{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T03:36:22Z","timestamp":1760240182679,"version":"build-2065373602"},"reference-count":59,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2019,4,1]],"date-time":"2019-04-01T00:00:00Z","timestamp":1554076800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["OPUS 2 2011\/03\/B\/NZ2\/01420","HARMONIA 7 2015\/18\/M\/NZ2\/00422"],"award-info":[{"award-number":["OPUS 2 2011\/03\/B\/NZ2\/01420","HARMONIA 7 2015\/18\/M\/NZ2\/00422"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Plant genome evolution can be very complex and challenging to describe, even within a genus. Mechanisms that underlie genome variation are complex and can include whole-genome duplications, gene duplication and\/or loss, and, importantly, multiple chromosomal rearrangements. Lupins (Lupinus) diverged from other legumes approximately 60 mya. In contrast to New World lupins, Old World lupins show high variability not only for chromosome numbers (2n = 32\u201352), but also for the basic chromosome number (x = 5\u20139, 13) and genome size. The evolutionary basis that underlies the karyotype evolution in lupins remains unknown, as it has so far been impossible to identify individual chromosomes. To shed light on chromosome changes and evolution, we used comparative chromosome mapping among 11 Old World lupins, with Lupinus angustifolius as the reference species. We applied set of L. angustifolius-derived bacterial artificial chromosome clones for fluorescence in situ hybridization. We demonstrate that chromosome variations in the species analyzed might have arisen from multiple changes in chromosome structure and number. We hypothesize about lupin karyotype evolution through polyploidy and subsequent aneuploidy. Additionally, we have established a cytogenomic map of L. angustifolius along with chromosome markers that can be used for related species to further improve comparative studies of crops and wild lupins.<\/jats:p>","DOI":"10.3390\/genes10040259","type":"journal-article","created":{"date-parts":[[2019,4,2]],"date-time":"2019-04-02T03:21:26Z","timestamp":1554175286000},"page":"259","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Impact of Chromosomal Rearrangements on the Interpretation of Lupin Karyotype Evolution"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8518-4720","authenticated-orcid":false,"given":"Karolina","family":"Susek","sequence":"first","affiliation":[{"name":"Department of Genomics, Institute of Plant Genetics, Polish Academy of Sciences, 60-479 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6174-2898","authenticated-orcid":false,"given":"Wojciech","family":"Bielski","sequence":"additional","affiliation":[{"name":"Department of Genomics, Institute of Plant Genetics, Polish Academy of Sciences, 60-479 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3466-357X","authenticated-orcid":false,"given":"Katarzyna B.","family":"Czy\u017c","sequence":"additional","affiliation":[{"name":"Department of Biometry and Bioinformatics, Institute of Plant Genetics, Polish Academy of Sciences, 60-479 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6667-2721","authenticated-orcid":false,"given":"Robert","family":"Hasterok","sequence":"additional","affiliation":[{"name":"Department of Plant Anatomy and Cytology, University of Silesia in Katowice, 40-032 Katowice, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Scott A.","family":"Jackson","sequence":"additional","affiliation":[{"name":"Center for Applied Genetic Technologies, University of Georgia, Athens, GA 30602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bogdan","family":"Wolko","sequence":"additional","affiliation":[{"name":"Department of Genomics, Institute of Plant Genetics, Polish Academy of Sciences, 60-479 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4393-2655","authenticated-orcid":false,"given":"Barbara","family":"Naganowska","sequence":"additional","affiliation":[{"name":"Department of Genomics, Institute of Plant Genetics, Polish Academy of Sciences, 60-479 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,4,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.tig.2011.03.004","article-title":"Interpretation of karyotype evolution should consider chromosome structural constraints","volume":"27","author":"Schubert","year":"2011","journal-title":"Trends Genet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.biotechadv.2013.12.011","article-title":"Advances in plant chromosome genomics","volume":"32","year":"2014","journal-title":"Biotechnol. Adv."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1007\/s10577-015-9515-3","article-title":"Highly distinct chromosomal structures in cowpea (Vigna unguiculata), as revealed by molecular cytogenetic analysis","volume":"24","author":"Lin","year":"2016","journal-title":"Chromosome Res."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Kim, H., Choi, S.R., Bae, J., Hong, C.P., Lee, S.Y., Hossain, M.J., Van Nguyen, D., Jin, M., Park, B.-S., and Bang, J.