{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T19:10:49Z","timestamp":1791400249245,"version":"4.3.3"},"reference-count":75,"publisher":"Wiley","issue":"6","license":[{"start":{"date-parts":[[2023,9,14]],"date-time":"2023-09-14T00:00:00Z","timestamp":1694649600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32070663"],"award-info":[{"award-number":["32070663"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32125009"],"award-info":[{"award-number":["32125009"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32200510"],"award-info":[{"award-number":["32200510"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["The Plant Journal"],"published-print":{"date-parts":[[2023,12]]},"abstract":"<jats:title>SUMMARY<\/jats:title>\n                  <jats:p>\n                    Whole\u2010genome duplication (WGD) leads to the duplication of both coding and non\u2010coding sequences within an organism's genome, providing an abundant supply of genetic material that can drive evolution, ultimately contributing to plant adaptation and speciation. Although non\u2010coding sequences contain numerous regulatory elements, they have been understudied compared to coding sequences. In order to address this gap, we explored the evolutionary patterns of regulatory sequences, coding sequences and transcriptomes using conserved non\u2010coding elements (CNEs) as regulatory element proxies following the recent WGD event in opium poppy (\n                    <jats:italic>Papaver somniferum<\/jats:italic>\n                    ). Our results showed similar evolutionary patterns in subgenomes of regulatory and coding sequences. Specifically, the biased or unbiased retention of coding sequences reflected the same pattern as retention levels in regulatory sequences. Further, the divergence of gene expression patterns mediated by regulatory element variations occurred at a more rapid pace than that of gene coding sequences. However, gene losses were purportedly dependent on relaxed selection pressure in coding sequences. Specifically, the rapid evolution of tissue\u2010specific benzylisoquinoline alkaloid production in\n                    <jats:italic>P. somniferum<\/jats:italic>\n                    was associated with regulatory element changes. The origin of a novel stem\u2010specific ACR, which utilized ancestral cis\u2010elements as templates, is likely to be linked to the evolutionary trajectory behind the transition of the\n                    <jats:italic>PSMT1<\/jats:italic>\n                    \u2010\n                    <jats:italic>CYP719A21<\/jats:italic>\n                    cluster from high levels of expression solely in\n                    <jats:italic>P. rhoeas<\/jats:italic>\n                    root tissue to its elevated expression in\n                    <jats:italic>P. somniferum<\/jats:italic>\n                    stem tissue. Our findings demonstrate that rapid regulatory element evolution can contribute to the emergence of new phenotypes and provide valuable insights into the high evolvability of regulatory elements.\n                  <\/jats:p>","DOI":"10.1111\/tpj.16466","type":"journal-article","created":{"date-parts":[[2023,9,14]],"date-time":"2023-09-14T13:20:10Z","timestamp":1694697610000},"page":"1804-1824","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Evolutionary analysis of conserved non\u2010coding elements subsequent to whole\u2010genome duplication in opium poppy"],"prefix":"10.1111","volume":"116","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3386-1379","authenticated-orcid":false,"given":"Yu","family":"Xu","sequence":"first","affiliation":[{"name":"School of Life Science and Technology Xi'an Jiaotong University  Xi'an Shaanxi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen J.","family":"Bush","sequence":"additional","affiliation":[{"name":"School of Automation Science and Engineering, Faculty of Electronic and Information Engineering Xi'an Jiaotong University  Xi'an Shaanxi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinyi","family":"Yang","sequence":"additional","affiliation":[{"name":"School of Life Science and Technology Xi'an Jiaotong University  Xi'an Shaanxi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linfeng","family":"Xu","sequence":"additional","affiliation":[{"name":"School of Automation Science and Engineering, Faculty of Electronic and Information Engineering Xi'an Jiaotong University  Xi'an Shaanxi China"},{"name":"MOE Key Lab for Intelligent Networks &amp; Networks Security, Faculty of Electronic and Information