{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:20:04Z","timestamp":1760145604878,"version":"build-2065373602"},"reference-count":54,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2024,8,5]],"date-time":"2024-08-05T00:00:00Z","timestamp":1722816000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"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":["Plants"],"abstract":"<jats:p>The flowering plants (angiosperms) are the dominant and defining group of the Earth ecosystems today. However, from which group and by what way flowers, especially their gynoecia (the key characteristic organs of angiosperms), are derived have been key questions in botany, and have remained unanswered despite botanists\u2019 efforts over centuries. Such an embarrassing situation can be attributed to the lack of plants with partially enclosed ovules, which are supposed fill a position between gymnosperms and angiosperms. Here, we report a fossil plant that has apparent coniferous vegetative and reproductive characters but has a single seed partially wrapped by the subtending bract. Such a morphology suggests that a carpel of some angiosperms is equivalent to a lateral appendage (a bract plus its axillary seed) of this fossil. Such a non-traditional interpretation of the homology of angiosperm carpels is compatible with various new progresses made in botany and is in line with Tomlinson\u2019s recent hypothesis. Together with other fossil evidence reported recently, it appears that gynoecia in angiosperms are derived in multiple ways.<\/jats:p>","DOI":"10.3390\/plants13152162","type":"journal-article","created":{"date-parts":[[2024,8,5]],"date-time":"2024-08-05T11:28:54Z","timestamp":1722857334000},"page":"2162","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Shaolinia: A Fossil Link between Conifers and Angiosperms"],"prefix":"10.3390","volume":"13","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, CAS Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Li-Jun","family":"Chen","sequence":"additional","affiliation":[{"name":"Shenzhen Key Laboratory for Orchid Conservation and Utilization, National Orchid Conservation Center of China and Orchid Conservation & Research Center of Shenzhen, Shenzhen 518114, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,8,5]]},"reference":[{"key":"ref_1","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_2","doi-asserted-by":"crossref","unstructured":"Wang, X. (2018). The Dawn Angiosperms, Springer. [2nd ed.].","DOI":"10.1007\/978-3-319-58325-9"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1007\/s12229-012-9104-5","article-title":"Rescuing Robert Brown-The origins of angio-ovuly in seed cones of conifers","volume":"78","author":"Tomlinson","year":"2012","journal-title":"Bot. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1111\/j.1095-8339.1907.tb01074.x","article-title":"On the origin of angiosperms","volume":"38","author":"Arber","year":"1907","journal-title":"J. Linn. Soc. Lond. Bot."},{"key":"ref_5","first-page":"335","article-title":"TOUSLED participates in apical tissue formation during gynoecium development in Arabidopsis","volume":"9","author":"Roe","year":"1997","journal-title":"Plant Cell"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Zhang, X., Liu, W., and Wang, X. (2017). How the ovules get enclosed in magnoliaceous carpels. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0174955"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Guo, X.-M., Xiao, X., Wang, G.-X., and Gao, R.-F. (2013). Vascular anatomy of kiwi fruit and its implications for the origin of carpels. Front. Plant Sci., 4.","DOI":"10.3389\/fpls.2013.00391"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1186\/1999-3110-55-28","article-title":"From leaf and branch into a flower: Magnolia tells the story","volume":"55","author":"Liu","year":"2014","journal-title":"Bot. Stud."},{"key":"ref_9","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_10","doi-asserted-by":"crossref","first-page":"53","DOI":"10.4236\/ajps.2013.412A1008","article-title":"Mechanical pressure, not genes, makes ovulate parts leaf-like in Cycas","volume":"4","author":"Wang","year":"2013","journal-title":"Am. J. Plant Sci."},{"key":"ref_11","first-page":"97","article-title":"Breaking the stasis of current plant systematics","volume":"33","author":"Wang","year":"2015","journal-title":"Sci. Technol. Rev."},{"key":"ref_12","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_13","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1111\/1755-6724.12100","article-title":"A new angiosperm genus from the Lower Cretaceous Yixian Formation, Western Liaoning, China","volume":"87","author":"Han","year":"2013","journal-title":"Acta Geol. Sin. Engl. Ed."