{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T14:25:07Z","timestamp":1788272707265,"version":"build-2803163510"},"reference-count":63,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,3,11]],"date-time":"2024-03-11T00:00:00Z","timestamp":1710115200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,3,11]],"date-time":"2024-03-11T00:00:00Z","timestamp":1710115200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100003627","name":"Rural Development Administration","doi-asserted-by":"publisher","award":["PJ01627602"],"award-info":[{"award-number":["PJ01627602"]}],"id":[{"id":"10.13039\/501100003627","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Lemnoideae, commonly referred to as the duckweed, are aquatic plants found worldwide. <jats:italic>Wolffia<\/jats:italic> species are known for their extreme reduction in size and complexity, lacking both roots and leaves, and they hold the distinction of being the smallest plants among angiosperms. Interestingly, it belongs to the Araceae family, despite its apparent morphological differences from land plants in the same family. Traditional morphological methods have limitations in classifying these plants, making molecular-level information essential. The chloroplast genome of <jats:italic>Wolffia arrhiza<\/jats:italic> is revealed that a total length of 169,602\u00a0bp and a total GC content of 35.78%. It follows the typical quadripartite structure, which includes a large single copy (LSC, 92,172\u00a0bp) region, a small single copy (SSC, 13,686\u00a0bp) region, and a pair of inverted repeat (IR, 31,872\u00a0bp each) regions. There are 131 genes characterized, comprising 86 Protein-Coding Genes, 37 Transfer RNA (tRNA) genes, and 8 ribosomal RNA (rRNA) genes. Moreover, 48 simple sequence repeats and 32 long repeat sequences were detected. Comparative analysis between <jats:italic>W. arrhiza<\/jats:italic> and six other Lemnoideae species identified 12 hotspots of high nucleotide diversity. In addition, a phylogenetic analysis was performed using 14 species belonging to the Araceae family and one external species as an outgroup. This analysis unveiled <jats:italic>W<\/jats:italic>. <jats:italic>arrhiza<\/jats:italic> and <jats:italic>Wolffia globosa<\/jats:italic> as closely related sister species. Therefore, this research has revealed the complete chloroplast genome data of <jats:italic>W<\/jats:italic>. <jats:italic>arrhiza<\/jats:italic>, offering a more detailed understanding of its evolutionary position and phylogenetic categorization within the Lemnoideae subfamily.<\/jats:p>","DOI":"10.1038\/s41598-024-56394-7","type":"journal-article","created":{"date-parts":[[2024,3,11]],"date-time":"2024-03-11T09:01:55Z","timestamp":1710147715000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Characterization of the complete chloroplast genome of Wolffia arrhiza and comparative genomic analysis with relative Wolffia species"],"prefix":"10.1038","volume":"14","author":[{"given":"Halim","family":"Park","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin Hwa","family":"Park","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang Jae","family":"Kang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,3,11]]},"reference":[{"key":"56394_CR1","unstructured":"Landolt, E. Biosystematic investigations in the family of duckweeds (Lemnaceae). II: The family of Lemnaceae: a monographic study. 1. Ver\u00f6ffentlichungen des Geobotanischen Institutes der ETH, Stiftung R\u00fcbel, Z\u00fcrich (1986)."},{"key":"56394_CR2","unstructured":"Landolt, E. Taxonomy and ecology of the section Wolffia of the genus Wolffia (Lemnaceae). Ber. Geobot. Inst. ETH, Stiftung R\u00fcbel, Z\u00fcrich 60, 137\u2013151 (1994)."