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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [4];  [9];  [10];  [11];  [12];  [13];  [14];  [12];  [15];  [15];  [13];  [16] more »;  [17];  [18];  [19];  [20];  [15];  [21];  [22];  [23];  [23];  [24];  [23];  [25];  [26];  [20];  [21];  [27];  [28];  [23];  [29];  [30];  [20];  [21];  [23];  [7];  [23];  [23];  [7];  [31];  [28];  [23] « less
  1. University of Maine, Orono (Maine). School of Marine Sciences
  2. University of Maine, Orono (Maine). School of Marine Sciences; Univ. of Wyoming, Laramie, WY (United States). Department of Molecular Biology
  3. Sorbonne Universites, Universite Pierre and Marie Curie Paris (France). Integrative Biology of Marine Models, Station Biologique de Roscoff
  4. Marine Biological Association of the United Kingdom, Plymouth (United Kingdom)
  5. Johannes Gutenberg-Universitat Mainz (Germany). Institute for Molecular Biology
  6. University of Notre Dame, South Bend, IN (United States). Department of Chemistry & Biochemistry
  7. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  8. Brookhaven National Lab. (BNL), Upton, NY (United States). Biology Dept.
  9. Univ. of Queensland, Brisbane (Australia). Institute for Molecular Bioscience and School of Chemistry and Molecular Biosciences
  10. Kansas State Univ., Manhattan, KS (United States). Division of Biology
  11. Rutgers Univ., New Brunswick, NJ (United States). Department of Ecology, Evolution & Natural Resources
  12. Univ. of New Hampshire, Durham, NH (United States). Department of Biological Sciences
  13. Scottish Marine Institute (United Kingdom). Scottish Association for Marine Sciences
  14. Natural History Museum, Department of Life Sciences, London (United Kingdom)
  15. Sorbonne Universites, Universite Pierre and Marie Curie Paris (France). Integrative Biology of Marine Models, Station Biologique de Roscoff
  16. University of British Columbia, Vancouver BC (Canada). Department of Botany
  17. Tau Biosciences LLC, Edmond, OK (United States)
  18. University of California, Santa Cruz, CA (United States). Department of Biomolecular Engineering
  19. University of Cambridge (United Kingdom). Department of Plant Sciences
  20. University of Connecticut, Groton, CT (United States). Department of Marine Sciences
  21. Friedrich-Schiller University, Jena (Germany). Institute of General Botany and Plant Phisiology
  22. Kansas State University, Manhattan, KS (United States). Division of Biology
  23. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  24. Rutgers University, New Brunswick, NJ (United States). Department of Ecology, Evolution & Natural Resources
  25. University of Maine, Orono, ME (United States). Department of Molecular & Biomedical Science
  26. University of Cambridge (United Kingdom). Dept. of Plant Sciences
  27. Fujian Agriculture and Forestry University, Fuzhou (China). Basic Forestry and Proteomics Research Center, HIST
  28. Carnegie Institution for Science, Stanford, CA (United States). Dept. of Plant Science
  29. University of Connecticut, Stamford, CT (United States). Department of Ecology & Evolutionary Biology
  30. University of Bonn (Germany). Institute of Molecular Physiology and Biotechnology
  31. East Carolina University, Greenville, NC (United States). Department of Biology
+ Show Author Affiliations
Porphyra umbilicalis (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 Porphyra 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 Porphyra 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 Porphyra 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 Porphyra, 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.
Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Grant/Contract Number:
AC02-05CH11231; SC0012704
OSTI ID:
1376126
Alternate ID(s):
OSTI ID: 1616054
Report Number(s):
BNL--114055-2017-JA
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 31 Vol. 114; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English

References (103)

Rhodophyta book January 2016
Growth, cell volume, and fine structure of Porphyra umbilicalis in relation to osmotic tolerance journal December 1980
A possible role for actin dots in the formation of the contractile ring in the ultra-micro algaCyanidium caldarium RK-1 journal March 1998
The chemistry and antioxidant properties of tocopherols and tocotrienols journal July 1996
An AFLP-based test of clonality in widespread, putatively asexual populations of Porphyra umbilicalis (Rhodophyta) in the Northwest Atlantic with an in silico analysis for bacterial contamination journal August 2012
Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species journal December 2015
The novel functions of kinesin motor proteins in plants journal December 2011
The littoral red alga Pyropia haitanensis uses rapid accumulation of floridoside as the desiccation acclimation strategy journal June 2014
Ethylene regulation of sexual reproduction in the marine red alga Pyropia yezoensis (Rhodophyta) journal July 2016
Algae as nutritional and functional food sources: revisiting our understanding journal November 2016
Evaluation of Bioactive Compounds in Fresh Edible Seaweeds journal October 2011
Increasing complexity and versatility: How the calcium signaling toolkit was shaped during plant land colonization journal March 2015
