{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T06:05:03Z","timestamp":1789538703782,"version":"build-2803163510"},"reference-count":133,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T00:00:00Z","timestamp":1789516800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:sec>\n                    <jats:title>Introduction<\/jats:title>\n                    <jats:p>\n                      <jats:italic>Primula<\/jats:italic>\n                      is the largest genus in Primulaceae and a classic model for studying heterostyly and plant evolution.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      In this study, we sequenced, assembled, and annotated the complete chloroplast genomes of seven\n                      <jats:italic>Primula<\/jats:italic>\n                      species from China. Two additional plastomes of\n                      <jats:italic>Primula dejuniana<\/jats:italic>\n                      and\n                      <jats:italic>Primula meishanensis<\/jats:italic>\n                      , previously generated and published by our research group, were retrieved from GenBank and integrated into our dataset. We further combined these nine plastome resources with 48 published\n                      <jats:italic>Primula<\/jats:italic>\n                      plastomes and three outgroup plastomes downloaded from GenBank, forming a total dataset of 60 chloroplast genomes to conduct comparative genomic analyses, repeat sequence detection, hypervariable region identification, phylogenetic reconstruction, divergence time estimation, and ancestral trait reconstruction.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      The chloroplast genomes exhibited a typical quadripartite structure and high conservation, with lengths ranging from 151, 555 to 154, 653 bp. We detected 433 SSRs, 242 long repeat sequences, and six highly variable regions that can be used as candidate molecular markers. Phylogenetic analyses firmly clarified the relationships of several sections and newly sequenced species. Divergence time analyses indicated that\n                      <jats:italic>Primula<\/jats:italic>\n                      initiated its rapid radiation at approximately 19.59 Mya (95% HPD: 13.19\u201325.89 Mya, Early Miocene). Ancestral state reconstruction supported that the genus was ancestrally characterized by umbellate inflorescences, heterostyly, purple corollas, and campanulate calyces, with derived traits evolving repeatedly.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Discussion<\/jats:title>\n                    <jats:p>\n                      Our results provide valuable chloroplast genomic resources and robust phylogenetic evidence for the evolutionary study of\n                      <jats:italic>Primula<\/jats:italic>\n                      species.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fpls.2026.1889564","type":"journal-article","created":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T05:33:12Z","timestamp":1789536792000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Chloroplast genomes of nine Primula species: comparative genomics and phylogenetic implications"],"prefix":"10.3389","volume":"17","author":[{"given":"Yanru","family":"Zhang","sequence":"first","affiliation":[{"name":"College of Life Sciences, Sichuan Normal University","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shihao","family":"Jiang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Sichuan Normal University","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qinyi","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Sichuan Normal University","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xingyu","family":"Du","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Sichuan Normal University","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiazhen","family":"Wu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Sichuan Normal University","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiang","family":"Li","sequence":"additional","affiliation":[{"name":"Meishan Ecological Environment Monitoring Center Station","place":["Meishan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jieli","family":"Yue","sequence":"additional","affiliation":[{"name":"Meishan Ecological Environment Monitoring Center Station","place":["Meishan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Min","family":"Pan","sequence":"additional","affiliation":[{"name":"Meishan Ecological Environment Monitoring Center Station","place":["Meishan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoqin","family":"Liu","sequence":"additional","affiliation":[{"name":"Meishan Ecological Environment Monitoring Center Station","place":["Meishan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yizhen","family":"Shao","sequence":"additional","affiliation":[{"name":"College of Life Science, Henan Agricultural University","place":["Zhengzhou, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xianhua","family":"Gu","sequence":"additional","affiliation":[{"name":"Sichuan Leshan Ecological Environment Monitoring Center Station","place":["Leshan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liang","family":"Dou","sequence":"additional","affiliation":[{"name":"Museum of Natural History, College of Life Sciences, Sichuan University","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Zhou","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Sichuan Normal University","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhixi","family":"Fu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Sichuan Normal University","place":["Chengdu, China"]},{"name":"Sustainable Development Research Center of Resources and Environment of Western Sichuan, Sichuan Normal University","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,9,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"2320","DOI":"10.1038\/nprot.2006.384","article-title":"A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide","volume":"1","author":"Allen","year":"2006","journal-title":"Nat. Protoc."