Seagrass genomes reveal ancient polyploidy and adaptations to the marine environment.

Journal

Nature plants

ISSN: 2055-0278

Titre abrégé: Nat Plants

Pays: England

ID NLM: 101651677

Informations de publication

Date de publication:
26 Jan 2024

Historique:

received: 31 03 2023

accepted: 05 12 2023

medline: 27 1 2024

pubmed: 27 1 2024

entrez: 26 1 2024

Statut: aheadofprint

Résumé

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.

Identifiants

DOI: 10.1038/s41477-023-01608-5 PMID: 38278954

pubmed: 38278954

doi: 10.1038/s41477-023-01608-5

pii: 10.1038/s41477-023-01608-5

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Subventions

Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)

ID : No. 833522

Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)

ID : 497665889

Informations de copyright

Références

Green, E. P. & Short, F. T. World Atlas of Seagrasses: Prepared by the UNEP World Conservation Monitoring Centre 48–58 (Univ. California Press, 2003).

Short, F., Carruthers, T., Dennison, W. & Waycott, M. Global seagrass distribution and diversity: a bioregional model. J. Exp. Mar. Biol. Ecol. 350, 3–20 (2007).

doi: 10.1016/j.jembe.2007.06.012

Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinform. 10, 421 (2009).

doi: 10.1186/1471-2105-10-421

McKenzie, L. J. et al. The global distribution of seagrass meadows. Environ. Res. Lett. 15, 074041 (2020).

doi: 10.1088/1748-9326/ab7d06

Duffy, J. E. et al. Toward a coordinated global observing system for seagrasses and marine macroalgae. Front. Mar. Sci. 6, 317 (2019).

doi: 10.3389/fmars.2019.00317

Gallagher, A. J. et al. Tiger sharks support the characterization of the world’s largest seagrass ecosystem. Nat. Commun. 13, 6328 (2022).

pubmed: 36319621 pmcid: 9626626 doi: 10.1038/s41467-022-33926-1

Bertelli, C. M. & Unsworth, R. K. F. Protecting the hand that feeds us: seagrass (Zostera marina) serves as commercial juvenile fish habitat. Mar. Pollut. Bull. 83, 425–429 (2014).

pubmed: 23998854 doi: 10.1016/j.marpolbul.2013.08.011

Nordlund, L., Koch, E., Barbier, E. & Creed, J. Seagrass ecosystem services and their variability across genera and geographical regions. PLoS ONE 11, e0163091 (2016).

doi: 10.1371/journal.pone.0163091

Unsworth, R. K. F., Cullen-Unsworth, L. C., Jones, B. L. H. & Lilley, R. J. The planetary role of seagrass conservation. Science 377, 609–613 (2022).

pubmed: 35926055 doi: 10.1126/science.abq6923

Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl Acad. Sci. USA 106, 12377–12381 (2009).

pubmed: 19587236 pmcid: 2707273 doi: 10.1073/pnas.0905620106

Reusch, T. B. H. et al. Lower Vibrio spp. abundances in Zostera marina leaf canopies suggest a novel ecosystem function for temperate seagrass beds. Mar. Biol. 168, 149 (2021).

doi: 10.1007/s00227-021-03963-3

Sievers, M. et al. The role of vegetated coastal wetlands for marine megafauna conservation. Trends Ecol. Evol. 34, 807–817 (2019).

pubmed: 31126633 doi: 10.1016/j.tree.2019.04.004

Duarte, C. M., Sintes, T. & Marbà, N. Assessing the CO

doi: 10.1111/1365-2664.12155

Macreadie, P. I. et al. Blue carbon as a natural climate solution. Nat. Rev. Earth Environ. 2, 826–839 (2021).

doi: 10.1038/s43017-021-00224-1

Olsen, J. L. et al. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530, 331–335 (2016).

pubmed: 26814964 doi: 10.1038/nature16548

Chen, L.-Y. et al. Phylogenomic analyses of Alismatales shed light into adaptations to aquatic environments. Mol. Biol. Evol. 39, msac079 (2022).

pubmed: 35438770 pmcid: 9070837 doi: 10.1093/molbev/msac079

Ma, X. et al. Improved chromosome-level genome assembly and annotation of the seagrass, Zostera marina (eelgrass). F1000Res. 10, 289 (2021).