},{"key":"56394_CR3","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1007\/s10750-014-2014-2","volume":"743","author":"Y Xu","year":"2015","unstructured":"Xu, Y. et al. Species distribution, genetic diversity and barcoding in the duckweed family (Lemnaceae). Hydrobiologia 743, 75\u201387 (2015).","journal-title":"Hydrobiologia"},{"key":"56394_CR4","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1002\/clen.200800210","volume":"37","author":"JJ Cheng","year":"2009","unstructured":"Cheng, J. J. & Stomp, A. M. Growing duckweed to recover nutrients from wastewaters and for production of fuel ethanol and animal feed. Clean-Soil Air Water 37, 17\u201326 (2009).","journal-title":"Clean-Soil Air Water"},{"key":"56394_CR5","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1002\/tax.12188","volume":"69","author":"M Bog","year":"2020","unstructured":"Bog, M. et al. A taxonomic revision of Lemna sect: Uninerves (Lemnaceae). Taxon 69, 56\u201366 (2020).","journal-title":"Taxon"},{"key":"56394_CR6","doi-asserted-by":"publisher","DOI":"10.1111\/njb.02658","author":"M Bog","year":"2020","unstructured":"Bog, M. et al. Key to the determination of taxa of Lemnaceae: An update. Nordic J. Botany https:\/\/doi.org\/10.1111\/njb.02658 (2020).","journal-title":"Nordic J. Botany"},{"key":"56394_CR7","doi-asserted-by":"publisher","DOI":"10.1201\/9781315166339","volume-title":"Aquatic Monocotyledons of North America: Ecology, Life History, and Systematics","author":"DH Les","year":"2020","unstructured":"Les, D. H. Aquatic Monocotyledons of North America: Ecology, Life History, and Systematics (CRC Press, 2020)."},{"key":"56394_CR8","first-page":"221","volume":"27","author":"DH Les","year":"2002","unstructured":"Les, D. H. et al. Phylogeny and systematics of Lemnaceae, the duckweed family. Syst. Botany 27, 221\u2013240 (2002).","journal-title":"Syst. Botany"},{"key":"56394_CR9","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1111\/plb.12203","volume":"17","author":"N Tippery","year":"2015","unstructured":"Tippery, N. et al. Evaluation of phylogenetic relationships in Lemnaceae using nuclear ribosomal data. Plant Biol. 17, 50\u201358 (2015).","journal-title":"Plant Biol."},{"key":"56394_CR10","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1007\/BF00989203","volume":"204","author":"DH Les","year":"1997","unstructured":"Les, D. H. et al. Systematics of the Lemnaceae (duckweeds): Inferences from micromolecular and morphological data. Plant Syst. Evol. 204, 161\u2013177 (1997).","journal-title":"Plant Syst. Evol."},{"key":"56394_CR11","unstructured":"Pan, S. & Chen, S. Morphology of Wolffia arrhiza: a scanning electron microscopic study. Botanical bulletin of Academia Sinica. New series (1979)."},{"key":"56394_CR12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3724\/SP.J.1145.2013.00001","volume":"19","author":"KJ Appenroth","year":"2013","unstructured":"Appenroth, K. J. et al. Telling duckweed apart: Genotyping technologies for the Lemnaceae. Chin. J. Appl. Environ. Biol 19, 1\u201310 (2013).","journal-title":"Chin. J. Appl. Environ. Biol"},{"key":"56394_CR13","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12870-021-03165-5","volume":"21","author":"J Yang","year":"2021","unstructured":"Yang, J. et al. Frond architecture of the rootless duckweed Wolffia globosa. BMC Plant Biol. 21, 1\u201310 (2021).","journal-title":"BMC Plant Biol."},{"key":"56394_CR14","unstructured":"Iqbal, S. Duckweed aquaculture. Potentials, possibilities and limitations for combined wastewater treatment and animal feed production in developing countries. SAn-DEC Report (1999)."},{"key":"56394_CR15","volume-title":"Duckweed Aquaculture: A New Aquatic Farming System for Developing Countries","author":"P Skillicorn","year":"1993","unstructured":"Skillicorn, P. et al. Duckweed Aquaculture: A New Aquatic Farming System for Developing Countries (World Bank, 1993)."},{"key":"56394_CR16","first-page":"129","volume":"22","author":"M Ansal","year":"2010","unstructured":"Ansal, M. et al. Duckweed based bio-remediation of village ponds: An ecologically and economically viable integrated approach for rural development through aquaculture. Livestock Res. Rural Dev. 22, 129 (2010).","journal-title":"Livestock Res. Rural Dev."