabeth Ficko-Blean; Glen L Wheeler; Martin Lohr; Holly V Goodson; Jerry W Jenkins; Crysten E Blaby-Haas; Katherine E Helliwell; Cheong Xin Chan; Tara N Marriage; Debashish Bhattacharya; Anita S Klein; Yacine Badis; Juliet Brodie; Yuanyu Cao; Jonas Collén; Simon M Dittami; Claire M M Gachon; Beverley R Green; Steven J Karpowicz; Jay W Kim; Ulrich Johan Kudahl; Senjie Lin; Gurvan Michel; Maria Mittag; Bradley J S C Olson; Jasmyn L Pangilinan; Yi Peng; Huan Qiu; Shengqiang Shu; John T Singer; Alison G Smith; Brittany N Sprecher; Volker Wagner; Wenfei Wang; Zhi-Yong Wang; Juying Yan; Charles Yarish; Simone Zäuner-Riek; Yunyun Zhuang; Yong Zou; Erika A Lindquist; Jane Grimwood; Kerrie W Barry; Daniel S Rokhsar; Jeremy Schmutz; John W Stiller; Arthur R Grossman; Simon E Prochnik; Brookhaven National Lab. (BNL), Upton, NY (United States)

doi:10.1073/pnas.1703088114

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Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

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Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Susan H Brawley, Nicolas A Blouin, Elizabeth Ficko-Blean, Glen L Wheeler, Martin Lohr, Holly V Goodson, Jerry W Jenkins, Crysten E Blaby-Haas, Katherine E Helliwell, Cheong Xin Chan, …

Proceedings of the National Academy of Sciences - PNAS, Vol.114(31), pp.E6361-E6370

08/01/2017

DOI: https://doi.org/10.1073/pnas.1703088114

PMCID: PMC5547612

PMID: 28716924

Abstract

Actins - genetics

Calcium Signaling - genetics

Cell Cycle - genetics

Cell Wall - genetics

Cell Wall - metabolism

Chromatin - genetics

Cytoskeleton - genetics

Evolution, Molecular

Genome, Plant - genetics

Kinesin - genetics

Phylogeny

Porphyra - cytology

Porphyra - genetics

(laver) belongs to an ancient group of red algae (Bangiophyceae), is harvested for human food, and thrives in the harsh conditions of the upper intertidal zone. Here we present the 87.7-Mbp haploid genome (65.8% G + C content, 13,125 gene loci) and elucidate traits that inform our understanding of the biology of red algae as one of the few multicellular eukaryotic lineages. Novel features of the genome shared by other red algae relate to the cytoskeleton, calcium signaling, the cell cycle, and stress-tolerance mechanisms including photoprotection. Cytoskeletal motor proteins in are restricted to a small set of kinesins that appear to be the only universal cytoskeletal motors within the red algae. Dynein motors are absent, and most red algae, including , lack myosin. This surprisingly minimal cytoskeleton offers a potential explanation for why red algal cells and multicellular structures are more limited in size than in most multicellular lineages. Additional discoveries further relating to the stress tolerance of bangiophytes include ancestral enzymes for sulfation of the hydrophilic galactan-rich cell wall, evidence for mannan synthesis that originated before the divergence of green and red algae, and a high capacity for nutrient uptake. Our analyses provide a comprehensive understanding of the red algae, which are both commercially important and have played a major role in the evolution of other algal groups through secondary endosymbioses.

