{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,1]],"date-time":"2026-02-01T10:38:13Z","timestamp":1769942293134,"version":"3.49.0"},"reference-count":58,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2025,2,12]],"date-time":"2025-02-12T00:00:00Z","timestamp":1739318400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2024YFF0807601"],"award-info":[{"award-number":["2024YFF0807601"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["42288201"],"award-info":[{"award-number":["42288201"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2024YFF0807601"],"award-info":[{"award-number":["2024YFF0807601"]}],"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":["42288201"],"award-info":[{"award-number":["42288201"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>\u201cHow old are angiosperms\u201d is a frequently asked but still unanswered question. Although the underlying reason includes a lack of consensus on the criterion for fossil angiosperms, limited fossil finds, and other factors, the final answer to the question apparently lies in fossils, not wrangling among different schools. The currently mainstream idea in palaeobotany is that angiosperms cannot have existed earlier than the Early Cretaceous. This 64-year-old stereotype was recently iterated again in 2017. However, another hard-to-ignore fact is that this view is challenged by increasing pre-Cretaceous fossil evidence of angiosperms as well as molecular clock estimates. Here, we report a Permian angiosperm, Yuzhoua gen. nov. from Henan Province, China. This fossil plant has enclosed ovules, a defining feature idiosyncratic of angiosperms. In addition, a conspicuous style is seen on the top of the ovary, underscoring its distinction from known fossil seeds in gymnosperms. The combination of the Permian (Palaeozoic) age and these two unique features of Yuzhoua indicates that angiosperms first appeared much earlier than widely accepted, implying a much longer history of flowering plants. The occurrence of four specimens preserved in various states and unique morphology of Yuzhoua are beyond the expectations of all known theories on plant evolution, shedding new light on a previously unknown aspect of plant evolution in geological history.<\/jats:p>","DOI":"10.3390\/life15020286","type":"journal-article","created":{"date-parts":[[2025,2,12]],"date-time":"2025-02-12T10:25:57Z","timestamp":1739355957000},"page":"286","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Yuzhoua juvenilis: Another Angiosperm Seen in the Early Permian?"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4053-5515","authenticated-orcid":false,"given":"Xin","family":"Wang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and CAS Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yinggang","family":"Lei","sequence":"additional","affiliation":[{"name":"School of Materials Science and Engineering, Henan University of Science and Technology, Luoyang 471000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qiang","family":"Fu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and CAS Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China"},{"name":"University of Chinese Academy of Sciences, Nanjing (UCASNJ), Nanjing 211135, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,2,12]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"29","DOI":"10.2307\/2405502","article-title":"A theory of angiosperm evolution","volume":"6","author":"Axelord","year":"1952","journal-title":"Evolution"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Stebbins, G.L. (1974). Flowering Plants: Evolution Above Species Level, Harvard University Press.","DOI":"10.4159\/harvard.9780674864856"},{"key":"ref_3","first-page":"284","article-title":"How old are the angiosperms?","volume":"258-A","author":"Scott","year":"1960","journal-title":"Am. J. Sci."},{"key":"ref_4","first-page":"231","article-title":"The leaf venation and reproductive structures of a late Triassic angiosperm, Sanmiguelia lewisii","volume":"7","author":"Cornet","year":"1986","journal-title":"Evol. Theory"},{"key":"ref_5","first-page":"37","article-title":"Late Triassic angiosperm-like pollen from the Richmond rift basin of Virginia, USA","volume":"213","author":"Cornet","year":"1989","journal-title":"Pal\u00e4ontographica B"},{"key":"ref_6","first-page":"25","article-title":"The reproductive morphology and biology of Sanmiguelia lewisii, and its bearing on angiosperm evolution in the late Triassic","volume":"3","author":"Cornet","year":"1989","journal-title":"Evol. Trends Plants"},{"key":"ref_7","first-page":"81","article-title":"Dicot-like leaf and flowers from the Late Triassic tropical Newark Supergroup rift zone, U.S.A","volume":"19","author":"Cornet","year":"1993","journal-title":"Mod. Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/0034-6667(92)90167-F","article-title":"Angiosperm-like pollen from the ammonite-dated Oxfordian (Upper Jurassic) of France","volume":"71","author":"Cornet","year":"1992","journal-title":"Rev. Palaeobot. Palynol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1144\/jm.23.2.97","article-title":"A boreal early cradle of angiosperms? angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway)","volume":"23","author":"Hochuli","year":"2004","journal-title":"J. Micropalaeontol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Hochuli, P.A., and Feist-Burkhardt, S. (2013). Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (Northern Switzerland). Front. Plant Sci., 4.","DOI":"10.3389\/fpls.2013.00344"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1111\/j.1759-6831.2010.00090.x","article-title":"Schmeissneria: An angiosperm from the Early Jurassic","volume":"48","author":"Wang","year":"2010","journal-title":"J. Syst. Evol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Wang, X. (2018). The Dawn Angiosperms, Springer. [2nd ed.].","DOI":"10.1007\/978-3-319-58325-9"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Wang, X., Duan, S., Geng, B., Cui, J., and Yang, Y. (2007). Schmeissneria: A missing link to angiosperms?. BMC Evol. Biol., 7.","DOI":"10.1186\/1471-2148-7-14"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"371","DOI":"10.26502\/jbb.2642-91280099","article-title":"Taiyuanostachya: An abominable angiosperm from the Early Permian of China","volume":"6","author":"Wang","year":"2023","journal-title":"J. Biotechnol. Biomed."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1038\/s41477-019-0421-0","article-title":"Origin of angiosperms and the puzzle of the Jurassic gap","volume":"5","author":"Li","year":"2019","journal-title":"Nat. Plants"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1038\/s41586-024-07324-0","article-title":"Phylogenomics and the rise of the angiosperms","volume":"629","author":"Zuntini","year":"2024","journal-title":"Nature"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"17015","DOI":"10.1038\/nplants.2017.15","article-title":"Palaeobotanical redux: Revisiting the age of the angiosperms","volume":"3","author":"Herendeen","year":"2017","journal-title":"Nat. Plants"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1111\/nph.15974","article-title":"Supposed Jurassic angiosperms lack pentamery, an important angiosperm-specific feature","volume":"228","author":"Sokoloff","year":"2020","journal-title":"New Phytol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1093\/jxb\/erz411","article-title":"Hunting the snark: The flawed search for mythical Jurassic angiosperms","volume":"71","author":"Bateman","year":"2020","journal-title":"J. Exp. Bot."},{"key":"ref_20","first-page":"91","article-title":"Criterion is a touchstone in study of early angiosperms","volume":"6","author":"Wang","year":"2021","journal-title":"Open J. Plant Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1692","DOI":"10.1126\/science.282.5394.1692","article-title":"In search of the first flower: A Jurassic angiosperm, Archaefructus, from Northeast China","volume":"282","author":"Sun","year":"1998","journal-title":"Science"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1250","DOI":"10.1139\/b02-112","article-title":"Seed cone structure in conifers in relation to development and pollination: A biological approach","volume":"80","author":"Tomlinson","year":"2002","journal-title":"Can. J. Bot."},{"key":"ref_23","unstructured":"Yang, G. (2006). The Permian Cathaysian Flora in Western Henan Province, China\u2013Yuzhou Flora, Geological Publishing House."},{"key":"ref_24","first-page":"319","article-title":"Current studies of gigantopterids","volume":"1","author":"Li","year":"1983","journal-title":"Palaeontol. Cathayana"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1130\/G48051.1","article-title":"High-precision U-Pb age constraints on the Permian floral turnovers, paleoclimate change, and tectonics of the North China block","volume":"49","author":"Wu","year":"2021","journal-title":"Geology"},{"key":"ref_26","unstructured":"Harper, D.R. (2025, February 08). The Online Etymology Dictionary. Available online: https:\/\/www.etymonline.com\/search?q=angiosperm."},{"key":"ref_27","unstructured":"Wu, Z.-Y., Lu, A.-M., Tang, Y.-C., Chen, Z.-D., and Li, D.-Z. (2003). The Families and Genera of Angiosperms in China, A Comprehensive Analysis, Science Press."},{"key":"ref_28","first-page":"343","article-title":"Pliocene floras of western Sichuan","volume":"17","author":"Guo","year":"1978","journal-title":"Acta Palaeontol. Sin."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1086\/701819","article-title":"Hedyosmum-like fossils in the Early Cretaceous diversification of angiosperms","volume":"180","author":"Friis","year":"2019","journal-title":"Int. J. Plant Sci."},{"key":"ref_30","unstructured":"Cronquist, A. (1988). The evolution and Classification of Flowering Plants, New York Botanical Garden. [2nd ed.]."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Eames, A.J. (1961). Morphology of the Angiosperms, McGraw-Hill Book Company, Inc.","DOI":"10.5962\/bhl.title.5986"},{"key":"ref_32","unstructured":"Takhtajan, A. (1969). Flowering Plants, Origin and Dispersal, Oliver AND Boyd Ltd."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1111","DOI":"10.1086\/321919","article-title":"The flowers in extant basal angiosperms and inferences on ancestral flowers","volume":"162","author":"Endress","year":"2001","journal-title":"Int. J. Plant Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1098\/rstb.2009.0228","article-title":"The evolution of floral biology in basal angiosperms","volume":"365","author":"Endress","year":"2010","journal-title":"Philos. Trans. R. Soc. B: Biol. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/boj.12099","article-title":"Multicarpellate gynoecia in angiosperms: Occurrence, development, organization and architectural constraints","volume":"174","author":"Endress","year":"2014","journal-title":"Bot. J. Linn. Soc."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1093\/botlinnean\/boy083","article-title":"The morphological relationship between carpels and ovules in angiosperms: Pitfalls of morphological interpretation","volume":"189","author":"Endress","year":"2019","journal-title":"Bot. J. Linn. Soc."