},{"key":"56394_CR17","volume-title":"Encyclopedia of Ecology","author":"SE Jorgensen","year":"2008","unstructured":"Jorgensen, S. E. & Fath, B. D. Encyclopedia of Ecology (Elsevier, 2008)."},{"key":"56394_CR18","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1016\/S1389-1723(99)89012-4","volume":"87","author":"M Fujita","year":"1999","unstructured":"Fujita, M. et al. Nutrient removal and starch production through cultivation of Wolffia arrhiza. J. Biosci. Bioeng. 87, 194\u2013198 (1999).","journal-title":"J. Biosci. Bioeng."},{"key":"56394_CR19","first-page":"677","volume":"12","author":"R Czerpak","year":"2003","unstructured":"Czerpak, R. & Szamrej, I. The effect of \u03b2-estradiol and corticosteroids on chlorophylls and carotenoids content in Wolffia arrhiza (L.) Wimm.(Lemnaceae growing in municipal Bialystok tap Tap T water. Pol. J. Environ. Stud. 12, 677 (2003).","journal-title":"Pol. J. Environ. Stud."},{"key":"56394_CR20","doi-asserted-by":"publisher","first-page":"1583","DOI":"10.2134\/jeq2003.1583","volume":"32","author":"S K\u00f6rner","year":"2003","unstructured":"K\u00f6rner, S. et al. The capacity of duckweed to treat wastewater: ecological considerations for a sound design. J. Environ. Qual. 32, 1583\u20131590 (2003).","journal-title":"J. Environ. Qual."},{"key":"56394_CR21","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1038\/232495a0","volume":"232","author":"K Bhanthumnavin","year":"1971","unstructured":"Bhanthumnavin, K. & Mcgarry, M. G. Wolffia arrhiza as a possible source of inexpensive protein. Nature 232, 495\u2013495 (1971).","journal-title":"Nature"},{"key":"56394_CR22","unstructured":"Chareontesprasit, N. & Jiwyam, W. An evaluation of Wolffia meal (Wolffia arrhiza) in replacing soybean meal in some formulated rations of Nile tilapia (Oreochromis niloticus L.). (2001)."},{"key":"56394_CR23","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2229-10-205","volume":"10","author":"W Wang","year":"2010","unstructured":"Wang, W. et al. DNA barcoding of the Lemnaceae, a family of aquatic monocots. BMC Plant Biol. 10, 1\u201311 (2010).","journal-title":"BMC Plant Biol."},{"key":"56394_CR24","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1111\/plb.12229","volume":"17","author":"N Borisjuk","year":"2015","unstructured":"Borisjuk, N. et al. Assessment, validation and deployment strategy of a two-barcode protocol for facile genotyping of duckweed species. Plant Biol. 17, 42\u201349 (2015).","journal-title":"Plant Biol."},{"key":"56394_CR25","doi-asserted-by":"publisher","first-page":"117","DOI":"10.3389\/fsufs.2019.00117","volume":"3","author":"M Bog","year":"2019","unstructured":"Bog, M. et al. Duckweed (Lemnaceae): Its molecular taxonomy. Front. Sustain. Food Syst. 3, 117 (2019).","journal-title":"Front. Sustain. Food Syst."},{"key":"56394_CR26","doi-asserted-by":"crossref","unstructured":"Palmer, J. D. et al. Chloroplast DNA variation and plant phylogeny. Ann. Missouri Botanical Garden, 1180\u20131206 (1988).","DOI":"10.2307\/2399279"},{"key":"56394_CR27","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1111\/brv.12104","volume":"90","author":"X Li","year":"2015","unstructured":"Li, X. et al. Plant DNA barcoding: From gene to genome. Biol. Rev. 90, 157\u2013166 (2015).","journal-title":"Biol. Rev."},{"key":"56394_CR28","doi-asserted-by":"publisher","first-page":"938","DOI":"10.1111\/j.1469-8137.2012.04220.x","volume":"195","author":"L Nauheimer","year":"2012","unstructured":"Nauheimer, L. et al. Global history of the ancient monocot family Araceae inferred with models accounting for past continental positions and previous ranges based on fossils. New Phytol. 195, 938\u2013950 (2012).","journal-title":"New Phytol."},{"key":"56394_CR29","doi-asserted-by":"crossref","unstructured":"Les, D. H. & Crawford, D. J. Landoltia (Lemnaceae), a new genus of duckweeds. Novon, 530\u2013533 (1999).","DOI":"10.2307\/3392157"},{"key":"56394_CR30","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1007\/s00239-008-9091-7","volume":"66","author":"AV Mardanov","year":"2008","unstructured":"Mardanov, A. V. et al. Complete sequence of the duckweed (Lemna minor) chloroplast genome: Structural organization and phylogenetic relationships to other angiosperms. J. Mol. Evol. 66, 555\u2013564 (2008).","journal-title":"J. Mol. Evol."