Seagrass genomes reveal ancient polyploidy and adaptations to the marine environment

Ma, Xiao; Vanneste, Steffen; Chang, Jiyang; Ambrosino, Luca; Barry, Kerrie; Bayer, Till; Bobrov, Alexander A.; Boston, LoriBeth; Campbell, Justin E.; Chen, Hengchi; Chiusano, Maria Luisa; Dattolo, Emanuela; Grimwood, Jane; He, Guifen; Jenkins, Jerry; Khachaturyan, Marina; Marín-Guirao, Lázaro; Mesterházy, Attila; Muhd, Danish-Daniel; Pazzaglia, Jessica; Plott, Chris; Rajasekar, Shanmugam; Rombauts, Stephane; Ruocco, Miriam; Scott, Alison; Tan, Min Pau; Van de Velde, Jozefien; Vanholme, Bartel; Webber, Jenell; Wong, Li Lian; Yan, Mi; Sung, Yeong Yik; Novikova, Polina; Schmutz, Jeremy; Reusch, Thorsten B. H.; Procaccini, Gabriele; Olsen, Jeanine L.; Van de Peer, Yves

doi:10.1038/s41477-023-01608-5

Seagrass genomes reveal ancient polyploidy and adaptations to the marine environment

Journal Article · Fri Jan 26 00:00:00 EST 2024 · Nature Plants (Online)

DOI:https://doi.org/10.1038/s41477-023-01608-5· OSTI ID:2466155

^[1]; Vanneste, Steffen ^[2]; ^[1]; ^[3]; ^[4]; ^[5]; ^[6]; Boston, LoriBeth ^[7]; Campbell, Justin E. ^[8]; ^[1]; Chiusano, Maria Luisa ^[9]; Dattolo, Emanuela ^[10]; ^[7]; He, Guifen ^[4]; ^[7]; ^[11]; ^[12]; Mesterházy, Attila ^[13]; ^[14]; ^[10] more »

Ghent Univ. (Belgium); Vlaams Instituut voor Biotechnologie (VIB), Ghent (Belgium)
Ghent Univ. (Belgium)
Stazione Zoologica Anton Dohrn (SZN), Naples (Italy)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
GEOMAR Helmholtz-Zentrum für Ozeanforschung Kiel (Germany)
Russian Academy of Sciences (RAS), Borok (Russian Federation). Papanin Institute for Biology of Inland Waters
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
Florida International Univ. (FIU), Miami, FL (United States)
Stazione Zoologica Anton Dohrn (SZN), Naples (Italy); Univ. of Naples Federico II (Italy)
Stazione Zoologica Anton Dohrn (SZN), Naples (Italy); National Biodiversity Future Centre (NBFC), Palermo (Italy)
GEOMAR Helmholtz-Zentrum für Ozeanforschung Kiel (Germany); Univ. of Kiel (Germany)
Stazione Zoologica Anton Dohrn (SZN), Naples (Italy); Spanish Institute of Oceanography (IEO-CSIC), Murcia (Spain)
Centre for Ecological Research, Debrecen (Hungary). Wetland Ecology Research Group
Universiti Malaysia Terengganu (Malaysia)
Univ. of Arizona, Tucson, AZ (United States)
Stazione Zoologica Anton Dohrn (SZN), Naples (Italy); Univ. of Bologna (Italy); Stazione Zoologica Anton Dohrn (SZN), Fano (Italy). Fano Marine Center
Max Planck Institute for Plant Breeding Research, Cologne (Germany)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
Univ. of Groningen (Netherlands)
Ghent Univ. (Belgium); Vlaams Instituut voor Biotechnologie (VIB), Ghent (Belgium); Univ. of Pretoria (South Africa); Nanjing Agricultural University (China)

Here, we present chromosome-level genome assemblies from representative species of three independently evolved seagrass lineages: Posidonia oceanica, Cymodocea nodosa, Thalassia testudinum and Zostera marina. We also include a draft genome of Potamogeton acutifolius, belonging to a freshwater sister lineage to Zosteraceae. All seagrass species share an ancient whole-genome triplication, while additional whole-genome duplications were uncovered for C. nodosa, Z. marina and P. acutifolius. Comparative analysis of selected gene families suggests that the transition from submerged-freshwater to submerged-marine environments mainly involved fine-tuning of multiple processes (such as osmoregulation, salinity, light capture, carbon acquisition and temperature) that all had to happen in parallel, probably explaining why adaptation to a marine lifestyle has been exceedingly rare. Major gene losses related to stomata, volatiles, defence and lignification are probably a consequence of the return to the sea rather than the cause of it. These new genomes will accelerate functional studies and solutions, as continuing losses of the savannahs of the sea are of major concern in times of climate change and loss of biodiversity.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2466155