A Novel Protein, Ubiquitous in Marine Phytoplankton, Concentrates Iron at the Cell Surface and Facilitates Uptake journal February 2015
Cyanobacteria and Eukaryotic Algae Use Different Chemical Variants of Vitamin B12 journal April 2016
Kinesin-4 Functions in Vesicular Transport on Cortical Microtubules and Regulates Cell Wall Mechanics during Cell Elongation in Plants journal July 2015
Dynein light chain family genes in 15 plant species: Identification, evolution and expression profiles journal January 2017
Stretch growth of integrated axon tracts: Extremes and exploitations journal November 2009
Designing selective inhibitors for calcium-dependent protein kinases in apicomplexans journal July 2015
Porphyra: a marine crop shaped by stress journal January 2011
How pollen tubes grow journal March 2007
The bladed Bangiales (Rhodophyta) of the South Eastern Pacific: Molecular species delimitation reveals extensive diversity journal January 2016
Fertilization and the cytoskeleton in the red alga Bostrychia moritziana (Rhodomelaceae, Rhodophyta) journal November 2002
Metabolic Phenotypes Associated with High-Temperature Tolerance of Porphyra haitanensis Strains journal August 2013
Cloning and characterization of a class II DNA photolyase from Chlamydomonas journal August 1999
Influence of UV radiation and visible light on Porphyra umbilicalis: Photoinhibition and MAA concentration journal October 1999
2,3-Butanedione monoxime (BDM) as a myosin inhibitor journal August 2002
Plant pathogens and integrated defence responses to infection journal June 2001
Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity journal May 2009
Chlamydomonas reinhardtii thermal tolerance enhancement mediated by a mutualistic interaction with vitamin B12-producing bacteria journal March 2013
Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D journal April 2004
OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis journal August 2014
The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea journal January 2016
Genome of the red alga Porphyridium purpureum journal June 2013
The evolution of photosynthesis in chromist algae through serial endosymbioses journal December 2014
Clustering of a kinesin-14 motor enables processive retrograde microtubule-based transport in plants journal June 2015
Chaperones in control of protein disaggregation journal January 2008
The J-protein family: modulating protein assembly, disassembly and translocation journal June 2004
A calcium sensor – protein kinase signaling module diversified in plants and is retained in all lineages of Bikonta species journal August 2016
The high-affinity metal Transporters NRAMP1 and IRT1 Team up to Take up Iron under Sufficient Metal Provision journal November 2016
The structure and biosynthesis of porphyran: a comparison of some samples journal August 1962
The role of F-Actin During Fertilization in the red alga Aglaothamnion Oosumiense (Rhodophyta) journal August 1999
Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida journal March 2013
Molecular Mechanism for Inhibition of a Critical Component in the Arabidopsis thaliana Abscisic Acid Signal Transduction Pathways, SnRK2.6, by Protein Phosphatase ABI1 journal November 2011
The Class III Cyclobutane Pyrimidine Dimer Photolyase Structure Reveals a New Antenna Chromophore Binding Site and Alternative Photoreduction Pathways journal March 2015
Essential Role of an Unusually Long-lived Tyrosyl Radical in the Response to Red Light of the Animal-like Cryptochrome aCRY journal May 2016
Sensitivity of intertidal and subtidal red algae to UVA and UVB radiation, as monitored by Chlorophyll fluorescence measurements: Influence of collection depth and season, and length of irradiation journal November 1996
The solution to the cytological paradox of isomorphy journal March 1987
Class II formin targeting to the cell cortex by binding PI(3,5)P 2 is essential for polarized growth journal July 2012
Cytoskeletal dynamics: A view from the membrane journal May 2015
Recognition of non-self-polysaccharides by C-type lectin receptors dectin-1 and dectin-2 journal March 2009
The Effects of Salinity upon Cellular Volume of the Marine Red Alga Porphyra purpurea (Roth) C.Ag. journal December 1980
The sucrose non-fermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield journal October 2010
Lateral Gene Transfer of a Multigene Region from Cyanobacteria to Dinoflagellates Resulting in a Novel Plastid-Targeted Fusion Protein journal May 2006
Insights into the Evolution of Vitamin B12 Auxotrophy from Sequenced Algal Genomes journal May 2011
Fine-Tuning Motile Cilia and Flagella: Evolution of the Dynein Motor Proteins from Plants to Humans at High Resolution journal October 2016
Kinomer v. 1.0: a database of systematically classified eukaryotic protein kinases journal January 2009
Abscisic Acid Participates in the Control of Cell Cycle Initiation Through Heme Homeostasis in the Unicellular Red Alga Cyanidioschyzon merolae journal April 2016
Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista journal January 2016
Characterization of cell-cycle-driven and light-driven gene expression in a synchronous culture system in the unicellular rhodophyte Cyanidioschyzon merolae journal March 2010
Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum journal June 2006