Engineering Xi'an Jiaotong University  Xi'an Shaanxi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9041-878X","authenticated-orcid":false,"given":"Bo","family":"Wang","sequence":"additional","affiliation":[{"name":"School of Automation Science and Engineering, Faculty of Electronic and Information Engineering Xi'an Jiaotong University  Xi'an Shaanxi China"},{"name":"MOE Key Lab for Intelligent Networks &amp; Networks Security, Faculty of Electronic and Information Engineering Xi'an Jiaotong University  Xi'an Shaanxi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kai","family":"Ye","sequence":"additional","affiliation":[{"name":"School of Life Science and Technology Xi'an Jiaotong University  Xi'an Shaanxi China"},{"name":"School of Automation Science and Engineering, Faculty of Electronic and Information Engineering Xi'an Jiaotong University  Xi'an Shaanxi China"},{"name":"MOE Key Lab for Intelligent Networks &amp; Networks Security, Faculty of Electronic and Information Engineering Xi'an Jiaotong University  Xi'an Shaanxi China"},{"name":"Genome Institute The First Affiliated Hospital of Xi'an Jiaotong University  Xi'an Shaanxi China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2023,9,14]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pbi.2020.03.004"},{"key":"e_1_2_9_3_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/25.17.3389"},{"key":"e_1_2_9_4_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1313759110"},{"key":"e_1_2_9_5_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00425-014-2056-8"},{"key":"e_1_2_9_6_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1207726109"},{"key":"e_1_2_9_7_1","doi-asserted-by":"publisher","DOI":"10.1093\/plcell\/koac076"},{"key":"e_1_2_9_8_1","doi-asserted-by":"publisher","DOI":"10.1093\/genetics\/iyad114"},{"key":"e_1_2_9_9_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/19.2.185"},{"key":"e_1_2_9_10_1","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.13765"},{"key":"e_1_2_9_11_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.113.121905"},{"key":"e_1_2_9_12_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2008.06.030"},{"key":"e_1_2_9_13_1","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2006-7-2-r13"},{"key":"e_1_2_9_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molp.2020.06.009"},{"key":"e_1_2_9_15_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1006266"},{"key":"e_1_2_9_16_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41477-018-0136-7"},{"key":"e_1_2_9_17_1","first-page":"2292","article-title":"The evolution of gene duplicates in angiosperms and the impact of protein\u2010protein interactions and the mechanism of duplication","volume":"11","author":"Defoort J.","year":"2019","journal-title":"Genome Biology and Evolution"},{"key":"e_1_2_9_18_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1673-8527(09)60003-5"},{"key":"e_1_2_9_19_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.17.00010"},{"key":"e_1_2_9_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-020-01354-3"},{"key":"e_1_2_9_21_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-015-0721-2"},{"key":"e_1_2_9_22_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1921046117"},{"key":"e_1_2_9_23_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/mst230"},{"key":"e_1_2_9_24_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.aat4096"},{"key":"e_1_2_9_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2010.05.004"},{"key":"e_1_2_9_26_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkz890"},{"key":"e_1_2_9_27_1","doi-asserted-by":"publisher","DOI":"10.1111\/nph.18173"},{"key":"e_1_2_9_28_1","doi-asserted-by":"publisher","DOI":"10.3389\/fgene.2023.1136736"},{"key":"e_1_2_9_29_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkw982"},{"key":"e_1_2_9_30_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-201X.2003.01166.x"},{"key":"e_1_2_9_31_1","unstructured":"Kolde R.(2019)pheatmap: pretty heatmaps. R package version 1.0. 12.R Packag. version 1.0 8."