},{"key":"B2","doi-asserted-by":"publisher","first-page":"3030","DOI":"10.1093\/bioinformatics\/bty220","article-title":"IRscope: an online program to visualize the junction sites of chloroplast genomes","volume":"34","author":"Amiryousefi","year":"2018","journal-title":"Bioinformatics"},{"key":"B3","doi-asserted-by":"publisher","first-page":"718","DOI":"10.1038\/s41561-018-0236-z","article-title":"Geological and climatic influences on mountain biodiversity","volume":"11","author":"Antonelli","year":"2018","journal-title":"Nat. Geosci."},{"key":"B4","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-540-68486-2_1","article-title":"New insights on heterostyly: Comparative biology, ecology and genetics","volume-title":"Self-Incompatibility in Flowering Plants: Evolution, Diversity, and Mechanisms","author":"Barrett","year":"2008"},{"key":"B5","doi-asserted-by":"publisher","first-page":"2583","DOI":"10.1093\/bioinformatics\/btx198","article-title":"MISA-web: a web server for microsatellite prediction","volume":"33","author":"Beier","year":"2017","journal-title":"Bioinformatics"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1006650","article-title":"BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis","volume":"15","author":"Bouckaert","year":"2019","journal-title":"PloS Comput. Biol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1093\/jxb\/ers391","article-title":"Plastid genome evolution across the genus Cuscuta (Convolvulaceae): two clades within subgenus Grammica exhibit extensive gene loss","volume":"64","author":"Braukmann","year":"2013","journal-title":"J. Exp. Bot."},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-12-56","article-title":"Polyploid evolution and Pleistocene glacial cycles: A case study from the alpine primrose Primula marginata (Primulaceae)","volume":"12","author":"Casazza","year":"2012","journal-title":"BMC Evol. Biol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"3838","DOI":"10.13271\/j.mpb.015.003838","article-title":"Studies on pollination insect species and their visiting behavior of Primula lithophila of endemic plants in Guizhou","volume":"15","author":"Changjiang","year":"2017","journal-title":"Mol. Plant Breed"},{"key":"B10","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1080\/11263504.2013.826745","article-title":"Evidence of hybrid speciation in the North American primroses Primula suffrutescensP. parryiP. rusbyi and P. angustifolia (Primulaceae)","volume":"149","author":"Cianchi","year":"2015","journal-title":"Plant Biosyst. - Int. J. Dealing Aspects Plant Biosyst."},{"key":"B11","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1111\/j.1095-8339.1978.tb02361.x","article-title":"Rhododendron seeds from the Palaeocene of southern England","volume":"76","author":"Collinson","year":"1978","journal-title":"Bot. J. Linn. Soc"},{"key":"B12","doi-asserted-by":"publisher","first-page":"432","DOI":"10.1016\/S1360-1385(98)01327-2","article-title":"The effect of Quaternary climatic changes on plant distribution and evolution","volume":"3","author":"Comes","year":"1998","journal-title":"Trends Plant Sci."},{"key":"B13","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/j.ympev.2009.08.008","article-title":"Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae)","volume":"54","author":"Cristina Acosta","year":"2010","journal-title":"Mol. Phylogenet. Evol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1127\/palb\/265\/2003\/1","article-title":"Pal\u00e4okarpologische untersuchungen von taphoz\u00f6nosen der unter- und mittelmioz\u00e4ns aus dem braunkohlentagebau berzdorf\/oberlausitz (sachsen)","volume":"265","author":"Czaja","year":"2003","journal-title":"Palaeontographica Abteilung B."},{"key":"B15","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1186\/s13059-016-1004-2","article-title":"Chloroplast genomes: diversity, evolution, and applications in genetic engineering","volume":"17","author":"Daniell","year":"2016","journal-title":"Genome Biol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"20230361","DOI":"10.1098\/rstb.2023.0361","article-title":"The evolution of flavonoid biosynthesis","volume":"379","author":"Davies","year":"2024","journal-title":"Philos. Trans. R. Soc Lond. B. Biol. Sci."},{"key":"B17","doi-asserted-by":"publisher","first-page":"2894","DOI":"10.1360\/TB-2019-0053","article-title":"Significant shift in the terrestrial ecosystem at the Paleogene\/Neogene boundary in the Tibetan Plateau","volume":"64","author":"Deng","year":"2019","journal-title":"Chin. Sci. Bull."