-W. (2009). Sequenced BAC anchored reference genetic map that reconciles the ten individual chromosomes of Brassica rapa. BMC Genom., 10.","DOI":"10.1186\/1471-2164-10-432"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Sun, J., Zhang, Z., Zong, X., Huang, S., Li, Z., and Han, Y. (2013). A high-resolution cucumber cytogenetic map integrated with the genome assembly. BMC Genom., 14.","DOI":"10.1186\/1471-2164-14-461"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2027","DOI":"10.1111\/pbi.12936","article-title":"Chromosome-level assembly, genetic and physical mapping of Phalaenopsis aphrodite genome provides new insights into species adaptation and resources for orchid breeding","volume":"16","author":"Chao","year":"2018","journal-title":"Plant Biotechnol. J."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1534\/g3.114.011197","article-title":"Fluorescence in situ hybridization and optical mapping to correct scaffold arrangement in the tomato genome","volume":"4","author":"Shearer","year":"2014","journal-title":"G3 (Bethesda)"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1424","DOI":"10.1111\/nph.13999","article-title":"Identification of peanut (Arachis hypogaea) chromosomes using a fluorescence in situ hybridization system reveals multiple hybridization events during tetraploid peanut formation","volume":"211","author":"Zhang","year":"2016","journal-title":"New Phytol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1534\/genetics.109.113753","article-title":"A fluorescence in situ hybridization system for karyotyping soybean","volume":"185","author":"Findley","year":"2010","journal-title":"Genetics"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1007\/s10577-010-9129-8","article-title":"Cytogenetic map of common bean (Phaseolus vulgaris L.)","volume":"18","author":"Ferreira","year":"2010","journal-title":"Chromosome Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1139\/gen-2013-0025","article-title":"Karyotype stability in the genus Phaseolus evidenced by the comparative mapping of the wild species Phaseolus microcarpus","volume":"56","year":"2013","journal-title":"Genome"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1111\/j.1469-8137.2012.04195.x","article-title":"Chromosome evolution in Solanum traced by cross-species BAC-FISH","volume":"195","author":"Szinay","year":"2012","journal-title":"New Phytol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1007\/s10577-011-9202-y","article-title":"Comparative FISH mapping of Daucus species (Apiaceae family)","volume":"19","author":"Iovene","year":"2011","journal-title":"Chromosome Res."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Gladstones, J.S., Atkins, C.A., and Hamblin, J. (1998). Distribution, origin, taxonomy, history and importance. Lupins as Crop Plants: Biology, Production, and Utilization, CAB International.","DOI":"10.1079\/9780851992242.0000"},{"key":"ref_15","first-page":"211","article-title":"Molecular phylogeny, diversification and character evolution in Lupinus (Fabaceae) with special attention to Mediterranean and African lupines","volume":"246","author":"Bayer","year":"2004","journal-title":"Plant Syst. Evol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1093\/aob\/mcg145","article-title":"Nuclear DNA content variation and species relationships in the genus Lupinus (Fabaceae)","volume":"92","author":"Naganowska","year":"2003","journal-title":"Ann. Bot."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1152","DOI":"10.3389\/fpls.2016.01152","article-title":"A first glimpse of wild lupin karyotype variation as revealed by comparative cytogenetic mapping","volume":"7","author":"Susek","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Susek, K., Braszewska-Zalewska, A., Bewick, A.J., Hasterok, R., Schmitz, R.J., and Naganowska, B. (2017). Epigenomic diversification within the genus Lupinus. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0179821"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1093\/dnares\/dsq001","article-title":"Aligning a new reference genetic map of Lupinus angustifolius with the genome sequence of the model legume, Lotus japonicus","volume":"17","author":"Nelson","year":"2010","journal-title":"DNA Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1111\/pbi.12615","article-title":"A comprehensive draft genome sequence for lupin (Lupinus angustifolius), an emerging health food: Insights into plant\u2013microbe interactions and legume evolution","volume":"15","author":"Hane","year":"2017","journal-title":"Plant Biotechnol. J."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"15335","DOI":"10.1038\/s41598-017-15625-w","article-title":"A high-density consensus linkage map of white lupin highlights synteny with narrow-leafed lupin and provides markers tagging key agronomic traits","volume":"7","author":"Nazzicari","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_22","first-page":"1","article-title":"Yellow lupin (Lupinus luteus L.) transcriptome sequencing: Molecular marker development and comparative studies","volume":"13","author":"Udall","year":"2012","journal-title":"BMC Genom."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1093\/jhered\/esq107","article-title":"Assignment of 3 genetic linkage groups to 3 chromosomes of narrow-leafed lupin","volume":"102","author":"Lesniewska","year":"2011","journal-title":"J. Hered."