},{"key":"e_1_2_9_32_1","first-page":"205","article-title":"A benchmark of gene expression tissue\u2010specificity metrics","volume":"18","author":"Kryuchkova\u2010Mostacci N.","year":"2017","journal-title":"Briefings in Bioinformatics"},{"key":"e_1_2_9_33_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msaa036"},{"key":"e_1_2_9_34_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2005.08.006"},{"key":"e_1_2_9_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.xplc.2020.100029"},{"key":"e_1_2_9_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molp.2017.12.010"},{"key":"e_1_2_9_37_1","doi-asserted-by":"publisher","DOI":"10.1093\/gbe\/evx035"},{"key":"e_1_2_9_38_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.19.00323"},{"key":"e_1_2_9_39_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg3802"},{"key":"e_1_2_9_40_1","doi-asserted-by":"publisher","DOI":"10.1093\/pcp\/pcu197"},{"key":"e_1_2_9_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2016.04.038"},{"key":"e_1_2_9_42_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-019-1650-2"},{"key":"e_1_2_9_43_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btq033"},{"key":"e_1_2_9_44_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gku365"},{"key":"e_1_2_9_45_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg3229"},{"key":"e_1_2_9_46_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2011.00002"},{"key":"e_1_2_9_47_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1101368108"},{"key":"e_1_2_9_48_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.109.144220"},{"key":"e_1_2_9_49_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-022-04823-w"},{"key":"e_1_2_9_50_1","unstructured":"Smit A. Hubley R.&Green P.(2015)RepeatMasker Open\u20104.0. 2013\u20132015."},{"key":"e_1_2_9_51_1","doi-asserted-by":"publisher","DOI":"10.1101\/gr.266528.120"},{"key":"e_1_2_9_52_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jprot.2019.103613"},{"key":"e_1_2_9_53_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molp.2022.10.018"},{"key":"e_1_2_9_54_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.17.00313"},{"key":"e_1_2_9_55_1","unstructured":"Team R.C.(2013)R: a language and environment for statistical computing."},{"key":"e_1_2_9_56_1","doi-asserted-by":"publisher","DOI":"10.1093\/bib\/bbs017"},{"key":"e_1_2_9_57_1","first-page":"D1104","article-title":"PlantRegMap: charting functional regulatory maps in plants","volume":"48","author":"Tian F.","year":"2020","journal-title":"Nucleic Acids Research"},{"key":"e_1_2_9_58_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2013.00170"},{"key":"e_1_2_9_59_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.152047199"},{"key":"e_1_2_9_60_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-022-04506-6"},{"key":"e_1_2_9_61_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.16.01177"},{"key":"e_1_2_9_62_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkr1293"},{"key":"e_1_2_9_63_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-319-24277-4"},{"key":"e_1_2_9_64_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1220757"},{"key":"e_1_2_9_65_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg3095"},{"key":"e_1_2_9_66_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg2063"},{"key":"e_1_2_9_67_1","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.15689"},{"key":"e_1_2_9_68_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.112.106716"},{"key":"e_1_2_9_69_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-26330-8"},{"key":"e_1_2_9_70_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pbi.2021.102139"},{"key":"e_1_2_9_71_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msab042"},{"key":"e_1_2_9_72_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btv145"},{"key":"e_1_2_9_73_1","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.12602"},{"key":"e_1_2_9_74_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molp.2020.12.020"},{"key":"e_1_2_9_75_1","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2008-9-9-r137"},{"key":"e_1_2_9_76_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.17.00595"}],"container-title":["The Plant Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/tpj.16466","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,26]],"date-time":"2023-12-26T05:59:38Z","timestamp":1703570378000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/tpj.16466"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,14]]},"references-count":75,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2023,12]]}},"alternative-id":["10.1111\/tpj.16466"],"URL":"https:\/\/doi.org\/10.1111\/tpj.16466","archive":["Portico"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.05.06.539671","asserted-by":"object"}]},"ISSN":["0960-7412","1365-313X"],"issn-type":[{"value":"0960-7412","type":"print"},{"value":"1365-313X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,14]]},"assertion":[{"value":"2022-04-19","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-09-05","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-09-14","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}