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.12705\/646.1","article-title":"Ancestral traits and specializations in the flowers of the basal grade of living angiosperms","volume":"64","author":"Endress","year":"2015","journal-title":"Taxon"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"S211","DOI":"10.1086\/317572","article-title":"Gynoecium structure and evolution in basal angiosperms","volume":"161","author":"Endress","year":"2000","journal-title":"Int. J. Plant Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1038\/46536","article-title":"The earliest angiosperms: Evidence from mitochondrial, plastid and nuclear genomes","volume":"402","author":"Qiu","year":"1999","journal-title":"Nature"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Wang, Y., Li, Y.-D., Wang, S., Tihelka, E., Engel, M.S., and Cai, C. (2024). Modeling compositional heterogeneity resolves deep phylogeny of flowering plants. Plant Divers.","DOI":"10.1016\/j.pld.2024.07.007"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"APG (2016). APG IV: An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Bot. J. Linn. Soc., 181, 1\u201320.","DOI":"10.1111\/boj.12385"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"e38827","DOI":"10.7554\/eLife.38827","article-title":"An unexpected noncarpellate epigynous flower from the Jurassic of China","volume":"7","author":"Fu","year":"2018","journal-title":"eLife"},{"key":"ref_43","first-page":"359","article-title":"Nanjinganthus is an angiosperm, isn\u2019t it?","volume":"3","author":"Fu","year":"2020","journal-title":"China Geol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Fu, Q., Hou, Y., Yin, P., Diez, J.B., Pole, M., Garc\u00eda-\u00c1vila, M., and Wang, X. (2023). Micro-CT results exhibit ovules enclosed in the ovaries of Nanjinganthus. Sci. Rep., 13.","DOI":"10.1038\/s41598-022-27334-0"},{"key":"ref_45","first-page":"401","article-title":"A new cycad\u2013Primocycas chinensis gen. et sp. nov. discovered from the Lower Permian in Shanxi, China and its significance","volume":"23","author":"Zhu","year":"1981","journal-title":"Acta Bot. Sin."},{"key":"ref_46","first-page":"1","article-title":"Palaeozoic plants from central Shansi","volume":"2","author":"Halle","year":"1927","journal-title":"Palaeontol. Sin."},{"key":"ref_47","unstructured":"Taylor, T.N., Taylor, E.L., and Krings, M. (2009). Paleobotany: The Biology and Evolution of Fossil Plants, Elsevier. [2nd ed.]."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1002\/j.1537-2197.1960.tb07107.x","article-title":"The comparative morphology and relationships of the Magnoliaceae. III. Carpels","volume":"47","author":"Canright","year":"1960","journal-title":"Am. J. Bot."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1086\/424024","article-title":"Floral developmental morphology of Amborella trichopoda (Amborellaceae)","volume":"165","author":"Buzgo","year":"2004","journal-title":"Int. J. Plant Sci."},{"key":"ref_50","first-page":"107","article-title":"Fossil and living cycads say \u201cNo more megasporophylls\u201d","volume":"1","author":"Miao","year":"2017","journal-title":"J. Morphol. Anat."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1038\/339046a0","article-title":"Molecular evidence for pre-Cretaceous angiosperm origins","volume":"339","author":"Martin","year":"1989","journal-title":"Nature"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1038\/342132a0","article-title":"Angiosperm origins","volume":"342","author":"Martin","year":"1989","journal-title":"Nature"},{"key":"ref_53","unstructured":"Thomas, D., and Pfefferkorn, H.W. (1985). Carboniferous and Permian floral provinces in East Asia. Papers for the 9th International Congress of Carboniferous Stratigraphy and Geology, South Illinois University Press."},{"key":"ref_54","first-page":"129","article-title":"Advances in the studies of paleobotany of China during the last decade","volume":"28","author":"Li","year":"1989","journal-title":"Acta Palaeontol. Sin."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Khramov, A., Foraponova, T., and W\u0119gierek, P. (2023). The earliest pollen-loaded insects from the Lower Permian of Russia. Biol. Lett., 19.","DOI":"10.1098\/rsbl.2022.0523"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1134\/S0013873820070015","article-title":"The fossil record of long-oribscid nectarivorous insects","volume":"100","author":"Khramov","year":"2020","journal-title":"Entomol. Rev."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1016\/j.tree.2023.03.008","article-title":"Insect pollination in deep time","volume":"38","author":"Engel","year":"2023","journal-title":"Trends Ecol. Evol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1126\/science.271.5246.188","article-title":"Permian vessel elements","volume":"271","author":"Li","year":"1996","journal-title":"Science"}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/15\/2\/286\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T16:32:14Z","timestamp":1760027534000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/15\/2\/286"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,2,12]]},"references-count":58,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2025,2]]}},"alternative-id":["life15020286"],"URL":"https:\/\/doi.org\/10.3390\/life15020286","relation":{},"ISSN":["2075-1729"],"issn-type":[{"value":"2075-1729","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,2,12]]}}}