Journal Information:: Nature Plants (Online), Journal Name: Nature Plants (Online) Journal Issue: 2 Vol. 10; ISSN 2055-0278

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (128)

BUSCO: Assessing Genome Assembly and Annotation Completeness Seppey, Mathieu; Manni, Mosè; Zdobnov, Evgeny M. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-9173-0_14	book	January 2019
GeMoMa: Homology-Based Gene Prediction Utilizing Intron Position Conservation and RNA-seq Data Keilwagen, Jens; Hartung, Frank; Grau, Jan Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-9173-0_9	book	January 2019
Systematics and Evolution of Australian Seagrasses in a Global Context Waycott, Michelle; Biffin, Edward; Les, Donald H. Seagrasses of Australia https://doi.org/10.1007/978-3-319-71354-0_5	book	January 2018
Lower Vibrio spp. abundances in Zostera marina leaf canopies suggest a novel ecosystem function for temperate seagrass beds Reusch, Thorsten B. H.; Schubert, Philipp R.; Marten, Silke-Mareike Marine Biology, Vol. 168, Issue 10 https://doi.org/10.1007/s00227-021-03963-3	journal	September 2021
Seasonal dynamics of arbuscular mycorrhizal fungi in differing wetland habitats Bohrer, Kelly E.; Friese, Carl F.; Amon, James P. Mycorrhiza, Vol. 14, Issue 5 https://doi.org/10.1007/s00572-004-0292-7	journal	March 2004
AM fungal communities inhabiting the roots of submerged aquatic plant Lobelia dortmanna are diverse and include a high proportion of novel taxa Moora, Mari; Öpik, Maarja; Davison, John Mycorrhiza, Vol. 26, Issue 7 https://doi.org/10.1007/s00572-016-0709-0	journal	May 2016
Heterologous expression of vacuolar H+-PPase enhances the electrochemical gradient across the vacuolar membrane and improves tobacco cell salt tolerance Duan, Xiao-Guang; Yang, Ai-Fang; Gao, Feng Protoplasma, Vol. 232, Issue 1-2 https://doi.org/10.1007/s00709-007-0268-5	journal	December 2007
Genetic Improvement of Sugarcane for Drought and Salinity Stress Tolerance Using Arabidopsis Vacuolar Pyrophosphatase (AVP1) Gene Kumar, Tanweer; Khan, Muhammad Ramzan Molecular Biotechnology, Vol. 56, Issue 3 https://doi.org/10.1007/s12033-013-9695-z	journal	September 2013
Conformations and interactions of pectins Morris, E. R.; Powell, D. A.; Gidley, M. J. Journal of Molecular Biology, Vol. 155, Issue 4 https://doi.org/10.1016/0022-2836(82)90484-3	journal	March 1982
Zostera capensis setchell: Root structure in relation to function Barnabas, Alban D.; Arnott, Howard J. Aquatic Botany, Vol. 27, Issue 4 https://doi.org/10.1016/0304-3770(87)90071-4	journal	May 1987
Apparent lack of vesicular–arbuscular mycorrhiza (VAM) in the seagrasses Zostera marina L. and Thalassia testudinum Banks ex König Nielsen, Søren Laurentius; Thingstrup, Ida; Wigand, Cathleen Aquatic Botany, Vol. 63, Issue 3-4 https://doi.org/10.1016/S0304-3770(98)00123-5	journal	April 1999
Building Beauty Lohmann, Jan U.; Weigel, Detlef Developmental Cell, Vol. 2, Issue 2 https://doi.org/10.1016/S1534-5807(02)00122-3	journal	February 2002
The plant heat stress transcription factor (Hsf) family: Structure, function and evolution Scharf, Klaus-Dieter; Berberich, Thomas; Ebersberger, Ingo Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1819, Issue 2 https://doi.org/10.1016/j.bbagrm.2011.10.002	journal	February 2012
U–Pb and Re–Os geochronology of the Aptian/Albian and Cenomanian/Turonian stage boundaries: Implications for timescale calibration, osmium isotope seawater composition and Re–Os systematics in organic-rich sediments Selby, David; Mutterlose, Jörg; Condon, Daniel J. Chemical Geology, Vol. 265, Issue 3-4 https://doi.org/10.1016/j.chemgeo.2009.05.005	journal	July 2009
Phylogenomic Evidence for the Monophyly of Bryophytes and the Reductive Evolution of Stomata Harris, Brogan J.; Harrison, C. Jill; Hetherington, Alistair M. Current Biology, Vol. 30, Issue 11 https://doi.org/10.1016/j.cub.2020.03.048	journal	June 2020
Global seagrass distribution and diversity: A bioregional model Short, F.; Carruthers, T.; Dennison, W. Journal of Experimental Marine Biology and Ecology, Vol. 350, Issue 1-2 https://doi.org/10.1016/j.jembe.2007.06.012	journal	November 2007