pubmed: 34621505 pmcid: 8482049 doi: 10.12688/f1000research.38156.1

Yu, L. et al. Ocean current patterns drive the worldwide colonization of eelgrass (Zostera marina). Nat. Plants 9, 1207–1220 (2023).

pubmed: 37474781 pmcid: 10435387 doi: 10.1038/s41477-023-01464-3

Dubin, M. J., Mittelsten Scheid, O. & Becker, C. Transposons: a blessing curse. Curr. Opin. Plant Biol. 42, 23–29 (2018).

pubmed: 29453028 doi: 10.1016/j.pbi.2018.01.003

Vicient, C. M. & Casacuberta, J. M. Impact of transposable elements on polyploid plant genomes. Ann. Bot. 120, 195–207 (2017).

pubmed: 28854566 pmcid: 5737689 doi: 10.1093/aob/mcx078

Böse, M., Lüthgens, C., Lee, J. R. & Rose, J. Quaternary glaciations of northern Europe. Quat. Sci. Rev. 44, 1–25 (2012).

doi: 10.1016/j.quascirev.2012.04.017

Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411–424 (2017).

pubmed: 28502977 doi: 10.1038/nrg.2017.26

Murat, F., Armero, A., Pont, C., Klopp, C. & Salse, J. Reconstructing the genome of the most recent common ancestor of flowering plants. Nat. Genet. 49, 490–496 (2017).

pubmed: 28288112 doi: 10.1038/ng.3813

Sensalari, C., Maere, S. & Lohaus, R. ksrates: positioning whole-genome duplications relative to speciation events in KS distributions. Bioinformatics 38, 530–532 (2022).

pubmed: 34406368 doi: 10.1093/bioinformatics/btab602

Zwaenepoel, A. & Van de Peer, Y. Inference of ancient whole-genome duplications and the evolution of gene duplication and loss rates. Mol. Biol. Evol. 36, 1384–1404 (2019).

pubmed: 31004147 doi: 10.1093/molbev/msz088

Arber, A. Water Plants: A Study of Aquatic Angiosperms (Cambridge Univ. Press, 1920).

Den Hartog, C. The Seagrasses of the World (North Holland, 1970).

Harris, B. J., Harrison, C. J., Hetherington, A. M. & Williams, T. A. Phylogenomic evidence for the monophyly of bryophytes and the reductive evolution of stomata. Curr. Biol. 30, 2001–2012.e2002 (2020).

pubmed: 32302587 doi: 10.1016/j.cub.2020.03.048

Shulaev, V., Silverman, P. & Raskin, I. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385, 718–721 (1997).

doi: 10.1038/385718a0

Golicz, A. A. et al. Genome-wide survey of the seagrass Zostera muelleri suggests modification of the ethylene signalling network. J. Exp. Bot. 66, 1489–1498 (2015).

pubmed: 25563969 pmcid: 4339605 doi: 10.1093/jxb/eru510

Sasidharan, R. & Voesenek, L. A. C. J. Ethylene-mediated acclimations to flooding stress. Plant Physiol. 169, 3–12 (2015).

pubmed: 25897003 pmcid: 4577390 doi: 10.1104/pp.15.00387

Hartman, S. et al. Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nat. Commun. 10, 4020 (2019).

pubmed: 31488841 pmcid: 6728379 doi: 10.1038/s41467-019-12045-4

Van de Poel, B., Smet, D. & Van Der Straeten, D. Ethylene and hormonal cross talk in vegetative growth and development. Plant Physiol. 169, 61–72 (2015).

pubmed: 26232489 pmcid: 4577414 doi: 10.1104/pp.15.00724

Sogin, E. M. et al. Sugars dominate the seagrass rhizosphere. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-022-01740-z (2022).

Kuo, J., Cambridge, M. L. & Kirkman, H. in Seagrasses of Australia: Structure, Ecology and Conservation (eds Larkum, A. W. D. et al.) 93–125 (Springer International, 2018).

