The presumed ginkgophyte Umaltolepis has seed-bearing structures resembling those of Peltaspermales and Umkomasiales

Fabiany Herrera; Gongle Shi; Niiden Ichinnorov; Masamichi Takahashi; Eugenia V. Bugdaeva; Patrick S. Herendeen; Peter R. Crane

doi:10.1073/pnas.1621409114

Contributed by Peter R. Crane, February 10, 2017 (sent for review December 29, 2016; reviewed by Jason M. Hilton and Stephen McLoughlin)

Significance

Understanding the origins of the five groups of living seed plants requires well-supported hypotheses of their relationships to extinct groups, many of which are poorly understood. New information from the Early Cretaceous of Mongolia on the enigmatic extinct plant Umaltolepis shows that its leaves are similar to those of Ginkgo, but its seed-bearing structures are unique, and more comparable to those of certain extinct Peltaspermales and Umkomasiales. Umaltolepis provides new data for understanding relationships among living and fossil seed plants and supports previous ideas that Ginkgo biloba may be the sole surviving relict of a once very diverse group of Mesozoic seed plants.

Abstract

The origins of the five groups of living seed plants, including the single relictual species Ginkgo biloba, are poorly understood, in large part because of very imperfect knowledge of extinct seed plant diversity. Here we describe well-preserved material from the Early Cretaceous of Mongolia of the previously enigmatic Mesozoic seed plant reproductive structure Umaltolepis, which has been presumed to be a ginkgophyte. Abundant new material shows that Umaltolepis is a seed-bearing cupule that was borne on a stalk at the tip of a short shoot. Each cupule is umbrella-like with a central column that bears a thick, resinous, four-lobed outer covering, which opens from below. Four, pendulous, winged seeds are attached to the upper part of the column and are enclosed by the cupule. Evidence from morphology, anatomy, and field association suggests that the short shoots bore simple, elongate Pseudotorellia leaves that have similar venation and resin ducts to leaves of living Ginkgo. Umaltolepis seed-bearing structures are very different from those of Ginkgo but very similar to fossils described previously as Vladimaria. Umaltolepis and Vladimaria do not closely resemble the seed-bearing structures of any living or extinct plant, but are comparable in some respects to those of certain Peltaspermales and Umkomasiales (corystosperms). Vegetative similarities of the Umaltolepis plant to Ginkgo, and reproductive similarities to extinct peltasperms and corystosperms, support previous ideas that Ginkgo may be the last survivor of a once highly diverse group of extinct plants, several of which exhibited various degrees of ovule enclosure.

The living species Ginkgo biloba, which today is native only to China (1), is the single remaining species of a group of plants that was once more widespread and more diverse. Fossil plants with characteristic Ginkgo-like leaves, or similar, more deeply divided forms (e.g., Ginkgoites leaves associated with Karkenia; Baiera leaves associated with Yimaia), are recorded from the Early Permian (Cisuralian) onward, and the morphology of their seed-bearing structures, where known, has been compared with that of extant Ginkgo (2). Two other extinct genera, Umaltolepis and Toretzia, have also been interpreted as part of the Ginkgo lineage (2 ⇓⇓–5), but in both cases the morphology of their seed-bearing structures is poorly understood, and the attribution to Ginkgoales is based mainly on the venation, resin bodies, and stomata of associated simple, strap-shaped, parallel-veined leaves assigned to Pseudotorellia (e.g., 2, 6).

In this paper we provide information on Umaltolepis, based on abundant and exceptionally well-preserved lignified material from the Early Cretaceous (Aptian–Albian; ∼100–125 Ma) of central Mongolia. The Umaltolepis seed-bearing structure is umbrella-like, quite different from how it was originally described and also very distinct from the seed-bearing structures of fossil and living Ginkgo. The seed-bearing structures of Umaltolepis are more similar to those of certain Peltaspermales and Umkomasiales (corystosperms), although they are unique in many respects. The combination of Ginkgo-like leaves with peltasperm-like and corystosperm-like seed-bearing structures exhibited by the reconstructed Umaltolepis plant is consistent with previous ideas that interpret extant G. biloba as the last survivor of a once highly diverse lineage that included not only extinct close relatives of living G. biloba, such as G. yimaensis and Yimaia, but also plants assigned to Peltaspermales, Umkomasiales, and perhaps other groups within a broadly defined Ginkgoopsida (7, 8).