},{"key":"56394_CR31","doi-asserted-by":"publisher","first-page":"609729","DOI":"10.3389\/fpls.2021.609729","volume":"12","author":"Y-Y Guo","year":"2021","unstructured":"Guo, Y.-Y. et al. Chloroplast genomes of two species of Cypripedium: Expanded genome size and proliferation of AT-biased repeat sequences. Front. Plant Sci. 12, 609729 (2021).","journal-title":"Front. Plant Sci."},{"key":"56394_CR32","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1007\/BF00175818","volume":"41","author":"BR Morton","year":"1995","unstructured":"Morton, B. R. & Clegg, M. T. Neighboring base composition is strongly correlated with base substitution bias in a region of the chloroplast genome. J. Mol. Evol. 41, 597\u2013603 (1995).","journal-title":"J. Mol. Evol."},{"key":"56394_CR33","doi-asserted-by":"crossref","unstructured":"Morton, B. R. The influence of neighboring base composition on substitutions in plant chloroplast coding sequences. (1997).","DOI":"10.1093\/oxfordjournals.molbev.a025752"},{"key":"56394_CR34","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1016\/j.ijbiomac.2020.02.201","volume":"152","author":"R-S Zhang","year":"2020","unstructured":"Zhang, R.-S. et al. A high level of chloroplast genome sequence variability in the Sawtooth Oak Quercus acutissima. Int. J. Biol. Macromol. 152, 340\u2013348 (2020).","journal-title":"Int. J. Biol. Macromol."},{"key":"56394_CR35","doi-asserted-by":"publisher","first-page":"e8251","DOI":"10.7717\/peerj.8251","volume":"8","author":"Z Wang","year":"2020","unstructured":"Wang, Z. et al. Comparative analysis of codon usage patterns in chloroplast genomes of six Euphorbiaceae species. PeerJ 8, e8251 (2020).","journal-title":"PeerJ"},{"key":"56394_CR36","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1093\/molbev\/mst261","volume":"31","author":"S Wicke","year":"2014","unstructured":"Wicke, S. et al. Disproportional plastome-wide increase of substitution rates and relaxed purifying selection in genes of carnivorous Lentibulariaceae. Mol. Biol. Evol. 31, 529\u2013545 (2014).","journal-title":"Mol. Biol. Evol."},{"key":"56394_CR37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12870-022-03529-5","volume":"22","author":"H Jiang","year":"2022","unstructured":"Jiang, H. et al. Comparative and phylogenetic analyses of six Kenya Polystachya (Orchidaceae) species based on the complete chloroplast genome sequences. BMC Plant Biol. 22, 1\u201321 (2022).","journal-title":"BMC Plant Biol."},{"key":"56394_CR38","doi-asserted-by":"publisher","first-page":"1854","DOI":"10.3389\/fpls.2017.01854","volume":"8","author":"Y Song","year":"2017","unstructured":"Song, Y. et al. Development of chloroplast genomic resources for Oryza species discrimination. Front. Plant Sci. 8, 1854 (2017).","journal-title":"Front. Plant Sci."},{"key":"56394_CR39","doi-asserted-by":"publisher","first-page":"275","DOI":"10.3732\/ajb.94.3.275","volume":"94","author":"J Shaw","year":"2007","unstructured":"Shaw, J. et al. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. Am. J. Botany 94, 275\u2013288 (2007).","journal-title":"Am. J. Botany"},{"key":"56394_CR40","doi-asserted-by":"publisher","first-page":"206","DOI":"10.1007\/BF00279998","volume":"232","author":"J Tsudzuki","year":"1992","unstructured":"Tsudzuki, J. et al. Chloroplast DNA of black pine retains a residual inverted repeat lacking rRNA genes: Nucleotide sequences of trnQ, trnK, psbA, trnI and trnH and the absence of rps16. Mol. Gener. Genet. MGG 232, 206\u2013214 (1992).","journal-title":"Mol. Gener. Genet. MGG"},{"key":"56394_CR41","doi-asserted-by":"publisher","first-page":"374","DOI":"10.1093\/gbe\/evs021","volume":"4","author":"C-P Lin","year":"2012","unstructured":"Lin, C.