},{"key":"B18","doi-asserted-by":"publisher","first-page":"20140075","DOI":"10.1098\/rspb.2014.0075","article-title":"Heterostyly accelerates diversification via reduced extinction in primroses","volume":"281","author":"De Vos","year":"2014","journal-title":"Proc. Biol. Sci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1126\/science.abb4484","article-title":"Ancient orogenic and monsoon-driven assembly of the world's richest temperate alpine flora","volume":"369","author":"Ding","year":"2020","journal-title":"Science"},{"key":"B20","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1093\/dnares\/dsr002","article-title":"The complete chloroplast genome of 17 individuals of pest species Jacobaea vulgaris: SNPs, microsatellites and barcoding markers for population and phylogenetic studies","volume":"18","author":"Doorduin","year":"2011","journal-title":"DNA Res."},{"key":"B21","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1007\/978-1-4615-3276-7_2","article-title":"Use of chloroplast DNA rearrangements in reconstructing plant phylogeny","author":"Downie","year":"1992","journal-title":"Mol. Systematics Plants"},{"key":"B22","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/0031-9422(80)85004-7","article-title":"A rapid DNA isolation procedure for small quantities of fresh leaf tissue","volume":"19","author":"Doyle","year":"1987","journal-title":"Phytochem. Bull."},{"key":"B23","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1111\/j.1759-6831.2010.00087.x","article-title":"Disentangling confusions in inflorescence morphology: Patterns and diversity of reproductive shoot ramification in angiosperms","volume":"48","author":"Endress","year":"2010","journal-title":"J. Syst. Evol."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.aax1697","article-title":"Past East Asian monsoon evolution controlled by paleogeography, not CO(2)","volume":"5","author":"Farnsworth","year":"2019","journal-title":"Sci. Adv."},{"key":"B25","doi-asserted-by":"publisher","first-page":"W273","DOI":"10.1093\/nar\/gkh458","article-title":"VISTA: computational tools for comparative genomics","volume":"32","author":"Frazer","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1016\/j.plantsci.2023.111599","article-title":"Molecular identification of a flavone synthase I\/flavanone 3\u03b2-hydroxylase bifunctional enzyme from fern species Psilotum nudum","volume":"329","author":"Fu","year":"2023","journal-title":"Plant Sci."},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1016\/j.ympev.2019.106553","article-title":"Calyx (con)fusion in a hyper-diverse genus: Parallel evolution of unusual flower patterns in Eugenia (Myrtaceae)","volume":"139","author":"Giaretta","year":"2019","journal-title":"Mol. Phylogenet. Evol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1111\/nph.13558","article-title":"On the origins of observations of heterostyly in Primula","volume":"208","author":"Gilmartin","year":"2015","journal-title":"New Phytol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1111\/evo.13870","article-title":"Do selfing species have greater niche breadth? Support from ecological niche modeling","volume":"74","author":"Grant","year":"2020","journal-title":"Evolution"},{"key":"B30","doi-asserted-by":"publisher","first-page":"W59","DOI":"10.1093\/nar\/gkz238","article-title":"OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes","volume":"47","author":"Greiner","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"B31","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1093\/sysbio\/syp010","article-title":"Disentangling reticulate evolution in an arctic-alpine polyploid complex","volume":"58","author":"Guggisberg","year":"2009","journal-title":"Syst. Biol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1093\/molbev\/msq229","article-title":"Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage","volume":"28","author":"Guisinger","year":"2011","journal-title":"Mol. Biol. Evol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1186\/s12864-017-3555-3","article-title":"Plastome phylogeny and early diversification of Brassicaceae","volume":"18","author":"Guo","year":"2017","journal-title":"BMC Genomics"},{"key":"B34","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1186\/s12870-021-03053-y","article-title":"The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions","volume":"21","author":"Guo","year":"2021","journal-title":"BMC Plant Biol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1007\/s11105-012-0461-3","article-title":"Loss of the acetyl-coA carboxylase (accD) gene in poales","volume":"31","author":"Harris","year":"2013","journal-title":"Plant Mol. Biol. Rep."},{"key":"B36","doi-asserted-by":"publisher","first-page":"12608","DOI":"10.3390\/ijms131012608","article-title":"Genetic diversity and population structure: implications for conservation of wild soybean (Glycine soja Sieb. et Zucc) based on nuclear and chloroplast microsatellite variation","volume":"13","author":"He","year":"2012","journal-title":"Int. J. Mol. Sci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"15285","DOI":"10.1038\/s41598-019-51601-2","article-title":"Structural variation of the complete chloroplast genome and plastid phylogenomics of the genus Asteropyrum (Ranunculaceae)","volume":"9","author":"He","year":"2019","journal-title":"Sci. Rep."