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Title: Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)
Creators: Susan H Brawley - School of Marine Sciences, University of Maine, Orono, ME 04469; Brawley@maine.edu
Nicolas A Blouin - Department of Molecular Biology, University of Wyoming, Laramie, WY 82071
Elizabeth Ficko-Blean - Sorbonne Universités, Université Pierre and Marie Curie Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, 29688 Roscoff, France
Glen L Wheeler - Marine Biological Association of the United Kingdom, Plymouth, PL1 2PB, United Kingdom
Martin Lohr - Institut für Molekulare Physiologie, Pflanzenbiochemie, Johannes Gutenberg-Universität Mainz, 55128 Mainz, Germany
Holly V Goodson - Department of Chemistry & Biochemistry, University of Notre Dame, South Bend, IN 46556
Jerry W Jenkins - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Crysten E Blaby-Haas - Biology Department, Brookhaven National Laboratory, Upton, NY 11973
Katherine E Helliwell - Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
Cheong Xin Chan - School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, QLD 4072, Australia
Tara N Marriage - Division of Biology, Kansas State University, Manhattan, KS 66506
Debashish Bhattacharya - Department of Ecology, Evolution & Natural Resources, Rutgers University, New Brunswick, NJ 08901
Anita S Klein - Department of Biological Sciences, University of New Hampshire, Durham, NH 03824
Yacine Badis - Scottish Association for Marine Sciences, Scottish Marine Institute, Oban PA37 1QA, United Kingdom
Juliet Brodie - Natural History Museum, Department of Life Sciences, London SW7 5BD, United Kingdom
Yuanyu Cao - Department of Biological Sciences, University of New Hampshire, Durham, NH 03824
Jonas Collén - Sorbonne Universités, Université Pierre and Marie Curie Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, 29688 Roscoff, France
Simon M Dittami - Sorbonne Universités, Université Pierre and Marie Curie Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, 29688 Roscoff, France
Claire M M Gachon - Scottish Association for Marine Sciences, Scottish Marine Institute, Oban PA37 1QA, United Kingdom
Beverley R Green - Department of Botany, University of British Columbia, Vancouver BC, Canada V6T 1Z4
Steven J Karpowicz - Tau Biosciences LLC, Edmond, OK 73003
Jay W Kim - Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064
Ulrich Johan Kudahl - Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
Senjie Lin - Department of Marine Sciences, University of Connecticut, Groton, CT 06340
Gurvan Michel - Sorbonne Universités, Université Pierre and Marie Curie Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, 29688 Roscoff, France
Maria Mittag - Institut für Allgemeine Botanik und Pflanzenphysiologie, Friedrich-Schiller-Universität Jena, 07743 Jena, Germany
Bradley J S C Olson - Division of Biology, Kansas State University, Manhattan, KS 66506
Jasmyn L Pangilinan - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Yi Peng - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Huan Qiu - Department of Ecology, Evolution & Natural Resources, Rutgers University, New Brunswick, NJ 08901
Shengqiang Shu - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
John T Singer - Department of Molecular & Biomedical Science, University of Maine, Orono, ME 04469
Alison G Smith - Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom
Brittany N Sprecher - Department of Marine Sciences, University of Connecticut, Groton, CT 06340
Volker Wagner - Institut für Allgemeine Botanik und Pflanzenphysiologie, Friedrich-Schiller-Universität Jena, 07743 Jena, Germany
Wenfei Wang - Basic Forestry and Proteomics Research Center, HIST, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Zhi-Yong Wang - Department of Plant Science, Carnegie Institution for Science, Stanford, CA 94305
Juying Yan - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Charles Yarish - Department of Ecology & Evolutionary Biology, University of Connecticut, Stamford, CT 06901
Simone Zäuner-Riek - Institute of Molecular Physiology and Biotechnology, University of Bonn, 53115 Bonn, Germany
Yunyun Zhuang - Department of Marine Sciences, University of Connecticut, Groton, CT 06340
Yong Zou - Institut für Allgemeine Botanik und Pflanzenphysiologie, Friedrich-Schiller-Universität Jena, 07743 Jena, Germany
Erika A Lindquist - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Jane Grimwood - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Kerrie W Barry - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Daniel S Rokhsar - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Jeremy Schmutz - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
John W Stiller - Department of Biology, East Carolina University, Greenville, NC 27858
Arthur R Grossman - Department of Plant Science, Carnegie Institution for Science, Stanford, CA 94305
Simon E Prochnik - Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598
Brookhaven National Lab. (BNL), Upton, NY (United States)
Publication Details: Proceedings of the National Academy of Sciences - PNAS, Vol.114(31), pp.E6361-E6370
Date published: 08/01/2017
Grant note: P20 GM103418 / NIGMS NIH HHS P20 GM103638 / NIGMS NIH HHS BB/1013164/1 / Biotechnology and Biological Sciences Research Council
Academic Unit: Biochemistry and Microbiology (SEBS)
Language: English
Resource Type: Journal article
Identifiers: 991031665495904646