-P. et al. The complete chloroplast genome of Ginkgo biloba reveals the mechanism of inverted repeat contraction. Genome Biol. Evol. 4, 374\u2013381 (2012).","journal-title":"Genome Biol. Evol."},{"key":"56394_CR42","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1007\/BF00223797","volume":"79","author":"E White","year":"1990","unstructured":"White, E. Chloroplast DNA in Pinus monticola: 1 Physical map. Theor. Appl. Genet. 79, 119\u2013124 (1990).","journal-title":"Theor. Appl. Genet."},{"key":"56394_CR43","doi-asserted-by":"publisher","first-page":"73","DOI":"10.3389\/fgene.2020.00073","volume":"11","author":"C Li","year":"2020","unstructured":"Li, C. et al. Initial characterization of the chloroplast genome of Vicia sepium, an important wild resource plant, and related inferences about its evolution. Front. Genet. 11, 73 (2020).","journal-title":"Front. Genet."},{"key":"56394_CR44","doi-asserted-by":"publisher","first-page":"1394","DOI":"10.1101\/gr.2289704","volume":"14","author":"AC Darling","year":"2004","unstructured":"Darling, A. C. et al. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394\u20131403 (2004).","journal-title":"Genome Res."},{"key":"56394_CR45","first-page":"257","volume":"27","author":"CA Butterworth","year":"2002","unstructured":"Butterworth, C. A. et al. Molecular systematics of tribe Cacteae (Cactaceae: Cactoideae): A phylogeny based on rpl16 intron sequence variation. Syst. Botany 27, 257\u2013270 (2002).","journal-title":"Syst. Botany"},{"key":"56394_CR46","doi-asserted-by":"publisher","first-page":"385","DOI":"10.1006\/mpev.1997.0432","volume":"8","author":"SA Kelchner","year":"1997","unstructured":"Kelchner, S. A. & Clark, L. G. Molecular evolution and phylogenetic utility of the chloroplast rpl16 intron in Chusquea and the Bambusoideae (poaceae). Mol. Phylogen. Evol. 8, 385\u2013397 (1997).","journal-title":"Mol. Phylogen. Evol."},{"key":"56394_CR47","doi-asserted-by":"publisher","first-page":"273","DOI":"10.2307\/2656915","volume":"87","author":"SR Downie","year":"2000","unstructured":"Downie, S. R. et al. A phylogeny of the flowering plant family Apiaceae based on chloroplast DNA rpl16 and rpoC1 intron sequences: Towards a suprageneric classification of subfamily Apioideae. Am. J. Botany 87, 273\u2013292 (2000).","journal-title":"Am. J. Botany"},{"key":"56394_CR48","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1006\/mpev.1999.0729","volume":"15","author":"W Zhang","year":"2000","unstructured":"Zhang, W. Phylogeny of the grass family (Poaceae) from rpl16 intron sequence data. Mol. Phylogen. Evol. 15, 135\u2013146 (2000).","journal-title":"Mol. Phylogen. Evol."},{"key":"56394_CR49","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1111\/j.1442-1984.2005.00131.x","volume":"20","author":"T Fukuda","year":"2005","unstructured":"Fukuda, T. et al. Molecular phylogeny of the genus Asparagus (Asparagaceae) inferred from plastid petB intron and petD\u2013rpoA intergenic spacer sequences. Plant Species Biol. 20, 121\u2013132 (2005).","journal-title":"Plant Species Biol."},{"key":"56394_CR50","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13059-020-02154-5","volume":"21","author":"J-J Jin","year":"2020","unstructured":"Jin, J.-J. et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21, 1\u201331 (2020).","journal-title":"Genome Biol."},{"key":"56394_CR51","doi-asserted-by":"publisher","first-page":"W6","DOI":"10.1093\/nar\/gkx391","volume":"45","author":"M Tillich","year":"2017","unstructured":"Tillich, M. et al. GeSeq\u2013versatile and accurate annotation of organelle genomes. Nucleic Acids Res. 45, W6\u2013W11 (2017).","journal-title":"Nucleic Acids Res."},{"key":"56394_CR52","doi-asserted-by":"publisher","first-page":"W59","DOI":"10.1093\/nar\/gkz238","volume":"47","author":"S Greiner","year":"2019","unstructured":"Greiner, S. et al. OrganellarGenomeDRAW (OGDRAW) version 1.3.1: Expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 47, W59\u2013W64 (2019).","journal-title":"Nucleic Acids Res."