},{"key":"B38","article-title":"Primulaceae","volume-title":"Flora of China","author":"Hu","year":"1996"},{"key":"B39","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1186\/s12870-022-03643-4","article-title":"Comprehensive analysis of complete chloroplast genome and phylogenetic aspects of ten Ficus species","volume":"22","author":"Huang","year":"2022","journal-title":"BMC Plant Biol."},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.17956","article-title":"Presence versus absence of CYP734A50 underlies the style-length dimorphism in primroses","volume":"5","author":"Huu","year":"2016","journal-title":"Elife"},{"key":"B41","doi-asserted-by":"publisher","first-page":"23148","DOI":"10.1073\/pnas.2006296117","article-title":"Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene","volume":"117","author":"Huu","year":"2020","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B42","doi-asserted-by":"publisher","first-page":"19369","DOI":"10.1073\/pnas.0709121104","article-title":"Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns","volume":"104","author":"Jansen","year":"2007","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B43","unstructured":"Jiaxin\n              W.\n            \n          \n          Beijing\n          University of Chinese Academy of Sciences\n          Genetic effects of mating system shifts in primula\n          \n          2020"},{"key":"B44","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1186\/s13059-020-02154-5","article-title":"GetOrganelle: A fast and versatile toolkit for accurate de novo assembly of organelle genomes","volume":"21","author":"Jin","year":"2020","journal-title":"Genome Biol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"159","DOI":"10.2475\/03.2019.01","article-title":"Mesozoic-Cenozoic geological evolution of the Himalayan-Tibetan orogen and working tectonic hypotheses","volume":"319","author":"Kapp","year":"2019","journal-title":"Am. J. Sci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"521","DOI":"10.5511\/plantbiotechnology.25.521","article-title":"Unreduced gametes are the major causal factor for the production of polyploid interspecific hybrids in Primula","volume":"25","author":"Kato","year":"2008","journal-title":"Plant Biotechnol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"1300","DOI":"10.3109\/19401736.2014.945566","article-title":"The complete chloroplast genome of Phalaenopsis \"Tiny Star","volume":"27","author":"Kim","year":"2016","journal-title":"Mitochondrial DNA A. DNA Mapp. Seq Anal."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1471","DOI":"10.1093\/aob\/mct267","article-title":"Inflorescences: concepts, function, development and evolution","volume":"112","author":"Kirchoff","year":"2013","journal-title":"Ann. Bot."},{"key":"B49","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1111\/j.1365-313X.2005.02533.x","article-title":"The tobacco plastid accD gene is essential and is required for leaf development","volume":"44","author":"Kode","year":"2005","journal-title":"Plant J."},{"key":"B50","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1139\/g11-026","article-title":"Complete chloroplast genome sequence of Magnolia kwangsiensis (Magnoliaceae): implication for DNA barcoding and population genetics","volume":"54","author":"Kuang","year":"2011","journal-title":"Genome"},{"key":"B51","doi-asserted-by":"publisher","first-page":"4633","DOI":"10.1093\/nar\/29.22.4633","article-title":"REPuter: the manifold applications of repeat analysis on a genomic scale","volume":"29","author":"Kurtz","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.3390\/genes13040567","article-title":"The complete chloroplast genomes of Primula obconica provide insight that neither species nor natural section represent monophyletic taxa in Primula (Primulaceae)","volume":"13","author":"Li","year":"2022","journal-title":"Genes (Basel)"},{"key":"B53","doi-asserted-by":"publisher","first-page":"73","DOI":"10.3897\/phytokeys.248.127117","article-title":"Primula meishanensis (primulaceae), a new species from sichuan, China","volume":"248","author":"Li","year":"2024","journal-title":"PhytoKeys"},{"key":"B54","doi-asserted-by":"publisher","first-page":"47","DOI":"10.3897\/phytokeys.218.91161","article-title":"Primula wolongensis (Primulaceae), a new species of the primrose from Sichuan, China","volume":"218","author":"Li","year":"2023","journal-title":"PhytoKeys"},{"key":"B55","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1186\/s12870-023-04034-z","article-title":"Insights into the phylogeny and chloroplast genome evolution of Eriocaulon (Eriocaulaceae)","volume":"23","author":"Li","year":"2023","journal-title":"BMC Plant Biol."},{"key":"B56","doi-asserted-by":"publisher","first-page":"1731","DOI":"10.1104\/pp.20.01185","article-title":"Molecular basis for chemical evolution of flavones to flavonols and anthocyanins in land plants","volume":"184","author":"Li","year":"2020","journal-title":"Plant Physiol."},{"key":"B57","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.abc7741","article-title":"Orographic evolution of northern Tibet shaped vegetation and plant diversity in eastern Asia","volume":"7","author":"Li","year":"2021","journal-title":"Sci. Adv."