Protecting the hand that feeds us: Seagrass (Zostera marina) serves as commercial juvenile fish habitat Bertelli, Chiara M.; Unsworth, Richard K. F. Marine Pollution Bulletin, Vol. 83, Issue 2 https://doi.org/10.1016/j.marpolbul.2013.08.011	journal	June 2014
Origin and Evolution of Core Components Responsible for Monitoring Light Environment Changes during Plant Terrestrialization Han, Xue; Chang, Xin; Zhang, Zhenhua Molecular Plant, Vol. 12, Issue 6 https://doi.org/10.1016/j.molp.2019.04.006	journal	June 2019
An angiosperm NLR Atlas reveals that NLR gene reduction is associated with ecological specialization and signal transduction component deletion Liu, Yang; Zeng, Zhen; Zhang, Yan-Mei Molecular Plant, Vol. 14, Issue 12 https://doi.org/10.1016/j.molp.2021.08.001	journal	December 2021
Transposons: a blessing curse Dubin, Manu J.; Mittelsten Scheid, Ortrun; Becker, Claude Current Opinion in Plant Biology, Vol. 42 https://doi.org/10.1016/j.pbi.2018.01.003	journal	April 2018
Phenolic chemistry of the seagrass Zostera noltei Hornem. Part 1: First evidence of three infraspecific flavonoid chemotypes in three distinctive geographical regions Grignon-Dubois, Micheline; Rezzonico, Bernadette Phytochemistry, Vol. 146 https://doi.org/10.1016/j.phytochem.2017.12.006	journal	February 2018
Root cell wall solutions for crop plants in saline soils Byrt, Caitlin S.; Munns, Rana; Burton, Rachel A. Plant Science, Vol. 269 https://doi.org/10.1016/j.plantsci.2017.12.012	journal	April 2018
Quaternary glaciations of northern Europe Böse, Margot; Lüthgens, Christopher; Lee, Jonathan R. Quaternary Science Reviews, Vol. 44 https://doi.org/10.1016/j.quascirev.2012.04.017	journal	June 2012
Plant Phenylalanine/Tyrosine Ammonia-lyases Barros, Jaime; Dixon, Richard A. Trends in Plant Science, Vol. 25, Issue 1 https://doi.org/10.1016/j.tplants.2019.09.011	journal	January 2020
The Role of Vegetated Coastal Wetlands for Marine Megafauna Conservation Sievers, Michael; Brown, Christopher J.; Tulloch, Vivitskaia J. D. Trends in Ecology & Evolution, Vol. 34, Issue 9 https://doi.org/10.1016/j.tree.2019.04.004	journal	September 2019
Light and Photosynthesis in Aquatic Ecosystems Kirk, John T. O. https://doi.org/10.1017/CBO9781139168212	journal	January 2010
Structural Characterization and Cytotoxic Properties of an Apiose-Rich Pectic Polysaccharide Obtained from the Cell Wall of the Marine Phanerogam Zostera marina Gloaguen, Vincent; Brudieux, Véronique; Closs, Brigitte Journal of Natural Products, Vol. 73, Issue 6 https://doi.org/10.1021/np100092c	journal	June 2010
Nutrients as the dominant control on the spread of anoxia and euxinia across the Cenomanian‐Turonian oceanic anoxic event (OAE2): Model‐data comparison Monteiro, F. M.; Pancost, R. D.; Ridgwell, A. Paleoceanography, Vol. 27, Issue 4 https://doi.org/10.1029/2012PA002351	journal	December 2012
Airborne signalling by methyl salicylate in plant pathogen resistance Shulaev, Vladimir; Silverman, Paul; Raskin, Ilya Nature, Vol. 385, Issue 6618 https://doi.org/10.1038/385718a0	journal	February 1997
A central integrator of transcription networks in plant stress and energy signalling Baena-González, Elena; Rolland, Filip; Thevelein, Johan M. Nature, Vol. 448, Issue 7156 https://doi.org/10.1038/nature06069	journal	August 2007
Strigolactone inhibition of shoot branching Gomez-Roldan, Victoria; Fermas, Soraya; Brewer, Philip B. Nature, Vol. 455, Issue 7210 https://doi.org/10.1038/nature07271	journal	August 2008
The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea Olsen, Jeanine L.; Rouzé, Pierre; Verhelst, Bram Nature, Vol. 530, Issue 7590 https://doi.org/10.1038/nature16548	journal	January 2016
Reconstructing the genome of the most recent common ancestor of flowering plants Murat, Florent; Armero, Alix; Pont, Caroline Nature Genetics, Vol. 49, Issue 4 https://doi.org/10.1038/ng.3813	journal	March 2017
The evolutionary significance of polyploidy Van de Peer, Yves; Mizrachi, Eshchar; Marchal, Kathleen Nature Reviews Genetics, Vol. 18, Issue 7 https://doi.org/10.1038/nrg.2017.26	journal	May 2017
