{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T12:50:00Z","timestamp":1789131000170,"version":"build-2803163510"},"reference-count":38,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2025,12,17]],"date-time":"2025-12-17T00:00:00Z","timestamp":1765929600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>\n                    Calcium biomineralization in plants occurs in a variety of patterns such as calcium carbonate cystoliths and calcium oxalate (CaOx) crystals and agglomerates in different forms. CaOx druses and prismatic crystals with sizes between 20\u2013100 \u00b5m are found in large amounts in the leaves of many extant plants, in angiosperms particularly in dicotyledons. In gymnosperms, large CaOx druses are often found in Cycadales and Ginkgo along the leaf veins, while most conifers contain microcrystals of &lt;10 \u00b5m size in the parenchyma. In plant fossils, patterns of calcium biominerals are rarely reported because they usually disappear during fossilization. Traces of CaOx druses have been reported recently in fossils of dicotyledon plant leaves from Oligocene; here the CaOx was replaced by organic or mineral compounds. But there is still no certain report of CaOx druses traces in Paleozoic or Mesozoic fossils. In the study presented here, granular structures in fossil leaves from different sites across the Devonian to the Neogene were investigated and compared with biomineral patterns in extant leaves of gymnosperm and angiosperm trees. These granular structures resembled patterns of CaOx druses in extant leaves in morphology and distribution and were interpreted as probable casts of CaOx druses. Well-preserved angiosperm fossils from various sites such as seed ferns since Devonian, and Ginkgophytae since Carboniferous all showed such granular traces. The diverse chemical composition of these casts of CaOx druses (e.g., pyrite, iron oxide, organic material, SiO\n                    <jats:sub>2<\/jats:sub>\n                    ) depends on fossilization conditions and the chemistry of the surrounding matrix. Good knowledge of the morphology and distribution patterns of biominerals in all relevant plant groups is a basic prerequisite for recognizing their traces in plant fossils. This first extensive study of previously overlooked traces of CaOx druses in plant fossils is a promising step toward a more detailed identification of these fossil microstructures.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0332423","type":"journal-article","created":{"date-parts":[[2025,12,17]],"date-time":"2025-12-17T18:23:56Z","timestamp":1765995836000},"page":"e0332423","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":1,"title":["Detection of traces of calcium oxalate druses in fossil leaves of angiosperms and gymnosperms from different sites and geological periods"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3847-918X","authenticated-orcid":true,"given":"Mahdieh","family":"Malekhosseini","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hans-J\u00fcrgen","family":"Ensikat","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victoria E.","family":"McCoy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1592-0988","authenticated-orcid":true,"given":"Torsten","family":"Wappler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jes","family":"Rust","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,12,17]]},"reference":[{"issue":"3","key":"pone.0332423.ref001","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.tplants.2013.11.002","article-title":"Physiological and ecological significance of biomineralization in plants","volume":"19","author":"H He","year":"2014","journal-title":"Trends Plant Sci"},{"issue":"3","key":"pone.0332423.ref002","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1139\/cjb-2014-0191","article-title":"Towards uncovering evolution of lineage-specific calcium oxalate crystal patterns in Piperales","volume":"93","author":"HT Horner","year":"2015","journal-title":"Botany"},{"issue":"7","key":"pone.0332423.ref003","doi-asserted-by":"crossref","first-page":"591","DOI":"10.3390\/cryst10070591","article-title":"Biocrystals in Plants: A Short Review on Biomineralization Processes and the Role of Phototropins into the Uptake of Calcium","volume":"10","author":"M Cu\u00e9llar-Cruz","year":"2020","journal-title":"Crystals"},{"key":"pone.0332423.ref004","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1016\/S0168-9452(03)00120-1","article-title":"Advances in our understanding of calcium oxalate crystal formation and function in plants","volume":"164","author":"PA Nakata","year":"2003","journal-title":"Plant Sci"},{"issue":"5","key":"pone.0332423.ref005","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1139\/B07-046","article-title":"Diversity of calcium oxalate crystals in Cactaceae","volume":"85","author":"WP