},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2025.1653128","article-title":"Organelle genomes reveal adaptive evolution and phylogenetic position of the endangered Primula mallophylla","volume":"16","author":"Li","year":"2025","journal-title":"Front. Plant Sci."},{"key":"B59","doi-asserted-by":"publisher","DOI":"10.3389\/fgene.2020.00802","article-title":"The complete chloroplast genome sequences of 14 curcuma species: Insights into genome evolution and phylogenetic relationships within zingiberales","volume":"11","author":"Liang","year":"2020","journal-title":"Front. Genet."},{"key":"B60","doi-asserted-by":"publisher","first-page":"1451","DOI":"10.1093\/bioinformatics\/btp187","article-title":"DnaSP v5: a software for comprehensive analysis of DNA polymorphism data","volume":"25","author":"Librado","year":"2009","journal-title":"Bioinformatics"},{"key":"B61","unstructured":"Liu\n              T.\n            \n          \n          Guangzhou\n          South China Agricultural University\n          Phylogenomic study of primula based on transcriptome data\n          \n          2018"},{"key":"B62","doi-asserted-by":"publisher","DOI":"10.3390\/ijms242216130","article-title":"Complete chloroplast genome of Hypericum perforatum and dynamic evolution in Hypericum (Hypericaceae)","volume":"24","author":"Liu","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"B63","doi-asserted-by":"publisher","first-page":"21796","DOI":"10.1073\/pnas.2004405117","article-title":"Synthetic conversion of leaf chloroplasts into carotenoid-rich plastids reveals mechanistic basis of natural chromoplast development","volume":"117","author":"Llorente","year":"2020","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B64","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1186\/s12864-021-07807-8","article-title":"Comparative chloroplast genome analysis of Impatiens species (Balsaminaceae) in the karst area of China: insights into genome evolution and phylogenomic implications","volume":"22","author":"Luo","year":"2021","journal-title":"BMC Genomics"},{"key":"B65","doi-asserted-by":"publisher","first-page":"1054","DOI":"10.1186\/s12870-024-05761-7","article-title":"Deciphering the complex organelle genomes of two Rhododendron species and insights into adaptive evolution patterns in high-altitude","volume":"24","author":"Lyu","year":"2024","journal-title":"BMC Plant Biol."},{"key":"B66","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1111\/jse.12077","article-title":"Evidence for natural hybridization between Primula beesiana and P. bulleyana, two heterostylous primroses in NW Yunnan, China","volume":"52","author":"Ma","year":"2014","journal-title":"J. Syst. Evol."},{"key":"B67","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0067350","article-title":"The complete chloroplast genome of banana (Musa acuminata, Zingiberales): insight into plastid monocotyledon evolution","volume":"8","author":"Martin","year":"2013","journal-title":"PloS One"},{"key":"B68","doi-asserted-by":"publisher","first-page":"439","DOI":"10.1111\/j.1469-8137.2006.01833.x","article-title":"The primrose path to heterostyly","volume":"171","author":"Mast","year":"2006","journal-title":"New Phytol."},{"key":"B69","doi-asserted-by":"publisher","first-page":"926","DOI":"10.3732\/ajb.91.6.926","article-title":"Buzz-pollinated Dodecatheon originated from within the heterostylous Primula subgenus Auriculastrum (Primulaceae): a seven-region cpDNA phylogeny and its implications for floral evolution","volume":"91","author":"Mast","year":"2004","journal-title":"Am. J. Bot."},{"key":"B70","doi-asserted-by":"publisher","first-page":"1109","DOI":"10.1016\/j.cell.2020.07.020","article-title":"A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens","volume":"182","author":"Medina-Puche","year":"2020","journal-title":"Cell"},{"key":"B71","doi-asserted-by":"publisher","first-page":"D30","DOI":"10.1093\/nar\/gkae978","article-title":"Database resources of the national genomics data center, China National Center for bioinformation in 2025","volume":"53","year":"2024","journal-title":"Nucleic Acids Res."},{"key":"B72","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1007\/s11105-016-1013-z","article-title":"Phylogeography of Achyranthes bidentata (Amaranthaceae) in China\u2019s warm-temperate zone inferred from chloroplast and nuclear DNA: insights into population dynamics in response to climate change during the Pleistocene","volume":"35","author":"Miao","year":"2017","journal-title":"Plant Mol. Biol. Rep."},{"key":"B73","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1105\/tpc.13.3.645","article-title":"Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus","volume":"13","author":"Millen","year":"2001","journal-title":"Plant Cell"},{"key":"B74","doi-asserted-by":"publisher","first-page":"19363","DOI":"10.1073\/pnas.0708072104","article-title":"Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms","volume":"104","author":"Moore","year":"2007","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B75","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1146\/annurev.arplant.51.1.111","article-title":"Nonphotosynthetic metabolism in plastids","volume":"51","author":"Neuhaus","year":"2000","journal-title":"Annu. Rev. Plant Physiol. Plant Mol. Biol."