Molecular mechanisms of flower development: an armchair guide Krizek, Beth A.; Fletcher, Jennifer C. Nature Reviews Genetics, Vol. 6, Issue 9 https://doi.org/10.1038/nrg1675	journal	September 2005
Microorganisms facilitate uptake of dissolved organic nitrogen by seagrass leaves Tarquinio, Flavia; Bourgoure, Jeremy; Koenders, Annette The ISME Journal, Vol. 12, Issue 11 https://doi.org/10.1038/s41396-018-0218-6	journal	July 2018
Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress Hartman, Sjon; Liu, Zeguang; van Veen, Hans Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12045-4	journal	September 2019
Tiger sharks support the characterization of the world’s largest seagrass ecosystem Gallagher, Austin J.; Brownscombe, Jacob W.; Alsudairy, Nourah A. Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-33926-1	journal	November 2022
Correlative adaptation between Rubisco and CO2-concentrating mechanisms in seagrasses Capó-Bauçà, Sebastià; Iñiguez, Concepción; Aguiló-Nicolau, Pere Nature Plants, Vol. 8, Issue 6 https://doi.org/10.1038/s41477-022-01171-5	journal	June 2022
Ocean current patterns drive the worldwide colonization of eelgrass (Zostera marina) Yu, Lei; Khachaturyan, Marina; Matschiner, Michael Nature Plants, Vol. 9, Issue 8 https://doi.org/10.1038/s41477-023-01464-3	journal	July 2023
Sugars dominate the seagrass rhizosphere Sogin, E. Maggie; Michellod, Dolma; Gruber-Vodicka, Harald R. Nature Ecology & Evolution, Vol. 6, Issue 7 https://doi.org/10.1038/s41559-022-01740-z	journal	May 2022
Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium Mohr, Wiebke; Lehnen, Nadine; Ahmerkamp, Soeren Nature, Vol. 600, Issue 7887 https://doi.org/10.1038/s41586-021-04063-4	journal	November 2021
Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype Kim, Daehwan; Paggi, Joseph M.; Park, Chanhee Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0201-4	journal	August 2019
Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm Cheng, Haoyu; Concepcion, Gregory T.; Feng, Xiaowen Nature Methods, Vol. 18, Issue 2 https://doi.org/10.1038/s41592-020-01056-5	journal	February 2021
Surface chemical defence of the eelgrass Zostera marina against microbial foulers Papazian, Stefano; Parrot, Delphine; Burýšková, Barbora Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-39212-3	journal	February 2019
A reference-grade genome identifies salt-tolerance genes from the salt-secreting mangrove species Avicennia marina Natarajan, Purushothaman; Murugesan, Ashok Kumar; Govindan, Ganesan Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-02384-8	journal	July 2021
Blue carbon as a natural climate solution Macreadie, Peter I.; Costa, Micheli D. P.; Atwood, Trisha B. Nature Reviews Earth & Environment, Vol. 2, Issue 12 https://doi.org/10.1038/s43017-021-00224-1	journal	November 2021
The biosynthesis of the branched-chain sugar d-apiose in plants: functional cloning and characterization of a UDP-d-apiose/UDP-d-xylose synthase from Arabidopsis Mølhøj, Michael; Verma, Rajeev; Reiter, Wolf-Dieter The Plant Journal, Vol. 35, Issue 6 https://doi.org/10.1046/j.1365-313X.2003.01841.x	journal	September 2003
Functional analysis of lactate dehydrogenase during hypoxic stress in Arabidopsis Dolferus, Rudy; Wolansky, Mark; Carroll, Rebecka Functional Plant Biology, Vol. 35, Issue 2 https://doi.org/10.1071/FP07228	journal	January 2008
Evolution of halophytes: multiple origins of salt tolerance in land plants Flowers, Timothy J.; Galal, Hanaa K.; Bromham, Lindell Functional Plant Biology, Vol. 37, Issue 7 https://doi.org/10.1071/FP09269	journal	January 2010
Rapid recent growth and divergence of rice nuclear genomes Ma, J.; Bennetzen, J. L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 34 https://doi.org/10.1073/pnas.0403715101	journal	July 2004
From The Cover: An algorithm for progressive multiple alignment of sequences with insertions Loytynoja, A.; Goldman, N. Proceedings of the National Academy of Sciences, Vol. 102, Issue 30 https://doi.org/10.1073/pnas.0409137102	journal	July 2005