Hartl","year":"2007","journal-title":"Can J Bot"},{"issue":"6","key":"pone.0332423.ref006","doi-asserted-by":"crossref","first-page":"432","DOI":"10.3390\/cryst10060432","article-title":"Characterization of Biominerals in Cacteae Species by FTIR","volume":"10","author":"A De la Rosa-Tilapa","year":"2020","journal-title":"Crystals"},{"key":"pone.0332423.ref007","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1146\/annurev.arplant.56.032604.144106","article-title":"Calcium oxalate in plants: formation and function","volume":"56","author":"VR Franceschi","year":"2005","journal-title":"Annu Rev Plant Biol"},{"issue":"1","key":"pone.0332423.ref008","doi-asserted-by":"crossref","first-page":"15959","DOI":"10.1038\/s41598-022-20144-4","article-title":"Traces of calcium oxalate biomineralization in fossil leaves from late Oligocene maar deposits from Germany","volume":"12","author":"M Malekhosseini","year":"2022","journal-title":"Sci Rep"},{"issue":"6","key":"pone.0332423.ref009","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1006\/anbo.1999.0975","article-title":"Calcium Oxalate Crystals in Monocotyledons: A Review of their Structure and Systematics","volume":"84","author":"C Prychid","year":"1999","journal-title":"Annals of Botany"},{"key":"pone.0332423.ref010","first-page":"1","article-title":"Die Sedimentationsgeschichte der Fossillagerst\u00e4tte Rott und ihre Alterseinstufung anhand neuer S\u00e4ugetierfunde (Oberoligoz\u00e4n, Rheinland)","volume":"187","author":"T M\u00f6rs","year":"1995","journal-title":"Courier Forschungsinstitut Senckenberg"},{"key":"pone.0332423.ref011","volume-title":"Fossillagerst\u00e4tte Rott bei Hennef im Siebengebirge. Das Leben an einem subtropischen See vor 25 Millionen Jahren","author":"WV Koenigswald","year":"1996","edition":"2"},{"key":"pone.0332423.ref012","first-page":"3","article-title":"Koniferen der Oberkreide und ihre Relikte im Terti\u00e4r Europas","volume":"45","author":"L Kunzmann","year":"1999","journal-title":"Abhandlungen des Staatlichen Museums f\u00fcr Mineralogie und Geologie Dresden"},{"issue":"4","key":"pone.0332423.ref013","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1111\/j.1096-0031.1985.tb00432.x","article-title":"Phylogenetic relationships in seed plants","volume":"1","author":"PR Crane","year":"1985","journal-title":"Cladistics"},{"issue":"2","key":"pone.0332423.ref014","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1089\/jmf.1998.1.89","article-title":"The anatomical features of powdered Ginkgo biloba L. Leaf as observed by light microscopy","volume":"1","author":"A Raman","year":"1998","journal-title":"Journal of Medicinal Food"},{"key":"pone.0332423.ref015","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1127\/palb\/274\/2006\/1","article-title":"The upper devonian flora of bear island","volume":"274","author":"H-J Schweitzer","year":"2006","journal-title":"palab"},{"key":"pone.0332423.ref016","doi-asserted-by":"crossref","first-page":"353","DOI":"10.3140\/bull.geosci.1192","article-title":"Cuticles of Paripteris gothan, 1941 (Pteridospermopsida) from the Westphalian of Poland","volume":"85","author":"Z \u0160im\u016fnek","year":"2010","journal-title":"Bull Geosci"},{"key":"pone.0332423.ref017","first-page":"1","article-title":"Die Pflanzenfossilien im Westfal D, Stefan und Rotliegend Norddeutschlands. Fortschr. Geol. Rheinld. u","volume":"39","author":"KH Josten","year":"1999","journal-title":"Westf"},{"key":"pone.0332423.ref018","first-page":"1","article-title":"Die oberschlesische steinkohlenflora. I. Teil. Farne und farn\u00e4hnliche gew\u00e4chse (cycadofilices bezw. pteridospermen)","volume":"75","author":"W Gothan","year":"1913","journal-title":"Abh kgl preu\u00df geol L-Anst"},{"key":"pone.0332423.ref019","first-page":"1","article-title":"\u00c9tude sur le flore fossile du Bassin houiller d\u2019H\u00e9racl\u00e9e","volume":"21","author":"R Zeiller","year":"1899","journal-title":"M\u00e9moires de la Soci\u00e9t\u00e9 G\u00e9ologique de la France, Pal\u00e9ontologie"},{"key":"pone.0332423.ref020","author":"Noel","year":"1828","journal-title":"Histoire des v\u00e9g\u00e9taux fossiles, ou, Recherches botaniques et g\u00e9ologiques sur les v\u00e9g\u00e9taux renferm\u00e9s dans les diverses couches du globe"},{"key":"pone.0332423.ref021","first-page":"52","article-title":"A pinnate leaf with reticulate venation from the Permian of New South Wales","volume":"102","author":"WBK Holmes","year":"1977","journal-title":"Proceedings of the Linnean Society of New South Wales"},{"key":"pone.0332423.ref022","first-page":"1","article-title":"Die fossile Flora der Rh\u00e4t-Lias-\u00dcbergangsschichten von Bayreuth (Oberfranken) unter besonderer Ber\u00fccksichtigung der Coenologie","volume":"72","author":"R Weber","year":"1968","journal-title":"Erlanger Geologische