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

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...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 31; pp. E6361 - E6370
Main Authors:	Brawley, Susan H., Blouin, Nicolas A., Ficko-Blean, Elizabeth, Wheeler, Glen L., Lohr, Martin, Goodson, Holly V., Jenkins, Jerry W., Blaby-Haas, Crysten E., Helliwell, Katherine E., Chan, Cheong Xin, Marriage, Tara N., Bhattacharya, Debashish, Klein, Anita S., Badis, Yacine, Brodie, Juliet, Cao, Yuanyu, Collén, Jonas, Dittami, Simon M., Gachon, Claire M. M., Green, Beverley R., Karpowicz, Steven J., Kim, Jay W., Kudahl, Ulrich Johan, Lin, Senjie, Michel, Gurvan, Mittag, Maria, Olson, Bradley J. S. C., Pangilinan, Jasmyn L., Peng, Yi, Qiu, Huan, Shu, Shengqiang, Singer, John T., Smith, Alison G., Sprecher, Brittany N., Wagner, Volker, Wang, Wenfei, Wang, Zhi-Yong, Yan, Juying, Yarish, Charles, Zäuner-Riek, Simone, Zhuang, Yunyun, Zou, Yong, Lindquist, Erika A., Grimwood, Jane, Barry, Kerrie W., Rokhsar, Daniel S., Schmutz, Jeremy, Stiller, John W., Grossman, Arthur R., Prochnik, Simon E.
Format:	Journal Article
Language:	English
Published:	United States National Academy of Sciences 01-08-2017 National Academy of Sciences, Washington, DC (United States)
Series:	PNAS Plus
Subjects:	Actins - genetics Algae antioxidants Bangiophycidae BASIC BIOLOGICAL SCIENCES Biological Sciences Calcium Calcium Signaling - genetics Calcium signalling carbohydrate-active enzymes (CAZymes) Cell cycle Cell Cycle - genetics Cell Wall - genetics Cell Wall - metabolism Cell walls Chromatin - genetics cyclin D Cytoskeleton Cytoskeleton - genetics Divergence Dynein Environmental Sciences Enzymes Eukaryotes Evolution Evolution, Molecular Food Genome, Plant - genetics Genomes Intertidal zone iron-uptake kinesin Kinesin - genetics Life Sciences Mannan mannan biosynthesis mycosporine-like amino acids (MAAs) Myosin Nutrient uptake Phylogeny PNAS Plus Porphyra Porphyra - cytology Porphyra - genetics Porphyra umbilicalis Proteins Rhodophyta septins sulfated galactans Sulfation vitamin B12 stress tolerance carbohydrate-active enzymes vitamin B12 calcium-signaling cytoskeleton
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Summary:	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.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 PMCID: PMC5547612 BNL-114055-2017-JA SC0012704; AC02-05CH11231 USDOE Office of Science (SC), Biological and Environmental Research (BER) 2Present address: Genetics Program, University of New Hampshire, Durham, NH 03824. 3Present address: College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China. Edited by Stephen R. Palumbi, Stanford University, Pacific Grove, CA, and approved June 6, 2017 (received for review February 22, 2017) Author contributions: S.H.B., N.A.B., D.B., S.L., C.Y., K.W.B., D.S.R., J.S., J.W.S., A.R.G., and S.E.P. designed research; S.H.B., N.A.B., E.F.-B., G.L.W., M.L., H.V.G., J.W.J., C.E.B.-H., K.E.H., C.X.C., T.N.M., D.B., A.S.K., Y.B., J.B., Y.C., J.C., S.M.D., C.M.M.G., B.R.G., S.J.K., J.W.K., U.J.K., S.L., G.M., M.M., B.J.S.C.O., J.L.P., Y.P., H.Q., S.S., A.G.S., B.N.S., V.W., W.W., Z.-Y.W., J.Y., S.Z.-R., Y. Zou, E.A.L., J.G., K.W.B., D.S.R., J.S., J.W.S., A.R.G., and S.E.P. performed research; S.H.B., N.A.B., E.F.-B., G.L.W., M.L., H.V.G., J.W.J., C.E.B.-H., K.E.H., C.X.C., D.B., S.M.D., C.M.M.G., S.J.K., G.M., H.Q., A.G.S., J.S., J.W.S., and S.E.P. contributed new reagents/analytic tools; S.H.B., N.A.B., E.F.-B., G.L.W., M.L., H.V.G., J.W.J., C.E.B.-H., K.E.H., C.X.C., T.N.M., D.B., A.S.K., Y.B., J.B., Y.C., J.C., S.M.D., C.M.M.G., B.R.G., S.J.K., J.W.K., U.J.K., S.L., G.M., M.M., B.J.S.C.O., H.Q., A.G.S., B.N.S., V.W., W.W., Z.-Y.W., S.Z.-R., Y. Zou, J.S., J.W.S., A.R.G., and S.E.P. analyzed data; S.H.B., N.A.B., S.L., J.T.S., C.Y., Y. Zhuang, and A.R.G. prepared samples; and S.H.B., N.A.B., E.F.-B., G.L.W., M.L., H.V.G., J.W.J., C.E.B.-H., K.E.H., C.X.C., T.N.M., D.B., A.S.K., Y.B., J.B., Y.C., J.C., S.M.D., C.M.M.G., B.R.G., S.J.K., J.W.K., U.J.K., S.L., G.M., M.M., B.J.S.C.O., H.Q., J.T.S., A.G.S., B.N.S., V.W., W.W., Z.-Y.W., C.Y., S.Z.-R., Y. Zhuang, Y. Zou, J.W.S., A.R.G., and S.E.P. wrote the paper.
ISSN:	0027-8424 1091-6490
DOI:	10.1073/pnas.1703088114