The presumed ginkgophyte Umaltolepis has PNAS PLUS seed-bearing structures resembling those of Peltaspermales and Umkomasiales Fabiany Herreraa, Gongle Shib, Niiden Ichinnorovc, Masamichi Takahashid, Eugenia V. Bugdaevae, Patrick S. Herendeena, and Peter R. Cranef,g,1 aChicago Botanic Garden, Glencoe, IL 60022; bNanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, People’s Republic of China; cInstitute of Paleontology and Geology, Mongolian Academy of Sciences, Ulaanbaatar-51, Mongolia; dDepartment of Environmental Sciences, Faculty of Sciences, Niigata University, Ikarashi, Nishi-ku, Niigata 950-2181, Japan; eInstitute of Biology and Soil Science, Far East Branch, Russian Academy of Sciences, Vladivostok 690022, Russia; fSchool of Forestry and Environmental Studies, Yale University, New Haven, CT 06511; and gOak Spring Garden Foundation, Oak Spring, Upperville, VA 20184 Contributed by Peter R. Crane, February 10, 2017 (sent for review December 29, 2016; reviewed by Jason M. Hilton and Stephen McLoughlin) The origins of the five groups of living seed plants, including the similar to those of certain Peltaspermales and Umkomasiales single relictual species Ginkgo biloba, are poorly understood, in large (corystosperms), although they are unique in many respects. part because of very imperfect knowledge of extinct seed plant di- The combination of Ginkgo-like leaves with peltasperm-like and versity. Here we describe well-preserved material from the Early corystosperm-like seed-bearing structures exhibited by the recon- Cretaceous of Mongolia of the previously enigmatic Mesozoic seed structed Umaltolepis plant is consistent with previous ideas that plant reproductive structure Umaltolepis, which has been presumed interpret extant G. biloba as the last survivor of a once highly to be a ginkgophyte. Abundant new material shows that Umaltole- diverse lineage that included not only extinct close relatives of pis is a seed-bearing cupule that was borne on a stalk at the tip of a living G. biloba, such as G. yimaensis and Yimaia, but also plants short shoot. Each cupule is umbrella-like with a central column that assigned to Peltaspermales, Umkomasiales, and perhaps other bears a thick, resinous, four-lobed outer covering, which opens from groups within a broadly defined Ginkgoopsida (7, 8). below. Four, pendulous, winged seeds are attached to the upper part of the column and are enclosed by the cupule. Evidence from mor- Results phology, anatomy, and field association suggests that the short The Early Cretaceous fossils described here consist of shoots shoots bore simple, elongate Pseudotorellia leaves that have similar with attached seed-bearing structures. They also include leaves venation and resin ducts to leaves of living Ginkgo. Umaltolepis (Pseudotorellia resinosa) (9) that are linked to the shoots by as- seed-bearing structures are very different from those of Ginkgo sociation evidence as well as by features of morphology and but very similar to fossils described previously as Vladimaria. Umal- anatomy. A detailed description of the fossils, illustrated by tolepis and Vladimaria do not closely resemble the seed-bearing additional light and scanning electron micrographs, is provided EVOLUTION structures of any living or extinct plant, but are comparable in some in SI Appendix. respects to those of certain Peltaspermales and Umkomasiales Order—Vladimariales Gordenko. (corystosperms). Vegetative similarities of the Umaltolepis plant to Ginkgo, and reproductive similarities to extinct peltasperms and Family—Umaltolepidaceae Zhou. corystosperms, support previous ideas that Ginkgo maybethelast Genus—Umaltolepis Krassilov, here emended. survivor of a once highly diverse group of extinct plants, several of which exhibited various degrees of ovule enclosure. Emended generic diagnosis—Woody plant with long and short shoots (Figs. 1C and 2 E and G). Short shoots with alternating Umaltolepis | Cretaceous | Mongolia | Ginkgo Significance he living species Ginkgo biloba, which today is native only to TChina (1), is the single remaining species of a group of plants Understanding the origins of the five groups of living seed plants that was once more widespread and more diverse. Fossil plants requires well-supported hypotheses of their relationships to ex- with characteristic Ginkgo-like leaves, or similar, more deeply tinct groups, many of which are poorly understood. New in- divided forms (e.g., Ginkgoites leaves associated with Karkenia; formation from the Early Cretaceous of Mongolia on the enigmatic Baiera leaves associated with Yimaia), are recorded from the extinct plant Umaltolepis shows that its leaves are similar to those Early Permian (Cisuralian) onward, and the morphology of their of Ginkgo, but its seed-bearing structures are unique, and more seed-bearing structures, where known, has been compared with comparable to those of certain extinct Peltaspermales and that of extant Ginkgo (2). Two other extinct genera, Umaltolepis Umkomasiales. Umaltolepis