},{"key":"ref_14","first-page":"1","article-title":"A Dichocarpum-like angiosperm from the Early Cretaceous of China","volume":"90","author":"Han","year":"2017","journal-title":"Acta Geol. Sin. Engl. Ed."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1111\/1755-6724.12592","article-title":"A whole plant herbaceous angiosperm from the Middle Jurassic of China","volume":"90","author":"Han","year":"2016","journal-title":"Acta Geol. Sin. Engl. Ed."},{"key":"ref_16","first-page":"419","article-title":"Zhangwuia: An enigmatic organ with bennettitalean appearance and enclosed ovules","volume":"108","author":"Liu","year":"2019","journal-title":"Earth Environ. Sci. Trans. R. Soc. Edinb."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1080\/08912963.2015.1020423","article-title":"A perfect flower from the Jurassic of China","volume":"28","author":"Liu","year":"2016","journal-title":"Hist. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1080\/08912963.2016.1178740","article-title":"Yuhania: A unique angiosperm from the Middle Jurassic of Inner Mongolia, China","volume":"29","author":"Liu","year":"2017","journal-title":"Hist. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1086\/699665","article-title":"Whole-plant reconstruction and updated phylogeny of Austrohamia acanthobractea (Cupressaceae) from the Middle Jurassic of Northeast China","volume":"179","author":"Dong","year":"2018","journal-title":"Int. J. Plant Sci."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Yang, Y., Lin, L., and Wang, Q. (2013). Chengia laxispicata gen. et sp. nov., a new ephedroid plant from the Early Cretaceous Yixian Formation of western Liaoning, Northeast China: Evolutionary, taxonomic, and biogeographic implications. BMC Evol. Biol., 13.","DOI":"10.1186\/1471-2148-13-72"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Yang, Y., Wang, Y., and Ferguson, D.K. (2020). A new macorfossil ephedroid plant with unusual bract morphology from the Lower Cretaceous Jiufotang Formation of northeastern China. BMC Evol. Biol., 20.","DOI":"10.1186\/s12862-019-1569-y"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Yang, Y., and Wang, Q. (2013). The earliest fleshy cone of Ephedra from the Early Cretaceous Yixian Formation of Northeast China. PLoS ONE, 8.","DOI":"10.1371\/annotation\/d1b28569-d9c0-4812-8332-9a6bfa9eb27f"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Han, L., Zhao, Y., Zhao, M., Sun, J., Sun, B., and Wang, X. (2023). New fossil evidence suggests that angiosperms flourished in the Middle Jurassic. Life, 13.","DOI":"10.3390\/life13030819"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Santos, A.A., and Wang, X. (2022). Pre-Carpels from the Middle Triassic of Spain. Plants, 11.","DOI":"10.3390\/plants11212833"},{"key":"ref_25","unstructured":"Taylor, T.N., Taylor, E.L., and Krings, M. (2009). Paleobotany: The Biology and Evolution of Fossil Plants, Elsevier. [2nd ed.]."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"716","DOI":"10.2307\/2399221","article-title":"Phylogenetic analysis of seed plants and the origin of angiosperms","volume":"72","author":"Crane","year":"1985","journal-title":"Ann. Mo. Bot. Gard."},{"key":"ref_27","unstructured":"Scott, D.H. (1962). Studies in Fossil Botany, Vol. I. Pteridophyta, Hafner Publishing Company. [3rd ed.]."},{"key":"ref_28","first-page":"547","article-title":"The morphology of the female fructifications in cordaites and conifers of Palaeozoic age","volume":"36","author":"Florin","year":"1939","journal-title":"Bot. Not."},{"key":"ref_29","first-page":"457","article-title":"Die Koniferen des Oberkarbons und des unteren Perms","volume":"85","author":"Florin","year":"1944","journal-title":"Pal\u00e4ontographica B"},{"key":"ref_30","first-page":"655","article-title":"Die Koniferen des Oberkarbons und des unteren Perms","volume":"85","author":"Florin","year":"1945","journal-title":"Pal\u00e4ontographica B"},{"key":"ref_31","first-page":"285","article-title":"Evolution in cordaites and conifers","volume":"15","author":"Florin","year":"1951","journal-title":"Acta Horti Bergiani"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1086\/589887","article-title":"Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower","volume":"169","author":"Doyle","year":"2008","journal-title":"Int. J. Plant Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"S32","DOI":"10.1105\/tpc.015933","article-title":"Regulation of ovule development","volume":"16","author":"Skinner","year":"2004","journal-title":"Plant Cell"},{"key":"ref_34","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_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2307\/4120346","article-title":"A new theory of the angiosperm flower: I. The gynoecium","volume":"16","author":"Melville","year":"1962","journal-title":"Kew Bull."