},{"key":"B76","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.31083\/j.fbl2806110","article-title":"Chloroplast genome structure and phylogenetic analysis of 13 Lamiaceae plants in Tibet","volume":"28","author":"Niu","year":"2023","journal-title":"Front. Biosci. (Landmark Ed)"},{"key":"B78","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1007\/s11033-021-06749-4","article-title":"Codon usage bias","volume":"49","author":"Parvathy","year":"2022","journal-title":"Mol. Biol. Rep."},{"key":"B79","doi-asserted-by":"publisher","first-page":"7759","DOI":"10.1073\/pnas.92.17.7759","article-title":"Polymorphic simple sequence repeat regions in chloroplast genomes: applications to the population genetics of pines","volume":"92","author":"Powell","year":"1995","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B80","doi-asserted-by":"publisher","first-page":"1452","DOI":"10.1126\/science.1140429","article-title":"Evolution and development of inflorescence architectures","volume":"316","author":"Prusinkiewicz","year":"2007","journal-title":"Science"},{"key":"B81","doi-asserted-by":"publisher","first-page":"1114","DOI":"10.1126\/science.aax0151","article-title":"Building mountain biodiversity: geological and evolutionary processes","volume":"365","author":"Rahbek","year":"2019","journal-title":"Science"},{"key":"B82","doi-asserted-by":"publisher","first-page":"3437","DOI":"10.1016\/j.jksus.2020.10.003","article-title":"Assessment of inter simple sequence repeat (ISSR) and simple sequence repeat (SSR) markers to reveal genetic diversity among Tamarix ecotypes","volume":"32","author":"Ramzan","year":"2020","journal-title":"J. King Saud Univ. Sci."},{"key":"B83","doi-asserted-by":"publisher","DOI":"10.3390\/plants9091143","article-title":"Phylogenetic and comparative analyses of complete chloroplast genomes of Chinese Viburnum and Sambucus (Adoxaceae)","volume":"9","author":"Ran","year":"2020","journal-title":"Plants (Basel)"},{"key":"B84","doi-asserted-by":"publisher","first-page":"4158","DOI":"10.1002\/ece3.7312","article-title":"Highly variable chloroplast genome from two endangered Papaveraceae lithophytes Corydalis tomentella and Corydalis saxicola","volume":"11","author":"Ren","year":"2021","journal-title":"Ecol. Evol."},{"key":"B85","doi-asserted-by":"publisher","DOI":"10.3390\/ijms19041050","article-title":"Comparative plastid genomes of Primula species: sequence divergence and phylogenetic relationships","volume":"19","author":"Ren","year":"2018","journal-title":"Int. J. Mol. Sci."},{"key":"B86","volume-title":"Primula","author":"Richards","year":"1993"},{"key":"B87","volume-title":"Primula","author":"Richards","year":"2002"},{"key":"B88","doi-asserted-by":"publisher","DOI":"10.1093\/gbe\/evad101","article-title":"The evolutionary constraints on angiosperm chloroplast adaptation","volume":"15","author":"Robbins","year":"2023","journal-title":"Genome Biol. Evol."},{"key":"B89","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1093\/sysbio\/sys029","article-title":"MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space","volume":"61","author":"Ronquist","year":"2012","journal-title":"Syst. Biol."},{"key":"B90","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.4299","article-title":"A 250 plastome phylogeny of the grass family (Poaceae): topological support under different data partitions","volume":"6","author":"Saarela","year":"2018","journal-title":"PeerJ"},{"key":"B91","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.ympev.2012.05.015","article-title":"Phylogenetic analysis of Primula section Primula reveals rampant non-monophyly among morphologically distinct species","volume":"65","author":"Schmidt-Lebuhn","year":"2012","journal-title":"Mol. Phylogenet. Evol."},{"key":"B92","doi-asserted-by":"publisher","DOI":"10.3389\/fgene.2021.674783","article-title":"Gene loss, pseudogenization in plastomes of genus Allium (Amaryllidaceae), and putative selection for adaptation to environmental conditions","volume":"12","author":"Scobeyeva","year":"2021","journal-title":"Front. Genet."},{"key":"B93","doi-asserted-by":"publisher","first-page":"5125","DOI":"10.1093\/nar\/14.13.5125","article-title":"Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes","volume":"14","author":"Sharp","year":"1986","journal-title":"Nucleic Acids Res."},{"key":"B94","doi-asserted-by":"publisher","first-page":"1987","DOI":"10.3732\/ajb.1400398","article-title":"Chloroplast DNA sequence utility for the lowest phylogenetic and phylogeographic inferences in angiosperms: the tortoise and the hare IV","volume":"101","author":"Shaw","year":"2014","journal-title":"Am. J. Bot."},{"key":"B95","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2020.00376","article-title":"Plastome evolution in Dolomiaea (Asteraceae, Cardueae) using phylogenomic and comparative analyses","volume":"11","author":"Shen","year":"2020","journal-title":"Front. Plant Sci."},{"key":"B96","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1017\/s0080456800004828","article-title":"The genus Primula: sections Obconica, Sinenses, Reinii, Pinnatae, Malacoides, Bullatae, Carolinella, Grandis and Denticulata","volume":"61","author":"Smith","year":"1947","journal-title":"Trans. R. Soc. Edinburgh"},{"key":"B97","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1186\/s43008-024-00149-6","article-title":"The complete mitochondrial genomes of five critical phytopathogenic Bipolaris species: features, evolution, and phylogeny","volume":"15","author":"Song","year":"2024","journal-title":"IMA Fungus"},{"key":"B98","doi-asserted-by":"publisher","DOI":"10.1093\/nsr\/nwaa091","article-title":"Why 'the uplift of the Tibetan Plateau' is a myth","volume":"8","author":"Spicer","year":"2021","journal-title":"Natl. Sci. Rev."