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1007\/s10577-016-9526-8","article-title":"Integration of Lupinus angustifolius L. (narrow-leafed lupin) genome maps and comparative mapping within legumes","volume":"24","author":"Wyrwa","year":"2016","journal-title":"Chromosome Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"396","DOI":"10.2478\/s11658-006-0033-3","article-title":"The bacterial artificial chromosome (BAC) library of the narrow-leafed lupin (Lupinus angustifolius L.)","volume":"11","author":"Kasprzak","year":"2006","journal-title":"Cell. Mol. Biol. Lett."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1007\/s10577-015-9513-5","article-title":"chromDraw: An R package for visualization of linear and circular karyotypes","volume":"24","author":"Lysak","year":"2016","journal-title":"Chromosome Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.pbi.2007.01.001","article-title":"Chromosome evolution","volume":"10","author":"Schubert","year":"2007","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1007\/s10577-014-9464-2","article-title":"Intra- and interchromosomal rearrangements between cowpea [Vigna unguiculata (L.) Walp.] and common bean (Phaseolus vulgaris L.) revealed by BAC-FISH","volume":"23","author":"Vasconcelos","year":"2015","journal-title":"Chromosome Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1007\/s00412-010-0303-8","article-title":"Compact genomes and complex evolution in the genus Brachypodium","volume":"120","author":"Wolny","year":"2011","journal-title":"Chromosoma"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1093\/aob\/mcy086","article-title":"Chromosome identification and reconstruction of evolutionary rearrangements in Brachypodium distachyon, B. stacei and B. hybridum","volume":"122","author":"Lusinska","year":"2018","journal-title":"Ann. Bot."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.pbi.2016.02.001","article-title":"Comparative paleogenomics of crucifers: Ancestral genomic blocks revisited","volume":"30","author":"Lysak","year":"2016","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1007\/s00412-015-0548-3","article-title":"Speeding up chromosome evolution in Phaseolus: Multiple rearrangements associated with a one-step descending dysploidy","volume":"125","author":"Ferraz","year":"2016","journal-title":"Chromosoma"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Soltis, P.S., and Soltis, D.E. (2012). Polyploidy in Legumes. Polyploidy and Genome Evolution, Springer.","DOI":"10.1007\/978-3-642-31442-1"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1093\/aob\/mcu237","article-title":"Arachis batizocoi: A study of its relationship to cultivated peanut (A. hypogaea) and its potential for introgression of wild genes into the peanut crop using induced allotetraploids","volume":"115","author":"Santos","year":"2015","journal-title":"Ann. Bot."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1007\/s13237-012-0059-z","article-title":"Meiotic consequences of selfing in grass pea (Lathyrus sativus L.) autotetraploids in the advanced generations: Cytogenetics of chromosomal rearrangement and detection of aneuploids","volume":"55","author":"Talukdar","year":"2012","journal-title":"Nucleus"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1142","DOI":"10.3732\/ajb.1000009","article-title":"Phylogeny and character evolution in Medicago (Leguminosae): Evidence from analyses of plastid trnK\/matK and nuclear GA3ox1 sequences","volume":"97","author":"Steele","year":"2010","journal-title":"Am. J. Bot."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1093\/gbe\/evv014","article-title":"Karyotype and gene order evolution from reconstructed extinct ancestors highlight contrasts in genome plasticity of modern rosid crops","volume":"7","author":"Murat","year":"2015","journal-title":"Genome Biol. Evol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1016\/j.ympev.2008.03.009","article-title":"Diversification of Lupinus (Leguminosae) in the western New World: Derived evolution of perennial life history and colonization of montane habitats","volume":"48","author":"Drummond","year":"2008","journal-title":"Mol. Phylogenet. Evol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1007\/s00122-014-2294-y","article-title":"New evidence of ancestral polyploidy in the Genistoid legume Lupinus angustifolius L. (narrow-leafed lupin)","volume":"127","author":"Kroc","year":"2014","journal-title":"Theor. Appl. Genet."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1111\/j.1095-8339.2006.00443.x","article-title":"New chromosome numbers, meiotic behaviour and pollen fertility in American taxa of Lupinus (Leguminosae): Contributions to taxonomic and evolutionary studies","volume":"150","author":"Conterato","year":"2006","journal-title":"Bot. J. Linn. Soc."