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"200","DOI":"10.11646\/phytotaxa.416.3.1","article-title":"Floral ontogeny of Illicium lanceolatum (Schisandraceae) and its implications on carpel homology","volume":"416","author":"Zhang","year":"2019","journal-title":"Phytotaxa"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/0169-5347(91)90025-S","article-title":"The origin of angiosperms: New and old problems","volume":"6","author":"Krassilov","year":"1991","journal-title":"Trends Ecol. Evol."},{"key":"ref_38","first-page":"100","article-title":"Dirhopalostachyaceae\u2014A new family of proangiosperms and its bearing on the problem of angiosperm ancestry","volume":"153","author":"Krassilov","year":"1975","journal-title":"Pal\u00e4ontographica B"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1111\/1755-6724.14591","article-title":"A new infructescence of angiosperms from the Early Cretaceous of China","volume":"94","author":"Han","year":"2020","journal-title":"Acta Geol. Sin. Engl. Ed."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.palwor.2020.03.008","article-title":"A whole-plant monocot from Lower Cretaceous","volume":"30","author":"Liu","year":"2021","journal-title":"Palaeoworld"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1293","DOI":"10.1111\/1755-6724.13627","article-title":"A novel angiosperm from the Early Cretaceous and its implications on carpel-deriving","volume":"92","author":"Liu","year":"2018","journal-title":"Acta Geol. Sin. Engl. Ed."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2706","DOI":"10.1080\/08912963.2020.1825411","article-title":"A novel angiosperm including various parts from the Early Cretaceous sheds new light on flower evolution","volume":"33","author":"Liu","year":"2021","journal-title":"Hist. Biol."},{"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":"Friis, E.M., Crane, P.R., and Pedersen, K.R. (2011). The Early Flowers and Angiosperm Evolution, Cambridge University Press.","DOI":"10.1017\/CBO9780511980206"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1080\/00173134.2014.932431","article-title":"Fossil Kajanthus lusitanicus gen. et sp. nov. from Portugal: Floral evidence for Early Cretaceous Lardizabalaceae (Ranunculales, basal eudicot)","volume":"53","author":"Mendes","year":"2014","journal-title":"Grana"},{"key":"ref_46","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_47","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1139\/b03-004","article-title":"Aspects of inflorescence and floral development in the putative basal angiosperm Amborella trichopoda (Amborellaceae)","volume":"81","author":"Posluszny","year":"2003","journal-title":"Can. J. Bot."},{"key":"ref_48","first-page":"1","article-title":"The Jurassic disseminules with pappus and their bearing on the problem of angiosperm ancestry","volume":"3","author":"Krassilov","year":"1973","journal-title":"Geophytology"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1007\/BF02860852","article-title":"The origin of angiosperms","volume":"43","author":"Krassilov","year":"1977","journal-title":"Bot. Rev."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"577","DOI":"10.2307\/2399038","article-title":"New paleobotanical data on origin and early evolution of angiospermy","volume":"71","author":"Krassilov","year":"1984","journal-title":"Ann. Mo. Bot. Gard."},{"key":"ref_51","first-page":"289","article-title":"Synopsis of a new \u201cpolyphyletic-polychronic-polytopic\u201d system of the angiosperms","volume":"40","author":"Wu","year":"2002","journal-title":"Acta Phytotaxon. Sin."},{"key":"ref_52","unstructured":"Syvanen, M., and Kado, C.I. (2002). Character parallelism and reticulation in the origin of angiosperms. Horizontal Gene Transfer, Academic Press."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"159","DOI":"10.11648\/j.jps.20140205.13","article-title":"Carpel-fruit in a coniferous genus Araucaria and the enigma of angiosperm origin","volume":"2","author":"Krassilov","year":"2014","journal-title":"J. Plant Sci."},{"key":"ref_54","first-page":"163","article-title":"Offspring development conditioning (ODC): A universal evolutionary trend in sexual reproduction of organisms","volume":"51","author":"Fu","year":"2021","journal-title":"J. Northwest Univ. Nat. Sci. Ed."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/15\/2162\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:30:07Z","timestamp":1760110207000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/15\/2162"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,5]]},"references-count":54,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2024,8]]}},"alternative-id":["plants13152162"],"URL":"https:\/\/doi.org\/10.3390\/plants13152162","relation":{},"ISSN":["2223-7747"],"issn-type":[{"type":"electronic","value":"2223-7747"}],"subject":[],"published":{"date-parts":[[2024,8,5]]}}}