Barnabas, A. D. & Arnott, H. J. Zostera capensis Setchell: root structure in relation to function. Aquat. Bot. 27, 309–322 (1987).

doi: 10.1016/0304-3770(87)90071-4

Taylor, A. R. A. Studies of the development of Zostera marina L.: II. Germination and seedling development. Can. J. Bot. 35, 477–499 (1957).

doi: 10.1139/b57-042

Zhuo, C. et al. Developmental changes in lignin composition are driven by both monolignol supply and laccase specificity. Sci. Adv. 8, eabm8145 (2022).

pubmed: 35263134 pmcid: 8906750 doi: 10.1126/sciadv.abm8145

Zhao, Q. et al. Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell 25, 3976–3987 (2013).

pubmed: 24143805 pmcid: 3877815 doi: 10.1105/tpc.113.117770

Barros, J. & Dixon, R. A. Plant phenylalanine/tyrosine ammonia-lyases. Trends Plant Sci. 25, 66–79 (2020).

pubmed: 31679994 doi: 10.1016/j.tplants.2019.09.011

Wang, B. et al. 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. N. Phytol. 186, 514–525 (2010).

doi: 10.1111/j.1469-8137.2009.03137.x

Strullu-Derrien, C., Selosse, M.-A., Kenrick, P. & Martin, F. M. The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. N. Phytol. 220, 1012–1030 (2018).

doi: 10.1111/nph.15076

Kohout, P. et al. Surprising spectra of root-associated fungi in submerged aquatic plants. FEMS Microbiol. Ecol. 80, 216–235 (2012).

pubmed: 22224638 doi: 10.1111/j.1574-6941.2011.01291.x

Moora, M. et al. AM fungal communities inhabiting the roots of submerged aquatic plant Lobelia dortmanna are diverse and include a high proportion of novel taxa. Mycorrhiza 26, 735–745 (2016).

pubmed: 27246225 doi: 10.1007/s00572-016-0709-0

Bohrer, K. E., Friese, C. F. & Amon, J. P. Seasonal dynamics of arbuscular mycorrhizal fungi in differing wetland habitats. Mycorrhiza 14, 329–337 (2004).

pubmed: 15015060 doi: 10.1007/s00572-004-0292-7

Nielsen, S. L., Thingstrup, I. & Wigand, C. Apparent lack of vesicular–arbuscular mycorrhiza (VAM) in the seagrasses Zostera marina L. and Thalassia testudinum Banks ex König. Aquat. Bot. 63, 261–266 (1999).

doi: 10.1016/S0304-3770(98)00123-5

Gomez-Roldan, V. et al. Strigolactone inhibition of shoot branching. Nature 455, 189–194 (2008).

pubmed: 18690209 doi: 10.1038/nature07271

Chang, J. et al. The genome of the king protea, Protea cynaroides. Plant J. 113, 262–276 (2023).

pubmed: 36424853 doi: 10.1111/tpj.16044

Liu, Y. et al. An angiosperm NLR atlas reveals that NLR gene reduction is associated with ecological specialization and signal transduction component deletion. Mol. Plant 14, 2015–2031 (2021).

pubmed: 34364002 doi: 10.1016/j.molp.2021.08.001

Scharf, K. D., Berberich, T., Ebersberger, I. & Nover, L. The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta 1819, 104–119 (2012).

pubmed: 22033015 doi: 10.1016/j.bbagrm.2011.10.002

Papazian, S., Parrot, D., Buryskova, B., Weinberger, F. & Tasdemir, D. Surface chemical defence of the eelgrass Zostera marina against microbial foulers. Sci. Rep. 9, 3323 (2019).

pubmed: 30804483 pmcid: 6389981 doi: 10.1038/s41598-019-39212-3

Lamb, J. B. et al. Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science 355, 731–733 (2017).

pubmed: 28209895 doi: 10.1126/science.aal1956

Teles, Y. C. F., Souza, M. S. R. & Souza, M. F. V. Sulphated flavonoids: biosynthesis, structures, and biological activities. Molecules https://doi.org/10.3390/molecules23020480 (2018).