Results

The Early Cretaceous fossils described here consist of shoots with attached seed-bearing structures. They also include leaves (Pseudotorellia resinosa) (9) that are linked to the shoots by association evidence as well as by features of morphology and anatomy. A detailed description of the fossils, illustrated by additional light and scanning electron micrographs, is provided in SI Appendix.

Order—Vladimariales Gordenko.
Family—Umaltolepidaceae Zhou.
Genus—Umaltolepis Krassilov, here emended.
Emended generic diagnosis—Woody plant with long and short shoots (Figs. 1C and 2 E and G). Short shoots with alternating pseudowhorls of persistent bud scales and persistent leaf bases (Fig. 2 G and H). Short shoots generally branched, commonly with a seed-bearing structure near the tip (Fig. 1C). Seed-bearing structure a radially symmetrical cupule borne on a short stalk that expands into a prominent flange just below the cupule base (Fig. 1 B and H). Cupule consisting of a slender central column bearing an umbrella-like, four-lobed covering at the apex (Fig. 1 B–F). Each cupule lobe thick, resinous, and with a thick outer cuticle (Fig. 1 B–F). Cupule lobes extending downward to clasp the central column just above the level of the flange (Fig. 1 F and H). Near its tip, just below where the cupule covering is attached, the column is four-angled and bears four winged seeds, one along each angle (Fig. 2 A–D). Each seed is pendulous and entirely covered by one of the cupule lobes. The micropyle of each seed (Fig. 2 A–D) is inside the cupule just above the level of the flange (SI Appendix).
Species—Umaltolepis mongoliensis Herrera, Shi, Ichinnorov, Takahashi, Bugdaeva, Herendeen, et Crane sp. nov.
Species diagnosis—Each pseudowhorl of persistent bud scales on the short shoots consisting of about 8 to 10 scales. Each foliar pseudowhorl on the short shoots composed of five persistent leaf bases. Leaf bases with two lateral flaps flanking a broad cup-shaped leaf abscission scar (Fig. 2 G and H). Cuticle of leaf bases bearing deciduous to persistent, unicellular trichomes (Fig. 3E). Isolated four-lobed cupules ovate to elliptical in outline (Fig. 1 B and D–F). Each lobe with a semicircular distal notch, which clasps the four-angled central column (Fig. 1 E, G, and H). Outer cuticle of cupule lobes thick, with scattered, more or less longitudinally oriented stomata (Fig. 3 A and C). Six to eight resin ducts in each cupule lobe. Seeds winged, each pendulous from near the apex of the column. Each seed elliptical to ovate in outline, composed mainly of wing tissue with abundant resin bodies (Fig. 2 A–D). Seed body very small, wider than long, obovate to more or less triangular in outline, with a small apical micropyle.
Detailed description—See SI Appendix.
Holotype—PP56446 (Figs. 1B and 2 A–C).
Other material—PP56332–PP56445, PP56447, PP56450–PP56464, PP56470–PP56479.
Repository—Paleobotanical Collections, Department of Geology, The Field Museum, Chicago.
Etymology—Specific epithet refers to Mongolia, where the fossils were found.
Age, stratigraphic unit, and locality—Aptian–Albian stage, ∼100–125 Ma, Early Cretaceous. Tevshiin Govi Formation. Tevshiin Govi coal mine, central Mongolia (45°58′54′′ N, 106°07′12′′ E).

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). (E) Three-dimensionally -preserved open four-lobed cupule (lacking the stalk and column) from which the seeds have been shed: note the stippled appearance of the outer surface indicating the presence of abundant sunken stomata (PP56429). (F) A partially open four-lobed cupule attached to the stalk and column. (Right) The same cupule with two lobes removed to better expose the central column and the umbrella-like form of the cupule (PP56347). (G) SEM with line drawing showing the notch in the tip of each cupule lobe. Each notch clasps the four-angled central column (PP56375). (H) SEM with line drawing of an isolated stalk of a seed-bearing organ showing the flange and central column: note the corrugated surface of the column in its distal part (PP56334). [Scale bars, 5 mm (A–F); 2 mm (G and H).]

Fig. 2.