The Role of Homogentisate Phytyltransferase and Other Tocopherol Pathway Enzymes in the Regulation of Tocopherol Synthesis during Abiotic Stress journal September 2003
Floridoside, L-Isofloridoside, and D-Isofloridoside in the Red Alga Porphyra columbina (Seasonal and Osmotic Effects) journal October 1993
Genome-Wide Annotation and Expression Profiling of Cell Cycle Regulatory Genes in Chlamydomonas reinhardtii journal February 2005
Beyond the Green: Understanding the Evolutionary Puzzle of Plant and Algal Cell Walls journal April 2010
A Plant Cryptochrome Controls Key Features of the Chlamydomonas Circadian Clock and Its Life Cycle journal March 2017
Fluorescence Characteristics of Photoinhibition and Recovery in a Sun and a Shade Species of the Red Algal Genus Porphyra journal March 1988
Class XI Myosins Are Required for Development, Cell Expansion, and F-Actin Organization in Arabidopsis journal June 2010
Chemical Composition and Structure of the cell Walls of the Conchocelis and Thallus Phases of Porphyra Tenera (Rhodophyceae)1,2 journal June 1981
Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes: Cryptochrome/photolyase family members in Ostreococcus tauri journal September 2010
Chloroplast rotation and morphological plasticity of the unicellular alga Rhodosorus (Rhodophyta, Stylonematales) journal September 2002
The CBL-CIPK Ca 2+ -decoding signaling network: function and perspectives journal November 2009
The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes journal July 2010
Inferring dispersal patterns of the generalist root fungus Armillaria mellea journal December 2011
Chemical Composition and Structure of the cell Walls of the Conchocelis and Thallus Phases of Porphyra Tenera (Rhodophyceae)1,2 journal June 1981
ACTIN AND MYOSIN REGULATE PSEUDOPODIA OF PORPHYRA PULCHELLA (RHODOPHYTA) ARCHEOSPORES journal February 2007
A new look at an Ancient Order: Generic Revision of the Bangiales (Rhodophyta)1: Generic Revision of the Bangiales journal September 2011
Major Developmental Regulators and Their Expression in two Closely Related Species of Porphyra (Rhodophyta)1: Developmental Genes in Porphyra journal April 2012
How many Species of Algae are There? journal September 2012
Evidence of ancient genome reduction in red algae (Rhodophyta) journal May 2015
Floridoside and isofloridoside are synthesized by trehalose 6-phosphate synthase-like enzymes in the red alga Galdieria sulphuraria journal October 2014
The Genetic and Molecular Basis for Sunscreen Biosynthesis in Cyanobacteria journal September 2010
Cyanophora paradoxa Genome Elucidates Origin of Photosynthesis in Algae and Plants journal February 2012
Gene Transfer from Bacteria and Archaea Facilitated Evolution of an Extremophilic Eukaryote journal March 2013
Sweet and sour sugars from the sea: the biosynthesis and remodeling of sulfated cell wall polysaccharides from marine macroalgae [Sweet and sour sugars from the sea: the biosynthesis and remodeling of sulfated cell wall polysaccharides from marine macroalgae] journal May 2015
FEA1 , FEA2 , and FRE1 , Encoding Two Homologous Secreted Proteins and a Candidate Ferrireductase, Are Expressed Coordinately with FOX1 and FTR1 in Iron-Deficient Chlamydomonas reinhardtii journal July 2007
An ATP-Grasp Ligase Involved in the Last Biosynthetic Step of the Iminomycosporine Shinorine in Nostoc punctiforme ATCC 29133 journal September 2011
Phycomyces. journal January 1969
Phycomyces journal March 1969
The Cryptochromes: Blue Light Photoreceptors in Plants and Animals journal June 2011
Abscisic Acid: Emergence of a Core Signaling Network journal June 2010
The Circadian System in Higher Plants journal June 2009
Patterns of kinesin evolution reveal a complex ancestral eukaryote with a multifunctional cytoskeleton journal January 2010
Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily journal July 2010
A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids journal January 2013
The cellulose synthase superfamily in fully sequenced plants and algae journal January 2009
Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species journal January 2007
The First Symbiont-Free Genome Sequence of Marine Red Alga, Susabi-nori (Pyropia yezoensis) journal March 2013
Diversity and Abundance of the Bacterial Community of the Red Macroalga Porphyra umbilicalis: Did Bacterial Farmers Produce Macroalgae? journal March 2013
Polysaccharide Localization in the Cell Wall of Porphyra leucosticta (Bangiophyceae, Rhodophyta) during the Life Cycle journal January 1995
Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes journal September 2000
Algae as nutritional and functional food sources: revisiting our understanding. text January 2017
A freeze-substitution ultrastructural study of the cytoskeleton of the red alga Antithamnion kylinii (Ceramiales) journal July 1998
News about cryptochrome photoreceptors in algae journal February 2013

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Genetic toolkits of the red alga Pyropia tenera against the three most common diseases in Pyropia farms journal April 2019
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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
antioxidants
carbohydrate-active enzymes (CAZymes)
cyclin D
iron-uptake
kinesin
mannan biosynthesis
mycosporine-like amino acids (MAAs)
septins
sulfated galactans
vitamin B12