Grignon-Dubois, M. & Rezzonico, B. Phenolic chemistry of the seagrass Zostera noltei Hornem. Part 1: first evidence of three infraspecific flavonoid chemotypes in three distinctive geographical regions. Phytochemistry 146, 91–101 (2018).

pubmed: 29253735 doi: 10.1016/j.phytochem.2017.12.006

Vilas-Boas, C., Sousa, E., Pinto, M. & Correia-da-Silva, M. An antifouling model from the sea: a review of 25 years of zosteric acid studies. Biofouling 33, 927–942 (2017).

pubmed: 29171304 doi: 10.1080/08927014.2017.1391951

van Zelm, E., Zhang, Y. & Testerink, C. Salt tolerance mechanisms of plants. Annu. Rev. Plant Biol. 71, 403–433 (2020).

pubmed: 32167791 doi: 10.1146/annurev-arplant-050718-100005

Gaxiola, R. A. et al. Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc. Natl Acad. Sci. USA 98, 11444–11449 (2001).

pubmed: 11572991 pmcid: 58749 doi: 10.1073/pnas.191389398

Kumar, T., Uzma, M. R. K., Abbas, Z. & Ali, G. M. Genetic improvement of sugarcane for drought and salinity stress tolerance using Arabidopsis vacuolar pyrophosphatase (AVP1) gene. Mol. Biotechnol. 56, 199–209 (2014).

Yang, Y. et al. Overexpression of a Populus trichocarpa H+-pyrophosphatase gene PtVP1.1 confers salt tolerance on transgenic poplar. Tree Physiol. 35, 663–677 (2015).

pubmed: 25877769 doi: 10.1093/treephys/tpv027

Duan, X. G., Yang, A. F., Gao, F., Zhang, S. L. & Zhang, J. R. Heterologous expression of vacuolar H(+)-PPase enhances the electrochemical gradient across the vacuolar membrane and improves tobacco cell salt tolerance. Protoplasma 232, 87–95 (2007).

pubmed: 18094929 doi: 10.1007/s00709-007-0268-5

Nakamura, R. L. & Gaber, R. F. Ion selectivity of the Kat1 K+ channel pore. Mol. Membr. Biol. 26, 293–308 (2009).

pubmed: 19742379 doi: 10.1080/09687680903188332

Morris, E. R., Powell, D. A., Gidley, M. J. & Rees, D. A. Conformations and interactions of pectins. I. Polymorphism between gel and solid states of calcium polygalacturonate. J. Mol. Biol. 155, 507–516 (1982).

pubmed: 7086901 doi: 10.1016/0022-2836(82)90484-3

Gloaguen, V. et al. Structural characterization and cytotoxic properties of an apiose-rich pectic polysaccharide obtained from the cell wall of the marine phanerogam Zostera marina. J. Nat. Prod. 73, 1087–1092 (2010).

pubmed: 20465284 doi: 10.1021/np100092c

Byrt, C. S., Munns, R., Burton, R. A., Gilliham, M. & Wege, S. Root cell wall solutions for crop plants in saline soils. Plant Sci. 269, 47–55 (2018).

pubmed: 29606216 doi: 10.1016/j.plantsci.2017.12.012

Mølhøj, M., Verma, R. & Reiter, W. D. 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. Plant J. 35, 693–703 (2003).

pubmed: 12969423 doi: 10.1046/j.1365-313X.2003.01841.x

Xu, S. et al. The origin, diversification and adaptation of a major mangrove clade (Rhizophoreae) revealed by whole-genome sequencing. Natl Sci. Rev. 4, 721–734 (2017).

pubmed: 31258950 doi: 10.1093/nsr/nwx065

Natarajan, P. et al. A reference-grade genome identifies salt-tolerance genes from the salt-secreting mangrove species Avicennia marina. Commun. Biol. 4, 851 (2021).

pubmed: 34239036 pmcid: 8266904 doi: 10.1038/s42003-021-02384-8

Dolferus, R. et al. Functional analysis of lactate dehydrogenase during hypoxic stress in Arabidopsis. Funct. Plant Biol. 35, 131–140 (2008).

pubmed: 32688764 doi: 10.1071/FP07228

Baena-González, E., Rolland, F., Thevelein, J. M. & Sheen, J. A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938–942 (2007).

pubmed: 17671505 doi: 10.1038/nature06069

Cho, H.-Y., Lu, M.-Y. J. & Shih, M.-C. The SnRK1–eIFiso4G1 signaling relay regulates the translation of specific mRNAs in Arabidopsis under submergence. N. Phytol. 222, 366–381 (2019).

doi: 10.1111/nph.15589

Monteiro, F. M., Pancost, R. D., Ridgwell, A. & Donnadieu, Y. Nutrients as the dominant control on the spread of anoxia and euxinia across the Cenomanian–Turonian oceanic anoxic event (OAE2): model–data comparison. Paleoceanography https://doi.org/10.1029/2012PA002351 (2012).