Accelerating loss of seagrasses across the globe threatens coastal ecosystems Waycott, M.; Duarte, C. M.; Carruthers, T. J. B. Proceedings of the National Academy of Sciences, Vol. 106, Issue 30 https://doi.org/10.1073/pnas.0905620106	journal	July 2009
Plant evolution and environmental adaptation unveiled by long-read whole-genome sequencing of Spirodela An, Dong; Zhou, Yong; Li, Changsheng Proceedings of the National Academy of Sciences, Vol. 116, Issue 38 https://doi.org/10.1073/pnas.1910401116	journal	September 2019
Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump Gaxiola, R. A.; Li, J.; Undurraga, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 20 https://doi.org/10.1073/pnas.191389398	journal	September 2001
The number and kinds of embryo-bearing plants which have become aquatic: a survey Cook, Christopher D. K. Perspectives in Plant Ecology, Evolution and Systematics, Vol. 2, Issue 1 https://doi.org/10.1078/1433-8319-00066	journal	January 1999
An antifouling model from the sea: a review of 25 years of zosteric acid studies Vilas-Boas, Cátia; Sousa, Emília; Pinto, Madalena Biofouling, Vol. 33, Issue 10 https://doi.org/10.1080/08927014.2017.1391951	journal	November 2017
Ion selectivity of the Kat1 K⁺channel pore Nakamura, Robert L.; Gaber, Richard F. Molecular Membrane Biology, Vol. 26, Issue 5-7 https://doi.org/10.1080/09687680903188332	journal	January 2009
Encoded C₄ homologue enzymes genes function under abiotic stresses in C3 plant Chen, Siming; Peng, Wangmenghan; Ansah, Ebenezer Ottopah Plant Signaling & Behavior, Vol. 17, Issue 1 https://doi.org/10.1080/15592324.2022.2115634	journal	September 2022
The global distribution of seagrass meadows McKenzie, Len J.; Nordlund, Lina M.; Jones, Benjamin L. Environmental Research Letters, Vol. 15, Issue 7 https://doi.org/10.1088/1748-9326/ab7d06	journal	July 2020
Impact of transposable elements on polyploid plant genomes Vicient, Carlos M.; Casacuberta, Josep M. Annals of Botany, Vol. 120, Issue 2 https://doi.org/10.1093/aob/mcx078	journal	July 2017
MRBAYES: Bayesian inference of phylogenetic trees Huelsenbeck, J. P.; Ronquist, F. Bioinformatics, Vol. 17, Issue 8 https://doi.org/10.1093/bioinformatics/17.8.754	journal	August 2001
DeepTE: a computational method for de novo classification of transposons with convolutional neural network Yan, Haidong; Bombarely, Aureliano; Li, Song Bioinformatics, Vol. 36, Issue 15 https://doi.org/10.1093/bioinformatics/btaa519	journal	May 2020
ksrates: positioning whole-genome duplications relative to speciation events in KS distributions Sensalari, Cecilia; Maere, Steven; Lohaus, Rolf Bioinformatics, Vol. 38, Issue 2 https://doi.org/10.1093/bioinformatics/btab602	journal	August 2021
GMAP: a genomic mapping and alignment program for mRNA and EST sequences Wu, T. D.; Watanabe, C. K. Bioinformatics, Vol. 21, Issue 9 https://doi.org/10.1093/bioinformatics/bti310	journal	February 2005
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Infernal 1.1: 100-fold faster RNA homology searches Nawrocki, E. P.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 22 https://doi.org/10.1093/bioinformatics/btt509	journal	September 2013
ARCS: scaffolding genome drafts with linked reads Yeo, Sarah; Coombe, Lauren; Warren, René L. Bioinformatics, Vol. 34, Issue 5 https://doi.org/10.1093/bioinformatics/btx675	journal	October 2017
wgd—simple command line tools for the analysis of ancient whole-genome duplications Zwaenepoel, Arthur; Van de Peer, Yves Bioinformatics, Vol. 35, Issue 12 https://doi.org/10.1093/bioinformatics/bty915	journal	November 2018
Genome-wide survey of the seagrass Zostera muelleri suggests modification of the ethylene signalling network Golicz, Agnieszka A.; Schliep, Martin; Lee, Huey Tyng Journal of Experimental Botany, Vol. 66, Issue 5 https://doi.org/10.1093/jxb/eru510	journal	January 2015
Carbon-concentrating mechanisms in seagrasses Larkum, Anthony William D.; Davey, Peter A.; Kuo, John Journal of Experimental Botany, Vol. 68, Issue 14 https://doi.org/10.1093/jxb/erx206	journal	June 2017
IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era Minh, Bui Quang; Schmidt, Heiko A.; Chernomor, Olga Molecular Biology and Evolution, Vol. 37, Issue 5 https://doi.org/10.1093/molbev/msaa015	journal	February 2020
Phylogenomic Analyses of Alismatales Shed Light into Adaptations to Aquatic Environments Chen, Ling-Yun; Lu, Bei; Morales-Briones, Diego F. Molecular Biology and Evolution, Vol. 39, Issue 5 https://doi.org/10.1093/molbev/msac079	journal	April 2022
PAML 4: Phylogenetic Analysis by Maximum Likelihood Yang, Z. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm088	journal	April 2007
Bayesian Phylogenetics with BEAUti and the BEAST 1.7 Drummond, Alexei J.; Suchard, Marc A.; Xie, Dong Molecular Biology and Evolution, Vol. 29, Issue 8 https://doi.org/10.1093/molbev/mss075	journal	February 2012
Inference of Ancient Whole-Genome Duplications and the Evolution of Gene Duplication and Loss Rates Zwaenepoel, Arthur; Van de Peer, Yves Molecular Biology and Evolution, Vol. 36, Issue 7 https://doi.org/10.1093/molbev/msz088	journal	April 2019
Rfam 14: expanded coverage of metagenomic, viral and microRNA families Kalvari, Ioanna; Nawrocki, Eric P.; Ontiveros-Palacios, Nancy Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1047	journal	November 2020
UniProt: the universal protein knowledgebase in 2021 Bateman, Alex; Martin, Maria-Jesus; Orchard, Sandra Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1100	journal	November 2020
Inparanoid: a comprehensive database of eukaryotic orthologs O'Brien, K. P. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki107	journal	December 2004
InterProScan: protein domains identifier Quevillon, E.; Silventoinen, V.; Pillai, S. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki442	journal	July 2005
LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons Xu, Z.; Wang, H. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm286	journal	May 2007
MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity Wang, Y.; Tang, H.; DeBarry, J. D. Nucleic Acids Research, Vol. 40, Issue 7 https://doi.org/10.1093/nar/gkr1293	journal	January 2012
i-ADHoRe 3.0—fast and sensitive detection of genomic homology in extremely large data sets Proost, Sebastian; Fostier, Jan; De Witte, Dieter Nucleic Acids Research, Vol. 40, Issue 2 https://doi.org/10.1093/nar/gkr955	journal	November 2011
GenomeView: a next-generation genome browser Abeel, T.; Van Parys, T.; Saeys, Y. Nucleic Acids Research, Vol. 40, Issue 2 https://doi.org/10.1093/nar/gkr995	journal	November 2011
GenBank Benson, Dennis A.; Cavanaugh, Mark; Clark, Karen Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1195	journal	November 2012
The genome portal of the Department of Energy Joint Genome Institute: 2014 updates Nordberg, Henrik; Cantor, Michael; Dusheyko, Serge Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1069	journal	November 2013
Ribose-Map: a bioinformatics toolkit to map ribonucleotides embedded in genomic DNA Gombolay, Alli L.; Vannberg, Fredrik O.; Storici, Francesca Nucleic Acids Research, Vol. 47, Issue 1 https://doi.org/10.1093/nar/gky874	journal	October 2018
BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database Brůna, Tomáš; Hoff, Katharina J.; Lomsadze, Alexandre NAR Genomics and Bioinformatics, Vol. 3, Issue 1 https://doi.org/10.1093/nargab/lqaa108	journal	January 2021
The origin, diversification and adaptation of a major mangrove clade (Rhizophoreae) revealed by whole-genome sequencing Xu, Shaohua; He, Ziwen; Zhang, Zhang National Science Review, Vol. 4, Issue 5 https://doi.org/10.1093/nsr/nwx065	journal	June 2017
Overexpression of a Populus trichocarpa H+-pyrophosphatase gene PtVP1.1 confers salt tolerance on transgenic poplar Yang, Y.; Tang, R. J.; Li, B. Tree Physiology, Vol. 35, Issue 6 https://doi.org/10.1093/treephys/tpv027	journal	April 2015
The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000 Dudchenko, Olga; Shamim, Muhammad S.; Batra, Sanjit S. bioRxiv https://doi.org/10.1101/254797	preprint	January 2018
Circos: An information aesthetic for comparative genomics Krzywinski, M.; Schein, J.; Birol, I. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.092759.109	journal	June 2009