},{"key":"56394_CR53","doi-asserted-by":"publisher","first-page":"2583","DOI":"10.1093\/bioinformatics\/btx198","volume":"33","author":"S Beier","year":"2017","unstructured":"Beier, S. et al. MISA-web: A web server for microsatellite prediction. Bioinformatics 33, 2583\u20132585. https:\/\/doi.org\/10.1093\/bioinformatics\/btx198 (2017).","journal-title":"Bioinformatics"},{"key":"56394_CR54","doi-asserted-by":"publisher","first-page":"4633","DOI":"10.1093\/nar\/29.22.4633","volume":"29","author":"S Kurtz","year":"2001","unstructured":"Kurtz, S. et al. REPuter: The manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 29, 4633\u20134642 (2001).","journal-title":"Nucleic Acids Res."},{"key":"56394_CR55","unstructured":"Peden, J. F. Analysis of codon usage. (2000)."},{"key":"56394_CR56","doi-asserted-by":"publisher","first-page":"W273","DOI":"10.1093\/nar\/gkh458","volume":"32","author":"KA Frazer","year":"2004","unstructured":"Frazer, K. A. et al. VISTA: Computational tools for comparative genomics. Nucleic Acids Res. 32, W273\u2013W279 (2004).","journal-title":"Nucleic Acids Res."},{"key":"56394_CR57","doi-asserted-by":"publisher","first-page":"772","DOI":"10.1093\/molbev\/mst010","volume":"30","author":"K Katoh","year":"2013","unstructured":"Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772\u2013780 (2013).","journal-title":"Mol. Biol. Evol."},{"key":"56394_CR58","doi-asserted-by":"publisher","first-page":"3299","DOI":"10.1093\/molbev\/msx248","volume":"34","author":"J Rozas","year":"2017","unstructured":"Rozas, J. et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299\u20133302 (2017).","journal-title":"Mol. Biol. Evol."},{"key":"56394_CR59","doi-asserted-by":"publisher","first-page":"3030","DOI":"10.1093\/bioinformatics\/bty220","volume":"34","author":"A Amiryousefi","year":"2018","unstructured":"Amiryousefi, A. et al. IRscope: An online program to visualize the junction sites of chloroplast genomes. Bioinformatics 34, 3030\u20133031. https:\/\/doi.org\/10.1093\/bioinformatics\/bty220 (2018).","journal-title":"Bioinformatics"},{"key":"56394_CR60","doi-asserted-by":"crossref","unstructured":"L\u00f6ytynoja, A. Phylogeny-aware alignment with PRANK. Multiple sequence alignment methods, 155\u2013170 (2014).","DOI":"10.1007\/978-1-62703-646-7_10"},{"key":"56394_CR61","doi-asserted-by":"publisher","first-page":"1164","DOI":"10.1093\/bioinformatics\/btr088","volume":"27","author":"D Darriba","year":"2011","unstructured":"Darriba, D. et al. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164\u20131165. https:\/\/doi.org\/10.1093\/bioinformatics\/btr088 (2011).","journal-title":"Bioinformatics"},{"key":"56394_CR62","doi-asserted-by":"publisher","first-page":"1969","DOI":"10.1093\/molbev\/mss075","volume":"29","author":"AJ Drummond","year":"2012","unstructured":"Drummond, A. J. et al. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969\u20131973 (2012).","journal-title":"Mol. Biol. Evol."},{"key":"56394_CR63","doi-asserted-by":"publisher","first-page":"e1003537","DOI":"10.1371\/journal.pcbi.1003537","volume":"10","author":"R Bouckaert","year":"2014","unstructured":"Bouckaert, R. et al. BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537 (2014).","journal-title":"PLoS Comput. Biol."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-56394-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-56394-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-56394-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,14]],"date-time":"2024-03-14T13:12:27Z","timestamp":1710421947000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-56394-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,11]]},"references-count":63,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["56394"],"URL":"https:\/\/doi.org\/10.1038\/s41598-024-56394-7","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,11]]},"assertion":[{"value":"23 November 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 March 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 March 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"5873"}}