Selby, D., Mutterlose, J. & Condon, D. J. 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. Chem. Geol. 265, 394–409 (2009).

doi: 10.1016/j.chemgeo.2009.05.005

Kirk, J. T. O. Light and Photosynthesis in Aquatic Ecosystems 3rd edn (Cambridge University Press, 2010).

Campbell, J. E. & Fourqurean, J. W. Mechanisms of bicarbonate use influence the photosynthetic carbon dioxide sensitivity of tropical seagrasses. Limnol. Oceanogr. 58, 839–848 (2013).

doi: 10.4319/lo.2013.58.3.0839

Capó-Bauçà, S., Iñiguez, C., Aguiló-Nicolau, P. & Galmés, J. Correlative adaptation between Rubisco and CO

pubmed: 35729266 doi: 10.1038/s41477-022-01171-5

Rubio, L. et al. Direct uptake of HCO

pubmed: 28815648 doi: 10.1111/pce.13057

Larkum, A. W. D., Davey, P. A., Kuo, J., Ralph, P. J. & Raven, J. A. Carbon-concentrating mechanisms in seagrasses. J. Exp. Bot. 68, 3773–3784 (2017).

pubmed: 28911056 doi: 10.1093/jxb/erx206

Koch, M., Bowes, G., Ross, C. & Zhang, X.-H. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Change Biol. 19, 103–132 (2013).

doi: 10.1111/j.1365-2486.2012.02791.x

Chen, S., Peng, W., Ansah, E. O., Xiong, F. & Wu, Y. Encoded C

pubmed: 36102341 pmcid: 9481101 doi: 10.1080/15592324.2022.2115634

Han, X. et al. Origin and evolution of core components responsible for monitoring light environment changes during plant terrestrialization. Mol. Plant 12, 847–862 (2019).

pubmed: 31009752 doi: 10.1016/j.molp.2019.04.006

McClung, C. R. The plant circadian oscillator. Biology 8, 14 (2019).

pubmed: 30870980 pmcid: 6466001 doi: 10.3390/biology8010014

Mohr, W. et al. Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium. Nature 600, 105–109 (2021).

pubmed: 34732889 pmcid: 8636270 doi: 10.1038/s41586-021-04063-4

Tarquinio, F. et al. Microorganisms facilitate uptake of dissolved organic nitrogen by seagrass leaves. ISME J. 12, 2796–2800 (2018).

pubmed: 29977008 pmcid: 6194017 doi: 10.1038/s41396-018-0218-6

Kuo, J. & Hartog, C. D. in Seagrasses: Biology, Ecology and Conservation (eds Larkum, A. W. D. et al.) 51–87 (Springer Netherlands, 2006).

Krizek, B. A. & Fletcher, J. C. Molecular mechanisms of flower development: an armchair guide. Nat. Rev. Genet. 6, 688–698 (2005).

pubmed: 16151374 doi: 10.1038/nrg1675

Lohmann, J. U. & Weigel, D. Building beauty: the genetic control of floral patterning. Dev. Cell 2, 135–142 (2002).

pubmed: 11832239 doi: 10.1016/S1534-5807(02)00122-3

Remizowa, M. V., Sokoloff, D. D. & Rudall, P. J. Evolutionary history of the monocot flower. Ann. Mo. Bot. Gard. 97, 617–645 (2010).

doi: 10.3417/2009142

Ackerman, J. D. in Seagrasses: Biology, Ecology and Conservation (eds Larkum, A. W. D. et al.) 89–109 (Springer Netherlands, 2006).