},{"key":"B99","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.aav2189","article-title":"No high Tibetan Plateau until the Neogene","volume":"5","author":"Su","year":"2019","journal-title":"Sci. Adv."},{"key":"B100","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1007\/BF00015612","article-title":"The chloroplast genome","volume":"19","author":"Sugiura","year":"1992","journal-title":"Plant Mol. Biol."},{"key":"B101","doi-asserted-by":"publisher","first-page":"592","DOI":"10.1186\/s12864-017-3956-3","article-title":"Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family","volume":"18","author":"Sun","year":"2017","journal-title":"BMC Genomics"},{"key":"B102","doi-asserted-by":"publisher","DOI":"10.3390\/genes16010016","article-title":"From species to varieties: How modern sequencing technologies are shaping medicinal plant identification","volume":"16","author":"Wang","year":"2024","journal-title":"Genes (Basel)"},{"key":"B103","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2024.1459533","article-title":"Unraveling the specialized metabolic pathways in medicinal plant genomes: a review","volume":"15","author":"Wang","year":"2024","journal-title":"Front. Plant Sci."},{"key":"B104","doi-asserted-by":"publisher","DOI":"10.1186\/s12862-014-0262-4","article-title":"Analysis of codon usage bias of mitochondrial genome in Bombyx moriand its relation to evolution","volume":"14","author":"Wei","year":"2014","journal-title":"BMC Evol. Biol."},{"key":"B105","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1139\/gen-2016-0129","article-title":"Analysis of codon usage patterns in Morus notabilis based on genome and transcriptome data","volume":"60","author":"Wen","year":"2017","journal-title":"Genome"},{"key":"B106","article-title":"An account of Primula subgenus Sphondylia (Syn. Sect. Floribundae) with a review of the subdivisions of the genus","volume-title":"Studies in Primulaceae. II. Matematisk-Naturvitenskapelig Ser","author":"Wendelbo","year":"1961"},{"key":"B107","doi-asserted-by":"publisher","first-page":"3350","DOI":"10.1093\/bioinformatics\/btv383","article-title":"Bandage: Interactive visualization of de novo genome assemblies","volume":"31","author":"Wick","year":"2015","journal-title":"Bioinformatics"},{"key":"B108","article-title":"Next\u2010generation organellar genomics: Potentials and pitfalls of high\u2010throughput technologies for molecular evolutionary studies and plant systematics","volume-title":"Next\u2010Generation Sequencing in Plant Systematics","author":"Wicke","year":"2015"},{"key":"B109","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1007\/s11103-011-9762-4","article-title":"The evolution of the plastid chromosome in land plants: gene content, gene order, gene function","volume":"76","author":"Wicke","year":"2011","journal-title":"Plant Mol. Biol."},{"key":"B110","doi-asserted-by":"publisher","DOI":"10.3390\/genes14030703","article-title":"Complete chloroplast genome of four Thai native Dioscorea species: Structural, comparative and phylogenetic analyses","volume":"14","author":"Wonok","year":"2023","journal-title":"Genes (Basel)"},{"key":"B111","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/0378-1119(90)90491-9","article-title":"The 'effective number of codons' used in a gene","volume":"87","author":"Wright","year":"1990","journal-title":"Gene"},{"key":"B112","doi-asserted-by":"publisher","DOI":"10.3389\/fgene.2022.878182","article-title":"Comparative analysis of the chloroplast genome for aconitum species: Genome structure and phylogenetic relationships","volume":"13","author":"Xia","year":"2022","journal-title":"Front. Genet."},{"key":"B113","doi-asserted-by":"publisher","first-page":"W587","DOI":"10.1093\/nar\/gkad359","article-title":"Tree visualization by one table (tvBOT): a web application for visualizing, modifying and annotating phylogenetic trees","volume":"51","author":"Xie","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"B114","doi-asserted-by":"publisher","DOI":"10.3897\/imafungus.16.140572","article-title":"The six whole mitochondrial genomes for the Diaporthe species: features, evolution and phylogeny","volume":"16","author":"Xie","year":"2025","journal-title":"IMA Fungus"},{"key":"B115","doi-asserted-by":"publisher","DOI":"10.1002\/ece3.9730","article-title":"Comparative analysis of chloroplast genomes of endangered heterostylous species primula wilsonii and its closely related species","volume":"13","author":"Xie","year":"2023","journal-title":"Ecol. Evol."},{"key":"B116","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1111\/jipb.12546","article-title":"Natural hybridization and reproductive isolation between two Primula species","volume":"59","author":"Xie","year":"2017","journal-title":"J. Integr. Plant Biol."