provides new data for understanding and Toretzia, have also been interpreted as part of the Ginkgo relationships among living and fossil seed plants and supports lineage (2–5), but in both cases the morphology of their seed- previous ideas that Ginkgo biloba may be the sole surviving relict bearing structures is poorly understood, and the attribution to of a once very diverse group of Mesozoic seed plants. Ginkgoales is based mainly on the venation, resin bodies, and Author contributions: F.H., M.T., P.S.H., and P.R.C. designed research; F.H., G.S., N.I., E.V.B., stomata of associated simple, strap-shaped, parallel-veined and P.S.H. performed research; F.H. and P.R.C. analyzed data; and F.H., P.S.H., and P.R.C. leaves assigned to Pseudotorellia (e.g., 2, 6). wrote the paper. In this paper we provide information on Umaltolepis,basedon Reviewers: J.M.H., University of Birmingham; and S.M., Swedish Museum of Natural abundant and exceptionally well-preserved lignified material from History. the Early Cretaceous (Aptian–Albian; ∼100–125 Ma) of central The authors declare no conflict of interest. Mongolia. The Umaltolepis seed-bearing structure is umbrella-like, Freely available online through the PNAS open access option. quite different from how it was originally described and also very 1To whom correspondence should be addressed. Email: [email protected]. distinct from the seed-bearing structures of fossil and living This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. Ginkgo. The seed-bearing structures of Umaltolepis are more 1073/pnas.1621409114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1621409114 PNAS | Published online March 6, 2017 | E2385–E2391 pseudowhorls of persistent bud scales and persistent leaf bases foliar pseudowhorl on the short shoots composed of five per- (Fig. 2 G and H). Short shoots generally branched, commonly sistent leaf bases. Leaf bases with two lateral flaps flanking a with a seed-bearing structure near the tip (Fig. 1C). Seed- broad cup-shaped leaf abscission scar (Fig. 2 G and H). Cuticle bearing structure a radially symmetrical cupule borne on a of leaf bases bearing deciduous to persistent, unicellular tri- short stalk that expands into a prominent flange just below chomes (Fig. 3E). Isolated four-lobed cupules ovate to ellipti- the cupule base (Fig. 1 B and H). Cupule consisting of a cal in outline (Fig. 1 B and D–F). Each lobe with a slender central column bearing an umbrella-like, four-lobed semicircular distal notch, which clasps the four-angled central covering at the apex (Fig. 1 B–F). Each cupule lobe thick, column (Fig. 1 E, G, and H). Outer cuticle of cupule lobes resinous, and with a thick outer cuticle (Fig. 1 B–F). Cupule thick, with scattered, more or less longitudinally oriented sto- lobes extending downward to clasp the central column just mata (Fig. 3 A and C). Six to eight resin ducts in each cupule above the level of the flange (Fig. 1 F and H). Near its tip, lobe. Seeds winged, each pendulous from near the apex of the just below where the cupule covering is attached, the column is column. Each seed elliptical to ovate in outline, composed four-angled and bears four winged seeds, one along each angle mainly of wing tissue with abundant resin bodies (Fig. 2 A– (Fig. 2 A–D). Each seed is pendulous and entirely covered by D). Seed body very small, wider than long, obovate to more one of the cupule lobes. The micropyle of each seed (Fig. 2 A–D)is or less triangular in outline, with a small apical micropyle. inside the cupule just above the level of the flange (SI Appendix). Detailed description—See SI Appendix. Species—Umaltolepis mongoliensis Herrera, Shi, Ichinnorov, Takahashi, Bugdaeva, Herendeen, et Crane sp. nov. Holotype—PP56446 (Figs. 1B and 2 A–C). Species diagnosis—Each pseudowhorl of persistent bud scales Other material—PP56332–PP56445, PP56447, PP56450–PP56464, on the short shoots consisting of about 8 to 10 scales. Each PP56470–PP56479. Fig. 1. Light and scanning electron micrographs (SEM) of seed-bearing structures of Umaltolepis vachrameevii (A) from the Late Jurassic of the Bureya River Basin, Siberia, Russia, and U. mongoliensis sp. nov. from the Early Cretaceous of Mongolia (B–H). (A) U. vachrameevii [holotype: Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of Russian Academy of Sciences (FSCEATB FEBRAS), Russia, specimen no. 515–271a] with line drawing showing two isolated seed-bearing structures. Specimen on the Left shows the impression of the stalk and cupule in the sediment. Specimen on Right shows the stalk and three of the four cupule lobes. (B) U. mongoliensis seed-bearing structure (holotype: PP56446) showing stalk and closed cupule. Dissection of this specimen revealed three seeds in situ (Fig. 2 A–C). (C) Branched short shoot with two incomplete seed-bearing structures each consisting of a stalk, flange, and a broken central column (PP56348). (D) Seed-bearing structure showing the stalk and three partially open lobes of the cupule (PP56425).