Light and SEM of seed-bearing structure and shoots of Umaltolepis mongoliensis sp. nov. and associated leaves of Pseudotorellia resinosa from the Early Cretaceous of Mongolia. (A) Stalk showing flange and central column (Right) from the seed-bearing organ in Fig. 1B (holotype) showing one of three winged seeds (Top Left; line drawing below) dissected from the cupule: note seed body (Lower arrow). Each winged seed was attached to the upper part of the column and completely enclosed by the cupule: note remains of wing tissue (orange) attached to the edges of the column (Upper arrow). (B) SEM of micropylar region of second winged seed dissected from holotype (Fig. 1B) showing the transition (arrow) between the wing and the seed body that has an apical micropyle. (C) SEM of micropylar region of third winged seed dissected from holotype (Fig. 1B) showing the transition between the wing and seed body: note apical micropyle. (D) Isolated and macerated seed body from specimen in SI Appendix, Fig. S16F, showing isodiametric outlines of epidermal cells and micropyle (PP56428). (E) Fragment of branch showing transition (arrow) between a short shoot (below) and a long shoot (above): note numerous persistent bud scales and leaf bases on the short shoot (PP56338). (F) Leaf of P. resinosa associated with the seed-bearing structures of U. mongoliensis: note four longitudinal veins within the leaf that converge at the leaf apex and resin ducts between the veins (PP56268). (G) Detail of short shoot from E showing at least six growth increments, each consisting of a pseudowhorl of persistent bud scales below, with a pseudowhorl of persistent leaf bases above. (H) SEM of short shoot showing three pseudowhorls of persistent triangular bud scales alternating with two pseudowhorls of leaf bases (arrow) (PP56409). (I) Detail from F showing leaf base: note that two veins enter the lamina and that each dichotomizes, resulting in four longitudinal veins within the leaf. [Scale bars, 5 mm (A, E, F, and G); 2.5 mm (H); 500 µm (B); 200 µm (D); 100 µm (C).]

Fig. 3.

Light micrographs showing similarities between cuticles of the stomata on the cupule lobes of Umaltolepis mongoliensis (A and C) and Pseudotorellia resinosa (B and D), and similarities between the persistent leaf bases of U. mongoliensis and leaves of P. resinosa (E and F). (A) Stomatal complex from cupule lobe of U. mongoliensis showing a stoma with four lateral subsidiary cells and bow-shaped ridges flanking the stomatal pit (PP56447). (B) Stomatal complex from leaf lamina of P. resinosa showing a stoma with four lateral subsidiary cells and bow-shaped ridges flanking the stomatal pit (PP56448). (C) Line drawing of A: note four lateral subsidiary cells (light gray) and bow-shaped ridges (dark gray). (D) Line drawing from B; note four lateral subsidiary cells (light gray) and bow-shaped ridges (dark gray). (E) Well-developed unicellular trichomes on a persistent leaf base isolated from short shoot of U. mongoliensis (PP56430). (F) Well-developed unicellular trichomes on the lamina margin near the leaf base of P. resinosa (PP56449). [Scale bars, 20 µm (A and B); 100 µm (E and F).]

Assignment to Umaltolepis and Comparison with Previously Described Species.

The type species of Umaltolepis, U. vachrameevii (Fig. 1A), described from the Late Jurassic of the Bureya River Basin, Siberia (4), was reconstructed originally as an unlobed or bilobed bract with a single inverted seed in its axil, which Krassilov interpreted as a highly reduced fertile axis. However, examination of the type material (Fig. 1A) shows that U. vachrameevii is structurally very different from what Krassilov envisaged and is very similar to U. mongoliensis.

There are small differences in the Pseudotorellia leaves that are associated with U. mongoliensis (Fig. 1 B–H) and U. vachrameevii (see below; Fig. 1A), but otherwise U. mongoliensis differs from U. vachrameevii in only two relatively minor features: the absence of papillae on the lateral subsidiary cells of stomata on the outer cuticle of the cupule and the slightly larger cupule size (U. mongoliensis: ∼9–19 mm long, 5.6–9 mm wide vs. U. vachrameevii: ∼8–14 mm long, 4–6 mm wide) (SI Appendix).

Three other species of Umaltolepis have been reported from Lower Jurassic to Lower Cretaceous deposits based on compression and impression fossils (SI Appendix, Table S2). Both U. coleoptera from the Early Jurassic of Iran (10) and U. hebeiensis from the Early Cretaceous of China (11, 12) are known from only a few isolated cupules that are not well preserved. Both are probably valid records of the genus, but are difficult to compare with the better-preserved material from Mongolia. Umaltolepis rarinervis is better known based on material from the Bureya River Basin in Siberia (4), and is probably slightly younger (Early Cretaceous: Valanginian) than the material of U. vachrameevii. Umaltolepis rarinervis differs from U. mongoliensis in that the outer cuticle of the cupule has papillate epidermal cells and stomata that are arranged in more regular longitudinal rows than in U. mongoliensis. The impressions of elongate resin ducts in cupules of U. rarinervis also appear branched, rather than unbranched, as is the case in U. mongoliensis (SI Appendix).