},{"key":"B117","doi-asserted-by":"publisher","first-page":"20782","DOI":"10.1038\/s41598-020-77661-3","article-title":"The complete chloroplast genome sequences of five pinnate-leaved Primula species and phylogenetic analyses","volume":"10","author":"Xu","year":"2020","journal-title":"Sci. Rep."},{"key":"B118","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1111\/j.1759-6831.2010.00068.x","article-title":"Circumscription of Primula subgenus Auganthus (Primulaceae) based on chloroplast DNA sequences","volume":"48","author":"Yan","year":"2010","journal-title":"J. Syst. Evol."},{"key":"B119","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0122903","article-title":"DNA barcoding evaluation and its taxonomic implications in the species-rich genus Primula L. in China","volume":"10","author":"Yan","year":"2015","journal-title":"PloS One"},{"key":"B120","doi-asserted-by":"publisher","first-page":"788","DOI":"10.1111\/jse.13154","article-title":"Revisiting the phylogeny of primulaceae s.l. using whole plastid genomes: Highlighting phylogenetic conflicts and their implications","volume":"63","author":"Yan","year":"2025","journal-title":"J. Syst. Evol."},{"key":"B121","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1304264","article-title":"Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species","volume":"14","author":"Yang","year":"2023","journal-title":"Front. Plant Sci."},{"key":"B122","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1016\/j.ympev.2014.09.028","article-title":"Chloroplast capture and intra- and inter-continental biogeographic diversification in the Asian \u2013 New World disjunct plant genus Osmorhiza (Apiaceae)","volume":"85","author":"Yi","year":"2015","journal-title":"Mol. Phylogenet. Evol."},{"key":"B123","doi-asserted-by":"publisher","DOI":"10.3390\/genes14081597","article-title":"The first complete chloroplast genome of Campanula carpatica: Genome characterization and phylogenetic diversity","volume":"14","author":"Yoon","year":"2023","journal-title":"Genes (Basel)"},{"key":"B124","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.ympev.2015.03.008","article-title":"RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography","volume":"87","author":"Yu","year":"2015","journal-title":"Mol. Phylogenet. Evol."},{"key":"B125","doi-asserted-by":"publisher","first-page":"193","DOI":"10.3732\/ajb.1100394","article-title":"Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences","volume":"99","author":"Zalapa","year":"2012","journal-title":"Am. J. Bot."},{"key":"B126","doi-asserted-by":"publisher","DOI":"10.1093\/gpbjnl\/qzaf072","article-title":"The GSA family in 2025: A broadened sharing platform for multi-omics and multimodal data","volume":"23","author":"Zhang","year":"2025","journal-title":"Genomics Proteomics Bioinf."},{"key":"B127","doi-asserted-by":"publisher","DOI":"10.3390\/ijms25168689","article-title":"Comparative chloroplast genomes analysis provided adaptive evolution insights in Medicago ruthenica","volume":"25","author":"Zhang","year":"2024","journal-title":"Int. J. Mol. Sci."},{"key":"B128","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1111\/j.1744-7909.2007.00404.x","article-title":"Comparative analysis of codon usage patterns among mitochondrion, chloroplast and nuclear genes in Triticum aestivum L","volume":"49","author":"Zhang","year":"2007","journal-title":"J. Integr. Plant Biol."},{"key":"B129","doi-asserted-by":"publisher","first-page":"43","DOI":"10.3897\/zookeys.1173.102786","article-title":"Complete mitochondrial genomes of the slugs Deroceras laeve (Agriolimacidae) and Ambigolimax valentianus (Limacidae) provide insights into the phylogeny of Stylommatophora (Mollusca, Gastropoda)","volume":"1173","author":"Zhao","year":"2023","journal-title":"ZooKeys"},{"key":"B130","doi-asserted-by":"publisher","DOI":"10.3390\/ijms17071084","article-title":"Comparative analysis of the chloroplast genomic information of cunninghamia lanceolata (lamb.) hook with sibling species from the genera cryptomeria D. Don, Taiwania hayata, and calocedrus kurz","volume":"17","author":"Zheng","year":"2016","journal-title":"Int. J. Mol. Sci."},{"key":"B131","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1038\/35075035","article-title":"Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times","volume":"411","author":"Zhisheng","year":"2001","journal-title":"Nature"},{"key":"B132","doi-asserted-by":"publisher","first-page":"1290","DOI":"10.1111\/nph.15905","article-title":"Phylogenomic analysis reveals multiple evolutionary origins of selfing from outcrossing in a lineage of heterostylous plants","volume":"224","author":"Zhong","year":"2019","journal-title":"New Phytol."},{"key":"B133","doi-asserted-by":"publisher","first-page":"1368","DOI":"10.1111\/nph.14453","article-title":"Phylogeographic insights on the evolutionary breakdown of heterostyly","volume":"214","author":"Zhou","year":"2017","journal-title":"New Phytol."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2026.1889564\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T05:33:19Z","timestamp":1789536799000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2026.1889564\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,16]]},"references-count":133,"alternative-id":["10.3389\/fpls.2026.1889564"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2026.1889564","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,16]]},"article-number":"1889564"}}