Ultralow-input single-tube linked-read library method enables short-read second-generation sequencing systems to routinely generate highly accurate and economical long-range sequencing information Chen, Zhoutao; Pham, Long; Wu, Tsai-Chin Genome Research, Vol. 30, Issue 6 https://doi.org/10.1101/gr.260380.119	journal	June 2020
Ethylene-Mediated Acclimations to Flooding Stress Sasidharan, Rashmi; Voesenek, Laurentius A. C. J. Plant Physiology, Vol. 169, Issue 1 https://doi.org/10.1104/pp.15.00387	journal	April 2015
Ethylene and Hormonal Cross Talk in Vegetative Growth and Development Van de Poel, Bram; Smet, Dajo; Van Der Straeten, Dominique Plant Physiology, Vol. 169, Issue 1 https://doi.org/10.1104/pp.15.00724	journal	July 2015
LTR_retriever: A Highly Accurate and Sensitive Program for Identification of Long Terminal Repeat Retrotransposons Ou, Shujun; Jiang, Ning Plant Physiology, Vol. 176, Issue 2 https://doi.org/10.1104/pp.17.01310	journal	December 2017
LACCASE Is Necessary and Nonredundant with PEROXIDASE for Lignin Polymerization during Vascular Development in Arabidopsis Zhao, Qiao; Nakashima, Jin; Chen, Fang The Plant Cell, Vol. 25, Issue 10 https://doi.org/10.1105/tpc.113.117770	journal	October 2013
GenomeTools: A Comprehensive Software Library for Efficient Processing of Structured Genome Annotations Gremme, Gordon; Steinbiss, Sascha; Kurtz, Stefan IEEE/ACM Transactions on Computational Biology and Bioinformatics, Vol. 10, Issue 3 https://doi.org/10.1109/TCBB.2013.68	journal	May 2013
Assessing the CO₂capture potential of seagrass restoration projects Duarte, Carlos M.; Sintes, Tomás; Marbà, Núria Journal of Applied Ecology, Vol. 50, Issue 6 https://doi.org/10.1111/1365-2664.12155	journal	September 2013
Phenotypic plasticity under rapid global changes: The intrinsic force for future seagrasses survival Pazzaglia, Jessica; Reusch, Thorsten B. H.; Terlizzi, Antonio Evolutionary Applications, Vol. 14, Issue 5 https://doi.org/10.1111/eva.13212	journal	April 2021
Climate change and ocean acidification effects on seagrasses and marine macroalgae Koch, Marguerite; Bowes, George; Ross, Cliff Global Change Biology, Vol. 19, Issue 1 https://doi.org/10.1111/j.1365-2486.2012.02791.x	journal	September 2012
Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants Wang, Bin; Yeun, Li Huey; Xue, Jia-Yu New Phytologist, Vol. 186, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03137.x	journal	January 2010
Surprising spectra of root-associated fungi in submerged aquatic plants Kohout, Petr; Sýkorová, Zuzana; Čtvrtlíková, Martina FEMS Microbiology Ecology, Vol. 80, Issue 1 https://doi.org/10.1111/j.1574-6941.2011.01291.x	journal	January 2012
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics Strullu-Derrien, Christine; Selosse, Marc-André; Kenrick, Paul New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15076	journal	March 2018
The SnRK1‐eIFiso4G1 signaling relay regulates the translation of specific mRNAs in Arabidopsis under submergence Cho, Hsing‐Yi; Lu, Mei‐Yeh Jade; Shih, Ming‐Che New Phytologist, Vol. 222, Issue 1 https://doi.org/10.1111/nph.15589	journal	December 2018
Direct uptake of HCO ₃ ⁻ in the marine angiosperm Posidonia oceanica (L.) Delile driven by a plasma membrane H ⁺ economy Rubio, Lourdes; García, Delia; García-Sánchez, María J. Plant, Cell & Environment, Vol. 40, Issue 11 https://doi.org/10.1111/pce.13057	journal	September 2017
The genome of the king protea, Protea cynaroides Chang, Jiyang; Duong, Tuan A.; Schoeman, Cassandra The Plant Journal, Vol. 113, Issue 2 https://doi.org/10.1111/tpj.16044	journal	December 2022
Restoration of seagrass habitat leads to rapid recovery of coastal ecosystem services Orth, Robert J.; Lefcheck, Jonathan S.; McGlathery, Karen S. Science Advances, Vol. 6, Issue 41 https://doi.org/10.1126/sciadv.abc6434	journal	October 2020
Developmental changes in lignin composition are driven by both monolignol supply and laccase specificity Zhuo, Chunliu; Wang, Xin; Docampo-Palacios, Maite Science Advances, Vol. 8, Issue 10 https://doi.org/10.1126/sciadv.abm8145	journal	March 2022
Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates Lamb, Joleah B.; van de Water, Jeroen A. J. M.; Bourne, David G. Science, Vol. 355, Issue 6326 https://doi.org/10.1126/science.aal1956	journal	February 2017
The planetary role of seagrass conservation Unsworth, Richard K. F.; Cullen-Unsworth, Leanne C.; Jones, Benjamin L. H. Science, Vol. 377, Issue 6606 https://doi.org/10.1126/science.abq6923	journal	August 2022
Studies of the Development of Zostera Marina l.: i. the Embryo and seed Taylor, A. R. A. Canadian Journal of Botany, Vol. 35, Issue 4 https://doi.org/10.1139/b57-042	journal	July 1957
Salt Tolerance Mechanisms of Plants van Zelm, Eva; Zhang, Yanxia; Testerink, Christa Annual Review of Plant Biology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-arplant-050718-100005	journal	April 2020
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons Ellinghaus, David; Kurtz, Stefan; Willhoeft, Ute BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-18	journal	January 2008
Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments Haas, Brian J.; Salzberg, Steven L.; Zhu, Wei Genome Biology, Vol. 9, Issue 1 https://doi.org/10.1186/gb-2008-9-1-r7	journal	January 2008
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy Emms, David M.; Kelly, Steven Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0721-2	journal	August 2015
OrthoFinder: phylogenetic orthology inference for comparative genomics Emms, David M.; Kelly, Steven Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1832-y	journal	November 2019
Transcriptome assembly from long-read RNA-seq alignments with StringTie2 Kovaka, Sam; Zimin, Aleksey V.; Pertea, Geo M. Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1910-1	journal	December 2019
Improved chromosome-level genome assembly and annotation of the seagrass, Zostera marina (eelgrass) Ma, Xiao; Olsen, Jeanine L.; Reusch, Thorsten B. H. F1000Research, Vol. 10 https://doi.org/10.12688/f1000research.38156.1	journal	April 2021
Seagrass Ecosystem Services and Their Variability across Genera and Geographical Regions Mtwana Nordlund, Lina; Koch, Evamaria W.; Barbier, Edward B. PLOS ONE, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pone.0163091	journal	October 2016
Toward a Coordinated Global Observing System for Seagrasses and Marine Macroalgae Duffy, J. Emmett; Benedetti-Cecchi, Lisandro; Trinanes, Joaquin Frontiers in Marine Science, Vol. 6 https://doi.org/10.3389/fmars.2019.00317	journal	July 2019
The Plant Circadian Oscillator McClung, C. Biology, Vol. 8, Issue 1 https://doi.org/10.3390/biology8010014	journal	March 2019
Sulphated Flavonoids: Biosynthesis, Structures, and Biological Activities Teles, Yanna; Souza, Maria; Souza, Maria Molecules, Vol. 23, Issue 2 https://doi.org/10.3390/molecules23020480	journal	February 2018
Evolutionary History of the Monocot Flower¹ Remizowa, Margarita V.; Sokoloff, Dmitry D.; Rudall, P. J. Annals of the Missouri Botanical Garden, Vol. 97, Issue 4 https://doi.org/10.3417/2009142	journal	December 2010
Mechanisms of bicarbonate use influence the photosynthetic carbon dioxide sensitivity of tropical seagrasses Campbell, Justin E.; Fourqurean, James W. Limnology and Oceanography, Vol. 58, Issue 3 https://doi.org/10.4319/lo.2013.58.3.0839	journal	May 2013

Similar Records

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

Journal Article · Tue Jan 26 19:00:00 EST 2016 · Nature (London) · OSTI ID:1616045

Surface chemical defence of the eelgrass Zostera marina against microbial foulers

Journal Article · Mon Feb 25 19:00:00 EST 2019 · Scientific Reports · OSTI ID:1542435

Cadmium effects on oxidative metabolism in a marine seagrass: Posidonia oceanica

Journal Article · Wed Jan 31 23:00:00 EST 1996 · Bulletin of Environmental Contamination and Toxicology · OSTI ID:223895

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Seagrass genomes reveal ancient polyploidy and adaptations to the marine environment

Citation Formats

References (128)

Similar Records

Related Subjects