Among other fossils, U. mongoliensis is remarkably similar to the isolated, well-preserved seed-bearing structures described as Vladimaria octopartita from the Middle Jurassic of European Russia (13). The shoots and leaves of Vladimaria are unknown, but based on the seed-bearing structures there is no doubt that the two genera are closely related. Vladimaria was interpreted as a “composite seed-bearing capsule” in which each locule contained a pendulous winged seed (13). Like U. mongoliensis, Vladimaria is thick, resinous, and has a thick outer cuticle with sunken guard cells that have distinct butterfly-like flanges at their junction with the subsidiary cells (SI Appendix, Table S2). The most significant differences between the two taxa are that the cupule of U. mongoliensis splits into four lobes at maturity, whereas that of V. octopartita splits into eight, and that U. mongoliensis is borne on a more slender stalk. Stomata on the cupule lobes are also less regularly oriented in Vladimaria than in U. mongoliensis. However, in all other respects Vladimaria and U. mongoliensis are very similar. As in U. mongoliensis, the cupule of V. octopartita was attached to the apex of a central column and a few specimens show that, before dehiscence, the cupule lobes clasped the central column just above a prominent flange on the stalk as in U. mongoliensis (SI Appendix).

Leaves of Umaltolepis mongoliensis.

Krassilov (4) noted the pattern of co-occurrence between seed-bearing structures of U. vachrameevii and leaves of Pseudotorellia angustifolia, which in a few cases were attached to short shoots like those bearing U. vachrameevii. A similar pattern linking U. coleoptera and leaves of Pseudotorellia roobana was reported (10). In addition to this evidence based on field association, there are also similarities between the resin bodies and epidermal features of the seed-bearing organs and those of the shoots and leaves. The consistent association of these kinds of leaves and reproductive structures is also seen at Tevshiin Govi. Together with morphological and anatomical similarities, this suggests strongly that the short shoots of Umaltolepis bore simple, elongate, and deciduous Pseudotorellia leaves (Fig. 4).

Fig. 4.

Reconstruction of Umaltolepis mongoliensis sp. nov. showing four seed-bearing structures and attached Pseudotorellia resinosa leaves. Note that three seed-bearing organs have split at the level of the flange into four lobes releasing the seeds. The seeds (Right) were probably membranous and wind-dispersed. The cupule has been shed from one of the seed-bearing structures leaving the stalk, flange and column attached to the short shoot. Most, probably all, of the small dark spots on leaves are the remains of fungal stromata.

Two species of Pseudotorellia, P. resinosa (Fig. 2 F and I) and P. palustris, are consistently associated with the seed-bearing structures and shoots of U. mongoliensis at Tevshiin Govi (9) (SI Appendix, Table S1). Both species have thick cuticles with scattered, more or less longitudinally oriented stomata, in which the two guard cells are sunken and have butterfly-like flanges of cuticle at their junction with the subsidiary cells (Fig. 3). These features are similar to those on the cupule cuticle of U. mongoliensis (Fig. 3 A and C).

Of the two species of Pseudotorellia at Tevshiin Govi (9), P. resinosa is linked more strongly to U. mongoliensis than to P. palustris, by its abundant resin, which is consistent with the abundant resin found in the cupule lobes, seeds, and shoots of U. mongoliensis and also by the form of the stomata, which have two lateral bow-shaped cuticular ridges flanking the stomatal pit (Fig. 3 B and D). Still more decisive in linking U. mongoliensis and P. resinosa is that the margin of the leaf base in isolated P. resinosa leaves has unicellular trichomes (Fig. 3F) that are identical to those on the persistent leaf bases attached to the short shoots of U. mongoliensis (Fig. 3E). These trichomes are not present in the leaves of P. palustris. Leaves of P. resinosa that are associated with U. mongoliensis, and leaves of P. angustifolia associated with U. vachrameevii, are also very similar. As with the cupules, the only differences are that P. resinosa lacks the papillae seen on the lateral subsidiary cells of the stomata in P. angustifolia (4) and that P. angustifolia has well-defined stomatal bands, whereas in P. resinosa the stomata are scattered and less regularly arranged (9).