Orth, R. J. et al. Restoration of seagrass habitat leads to rapid recovery of coastal ecosystem services. Sci. Adv. https://doi.org/10.1126/sciadv.abc6434 (2020).

Cook, C. D. K. The number and kinds of embryo-bearing plants which have become aquatic: a survey. Perspect. Plant Ecol. Evol. Syst. 2, 79–102 (1999).

doi: 10.1078/1433-8319-00066

Waycott, M., Biffin, E. & Les, D. H. in Seagrasses of Australia: Structure, Ecology and Conservation (eds Larkum, A. W. D. et al.) 129–154 (Springer International, 2018).

Pazzaglia, J., Reusch, T. B. H., Terlizzi, A., Marín-Guirao, L. & Procaccini, G. Phenotypic plasticity under rapid global changes: the intrinsic force for future seagrasses survival. Evol. Appl. 14, 1181–1201 (2021).

pubmed: 34025759 pmcid: 8127715 doi: 10.1111/eva.13212

Flowers, T. J., Galal, H. K. & Bromham, L. Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct. Plant Biol. 37, 604–612 (2010).

doi: 10.1071/FP09269

Doyle, J. J. & Doyle, J. L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11–15 (1987).

Dudchenko, O. et al. The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000. Preprint at bioRxiv https://doi.org/10.1101/254797 (2018).

Cheng, H., Concepcion, G. T., Feng, X., Zhang, H. & Li, H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat. Methods 18, 170–175 (2021).

pubmed: 33526886 pmcid: 7961889 doi: 10.1038/s41592-020-01056-5

Chen, Z. et al. 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. Genome Res. 30, 898–909 (2020).

Yeo, S., Coombe, L., Warren, R. L., Chu, J. & Birol, I. ARCS: scaffolding genome drafts with linked reads. Bioinformatics 34, 725–731 (2018).

pubmed: 29069293 doi: 10.1093/bioinformatics/btx675

Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).

pubmed: 31375807 pmcid: 7605509 doi: 10.1038/s41587-019-0201-4

Kovaka, S. et al. Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biol. 20, 278 (2019).

pubmed: 31842956 pmcid: 6912988 doi: 10.1186/s13059-019-1910-1

Wu, T. D. & Watanabe, C. K. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21, 1859–1875 (2005).

pubmed: 15728110 doi: 10.1093/bioinformatics/bti310

Bruna, T., Hoff, K. J., Lomsadze, A., Stanke, M. & Borodovsky, M. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genom. Bioinform. 3, lqaa108 (2021).

pubmed: 33575650 pmcid: 7787252 doi: 10.1093/nargab/lqaa108

Keilwagen, J., Hartung, F. & Grau, J. GeMoMa: homology-based gene prediction utilizing intron position conservation and RNA-seq data. Methods Mol. Biol. 1962, 161–177 (2019).

pubmed: 31020559 doi: 10.1007/978-1-4939-9173-0_9

Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7 (2008).

pubmed: 18190707 pmcid: 2395244 doi: 10.1186/gb-2008-9-1-r7

Seppey, M., Manni, M. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness. Methods Mol. Biol. 1962, 227–245 (2019).

pubmed: 31020564 doi: 10.1007/978-1-4939-9173-0_14

Abeel, T., Van Parys, T., Saeys, Y., Galagan, J. & Van de Peer, Y. GenomeView: a next-generation genome browser. Nucleic Acids Res. 40, e12 (2012).

pubmed: 22102585 doi: 10.1093/nar/gkr995

Quevillon, E. et al. InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116–W120 (2005).

pubmed: 15980438 pmcid: 1160203 doi: 10.1093/nar/gki442

Nordberg, H. et al. The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res. 42, D26–D31 (2014).

pubmed: 24225321 doi: 10.1093/nar/gkt1069

Nawrocki, E. P. & Eddy, S. R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933–2935 (2013).

pubmed: 24008419 pmcid: 3810854 doi: 10.1093/bioinformatics/btt509

Kalvari, I. et al. Rfam 14: expanded coverage of metagenomic, viral and microRNA families. Nucleic Acids Res. 49, D192–D200 (2021).

pubmed: 33211869 doi: 10.1093/nar/gkaa1047

UniProt Consortium. UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res. 49, D480–D489 (2021).