Abhandlungen"},{"issue":"6","key":"pone.0332423.ref023","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1139\/cjes-2016-0043","article-title":"Eocene paleontology and geology of western North America","volume":"53","author":"DR Greenwood","year":"2016","journal-title":"Can J Earth Sci"},{"key":"pone.0332423.ref024","first-page":"263","article-title":"Das Eckfelder Maar in der Vulkaneifel - Fenster in einem k\u00fcstenfernen Lebensraum vor 44 Millionen Jahren","volume":"47","author":"H Frankenh\u00e4user","year":"2009","journal-title":"Mainzer naturwiss Archiv"},{"key":"pone.0332423.ref025","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/S0034-6667(97)00078-X","article-title":"A fresh look at the rich assemblage from the Pliocene sink-hole of Willershausen, Germany","volume":"101","author":"DK Ferguson","year":"1998","journal-title":"Rev Palaeobot Palynol"},{"issue":"3","key":"pone.0332423.ref026","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1111\/jmi.13187","article-title":"Visualisation of calcium oxalate crystal macropatterns in plant leaves using an improved fast preparation method","volume":"290","author":"H-J Ensikat","year":"2023","journal-title":"J Microsc"},{"key":"pone.0332423.ref027","first-page":"195","article-title":"The geological evolution of Bi\u00f8rn\u00f8ya, Arctic Norway: implications for the Barents Shelf","volume":"81","author":"D Worsley","year":"2001","journal-title":"Norwegian Journal of Geology"},{"key":"pone.0332423.ref028","author":"D Rickard","year":"2021"},{"key":"pone.0332423.ref029","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.chemgeo.2006.09.011","article-title":"Botanical constraints on pyrite formation","volume":"236","author":"DT Rickard","year":"2007","journal-title":"Chem Geol"},{"key":"pone.0332423.ref030","author":"B Anthoons","year":"2017"},{"issue":"3","key":"pone.0332423.ref031","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1046\/j.1469-8137.2003.00839.x","article-title":"Distribution of calcium oxalate crystals in the secondary phloem of conifers: a constitutive defense mechanism?","volume":"159","author":"JW Hudgins","year":"2003","journal-title":"New Phytol"},{"issue":"3","key":"pone.0332423.ref032","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1006\/anbo.1995.1022","article-title":"Calcium Oxalate Crystals in the Bark of Quercus robur, Ulmus glabra, Populus tremula and Betula pendula","volume":"75","author":"M Trockenbrodt","year":"1995","journal-title":"Annals of Botany"},{"issue":"11","key":"pone.0332423.ref033","doi-asserted-by":"crossref","first-page":"2666","DOI":"10.1002\/jemt.24636","article-title":"Morphology and composition of calcium oxalate monohydrate phytoliths in the bark of Betula ermanii (stone birch): Case study from Sakhalin Island","volume":"87","author":"EV Sokol","year":"2024","journal-title":"Microsc Res Tech"},{"issue":"6","key":"pone.0332423.ref034","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1016\/j.plantsci.2011.01.019","article-title":"Calcium and silicon mineralization in land plants: transport, structure and function","volume":"180","author":"P Bauer","year":"2011","journal-title":"Plant Sci"},{"key":"pone.0332423.ref035","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/S0367-2530(17)30398-5","article-title":"Calcium in the vacuoles and cell walls of plant tissue","volume":"182","author":"H Kinzel","year":"1989","journal-title":"Flora"},{"key":"pone.0332423.ref036","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1002\/j.1537-2197.1976.tb11860.x","article-title":"Morphology, fine structure and ontogeny of the stinging emergence of Tragia ramosa and T. saxicola (Euphorbiaceae)","volume":"63","author":"EL Thurston","year":"1976","journal-title":"Am J Bot"},{"issue":"2","key":"pone.0332423.ref037","doi-asserted-by":"crossref","first-page":"141","DOI":"10.3390\/toxins13020141","article-title":"Distribution, Ecology, Chemistry and Toxicology of Plant Stinging Hairs","volume":"13","author":"H-J Ensikat","year":"2021","journal-title":"Toxins (Basel)"},{"issue":"1","key":"pone.0332423.ref038","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1111\/nph.12643","article-title":"Middle Devonian liverwort herbivory and antiherbivore defence","volume":"202","author":"CC Labandeira","year":"2014","journal-title":"New Phytol"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0332423","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,17]],"date-time":"2025-12-17T18:24:04Z","timestamp":1765995844000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0332423"}},"subtitle":[],"editor":[{"given":"Borja","family":"Cascales-Mi\u00f1ana","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,12,17]]},"references-count":38,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2025,12,17]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0332423","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,12,17]]}}}