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/s00606-005-0364-y","article-title":"2C DNA variation and relationships among New World species of the genus Lupinus (Fabaceae)","volume":"256","author":"Naganowska","year":"2006","journal-title":"Plant Syst. Evol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1093\/gbe\/evt200","article-title":"Shared subgenome dominance following polyploidization explains grass genome evolutionary plasticity from a seven protochromosome ancestor with 16K protogenes","volume":"6","author":"Murat","year":"2014","journal-title":"Genome Biol. Evol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1093\/molbev\/msu296","article-title":"Multiple polyploidy events in the early radiation of nodulating and nonnodulating legumes","volume":"32","author":"Cannon","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2545","DOI":"10.1105\/tpc.110.074229","article-title":"Structural and functional divergence of a 1-Mb duplicated region in the soybean (Glycine max) genome and comparison to an orthologous region from Phaseolus vulgaris","volume":"22","author":"Lin","year":"2010","journal-title":"Plant Cell"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1111\/tpj.14065","article-title":"Hybridization-facilitated genome merger and repeated chromosome fusion after 8 million years","volume":"96","author":"Guo","year":"2018","journal-title":"Plant J."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"3280","DOI":"10.1105\/tpc.113.114405","article-title":"The more the merrier: Recent hybridization and polyploidy in Cardamine","volume":"25","author":"Shimizu","year":"2013","journal-title":"Plant Cell"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1093\/sysbio\/syr126","article-title":"Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): Testing for key innovation with incomplete taxon sampling","volume":"61","author":"Drummond","year":"2012","journal-title":"Syst. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.ympev.2011.04.017","article-title":"Isolation, phylogeny and evolution of the SymRK gene in the legume genus Lupinus L.","volume":"60","author":"Mahe","year":"2011","journal-title":"Mol. Phylogenet. Evol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"International Brachypodium Initiative (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature, 463, 763\u2013768.","DOI":"10.1038\/nature08747"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"15274","DOI":"10.1038\/s41598-017-14885-w","article-title":"Sub genome anchored physical frameworks of the allotetraploid Upland cotton (Gossypium hirsutum L.) genome, and an approach toward reference-grade assemblies of polyploids","volume":"7","author":"Saski","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1071\/AR07205","article-title":"Identification of quantitative trait loci (QTLs) influencing early vigour, height, flowering date, and seed size and their implications for breeding of narrow-leafed lupin (Lupinus angustifolius L.)","volume":"59","author":"Boersma","year":"2008","journal-title":"Aust. J. Agr. Res."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Yang, H., Tao, Y., Zheng, Z., Zhang, Q., Zhou, G., Sweetingham, M.W., Howieson, J.G., and Li, C. (2013). Draft genome sequence, and a sequence-defined genetic linkage map of the legume crop species Lupinus angustifolius L.. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0064799"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/s13007-016-0107-9","article-title":"An efficient approach to BAC based assembly of complex genomes","volume":"12","author":"Visendi","year":"2016","journal-title":"Plant Methods"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.1101\/gr.236273.118","article-title":"Chromosome assembly of large and complex genomes using multiple references","volume":"28","author":"Kolmogorov","year":"2018","journal-title":"Genome Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1007\/s00412-008-0151-y","article-title":"Integrated cytogenetic map of mitotic metaphase chromosome 9 of maize: Resolution, sensitivity, and banding paint development","volume":"117","author":"Danilova","year":"2008","journal-title":"Chromosoma"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1104\/pp.18.01165","article-title":"Healthy roots and leaves: Comparative genome structure of horseradish and watercress","volume":"179","author":"Lysak","year":"2019","journal-title":"Plant Physiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"6445","DOI":"10.1111\/mec.14379","article-title":"Multispeed genome diploidization and diversification after an ancient allopolyploidization","volume":"26","author":"Mandakova","year":"2017","journal-title":"Mol. Ecol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"5224","DOI":"10.1073\/pnas.0510791103","article-title":"Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species","volume":"103","author":"Lysak","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1534\/genetics.115.177642","article-title":"Chromosome-specific painting in Cucumis species using bulked oligonucleotides","volume":"200","author":"Han","year":"2015","journal-title":"Genetics"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/10\/4\/259\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:42:10Z","timestamp":1760186530000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/10\/4\/259"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,4,1]]},"references-count":59,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2019,4]]}},"alternative-id":["genes10040259"],"URL":"https:\/\/doi.org\/10.3390\/genes10040259","relation":{},"ISSN":["2073-4425"],"issn-type":[{"type":"electronic","value":"2073-4425"}],"subject":[],"published":{"date-parts":[[2019,4,1]]}}}