doi: 10.1093/nar/gkaa1100

Gremme, G., Steinbiss, S. & Kurtz, S. GenomeTools: a comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Trans. Comput. Biol. Bioinform. 10, 645–656 (2013).

pubmed: 24091398 doi: 10.1109/TCBB.2013.68

Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

pubmed: 20110278 pmcid: 2832824 doi: 10.1093/bioinformatics/btq033

Benson, D. A. et al. GenBank. Nucleic Acids Res. 41, D36–D42 (2013).

pubmed: 23193287 doi: 10.1093/nar/gks1195

Xu, Z. & Wang, H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, W265–W268 (2007).

pubmed: 17485477 pmcid: 1933203 doi: 10.1093/nar/gkm286

Ellinghaus, D., Kurtz, S. & Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinform. 9, 18 (2008).

doi: 10.1186/1471-2105-9-18

Ou, S. & Jiang, N. LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. 176, 1410–1422 (2017).

pubmed: 29233850 pmcid: 5813529 doi: 10.1104/pp.17.01310

Yan, H., Bombarely, A. & Li, S. DeepTE: a computational method for de novo classification of transposons with convolutional neural network. Bioinformatics 36, 4269–4275 (2020).

pubmed: 32415954 doi: 10.1093/bioinformatics/btaa519

Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).

pubmed: 20709691 doi: 10.1093/bioinformatics/btq461

Ma, J. & Bennetzen, J. L. Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl Acad. Sci. USA 101, 12404–12410 (2004).

pubmed: 15240870 pmcid: 515075 doi: 10.1073/pnas.0403715101

Zwaenepoel, A. & Van de Peer, Y. wgd—simple command line tools for the analysis of ancient whole-genome duplications. Bioinformatics 35, 2153–2155 (2019).

pubmed: 30398564 doi: 10.1093/bioinformatics/bty915

Proost, S. et al. i-ADHoRe 3.0—fast and sensitive detection of genomic homology in extremely large data sets. Nucleic Acids Res. 40, e11 (2012).

pubmed: 22102584 doi: 10.1093/nar/gkr955

Sensalari, C., Maere, S. & Lohaus, R. ksrates: positioning whole-genome duplications relative to speciation events in KS distributions. Bioinformatics https://doi.org/10.1093/bioinformatics/btab602 (2021).

Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).

pubmed: 31727128 pmcid: 6857279 doi: 10.1186/s13059-019-1832-y

Löytynoja, A. & Goldman, N. An algorithm for progressive multiple alignment of sequences with insertions. Proc. Natl Acad. Sci. USA 102, 10557–10562 (2005).

pubmed: 16000407 pmcid: 1180752 doi: 10.1073/pnas.0409137102

Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001).

pubmed: 11524383 doi: 10.1093/bioinformatics/17.8.754

Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

pubmed: 17483113 doi: 10.1093/molbev/msm088

An, D. et al. Plant evolution and environmental adaptation unveiled by long-read whole-genome sequencing of Spirodela. Proc. Natl Acad. Sci. USA 116, 18893–18899 (2019).

pubmed: 31484765 pmcid: 6754600 doi: 10.1073/pnas.1910401116

O’Brien, K. P., Remm, M. & Sonnhammer, E. L. Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res. 33, D476–D480 (2005).

pubmed: 15608241 doi: 10.1093/nar/gki107

Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

pubmed: 22367748 pmcid: 3408070 doi: 10.1093/molbev/mss075

Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).

pubmed: 26243257 pmcid: 4531804 doi: 10.1186/s13059-015-0721-2

Rozewicki, J., Li, S., Amada, K. M., Standley, D. M. & Katoh, K. MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res. 47, W5–W10 (2019).

pubmed: 31062021 pmcid: 6602451

Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

pubmed: 19505945 pmcid: 2712344 doi: 10.1093/bioinformatics/btp348

Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).

pubmed: 32011700 pmcid: 7182206 doi: 10.1093/molbev/msaa015

Wang, Y. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49 (2012).

pubmed: 22217600 pmcid: 3326336 doi: 10.1093/nar/gkr1293

Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009).

pubmed: 19541911 pmcid: 2752132 doi: 10.1101/gr.092759.109