Discussion

Ecology and Biology of the Umaltolepis–Pseudotorellia plant.

Records of the Umaltolepis–Pseudotorellia plant across Asia, from both Jurassic and Lower Cretaceous sediments (4, 10 ⇓–12), indicate that it was once widespread, and its abundance in many samples at Tevshiin Govi indicates that it was an important element in the swamp vegetation that created the lignite. Also present were Umkomasiales (Umkomasia mongolica) (14), extinct conifer-like plants (Krassilovia) (15), archaic probable Pinaceae (Schizolepidopsis) (16), early Pinaceae (Pityostrobus, Picea) (17), and Cupressaceae [Elatides (18); Pentakonos, Stutzeliastrobus (19)]. Diversity in the swamp flora was low, perhaps including only about 10 woody species, all of which have leaves with thick cuticles (except Podozamites) (9). Other than the tiny leaves of a probable epiphytic or climbing fern, the flora is devoid of pinnately compound leaves. In all cases the leaves in the fossil assemblage are needle-like (Schizolepidopsis, Picea) (16, 17), scale-like (Stutzeliastrobus) (19), or simple and parallel-veined (Podozamites, both species of Pseudotorellia) (9).

Based on what is known so far, all of the woody plants in the Tevshiin Govi swamp vegetation seem likely to have been wind-pollinated. The pendulous seeds, with the micropyle positioned just above the level of the flange where the cupule lobes separate from the stalk, suggest that this was probably also the case in Umaltolepis. Pollination probably involved a hanging pollination drop and buoyant pollen as in many extant conifers (20). Krassilov (4) associated bisaccate pollen (Entylissa umaltensis) with U. vachrameevii based on their occurrence on the surface of P. angustifolia leaves, but we regard this hypothesized link as unconfirmed.

We have been unable to establish conclusively if pollen had direct access to the micropyles of the seeds in U. mongoliensis; however, we think that this was likely the case, as has been shown in other Mesozoic seed plants (e.g., Caytonia, Umkomasia) in which the ovules are partially or completely enclosed (21 ⇓–23). Umaltolepis provides another example of ovule enclosure among Mesozoic seed plants, the main presumed advantage of which would have been protection of the ovules. This appears especially to have been the case in Umaltolepis in which the cupule is thick and resinous, whereas the seeds are thin-walled. Partial separation of the cupule lobes at maturity and shedding of the cupule from the stalk would have provided the means by which the seeds were released (Fig. 4). We have not identified dispersed seeds in the Tevshiin Govi samples, suggesting that the seeds, like those of some other Mesozoic plants (e.g., Bennettitales), were delicate and not easily preserved.

Phylogenetic Relationships of the Umaltolepis–Pseudotorellia Plant.

The order Vladimariales was erected to accommodate the seed-bearing organs of Vladimaria (13), and given the similarities to Umaltolepis, we place both genera within this order. Krassilov (4) proposed the family name Pseudotorelliaceae to accommodate the leaves of P. angustifolia and seed-bearing organs of U. vachrameevii (Fig. 1A). However, Umaltolepis is best placed in the family Umaltolepidaceae (2, 5), considering that Pseudotorellia is reserved for a specific kind of strap-shaped, parallel-veined leaf. We include U. mongoliensis in Umaltolepidaceae, along with U. vachrameevii (4), U. rarinervis (4), and also, less securely, U. coleoptera (10) and U. hebeiensis (11, 12). We regard Vladimaria as closely related to Umaltolepidaceae, but we exclude it from the family until it is better understood as a “whole plant.”

Previous authors have considered the Umaltolepis–Pseudotorellia plant as closely related to Ginkgoales (2, 4, 6, 9, 24), based on similarities between the cuticles of Pseudotorellia leaves and those of living Ginkgo, including stomata that are sparse and scattered in ill-defined bands on the presumed abaxial surface, together with the similarities between the elongated resin bodies that occur between adjacent veins in both the fossil and the modern leaves. There are also similarities in leaf venation. In both Pseudotorellia and extant Ginkgo, two veins enter the leaf lamina from the petiole, and each then dichotomizes one, two, or more times (9).

It is more difficult to reconcile the structure of the seed-bearing organs of Umaltolepis with those of Ginkgo. In Ginkgo, Yimaia (Middle Jurassic) (25, 26), and probably related fossil forms with simple leaves such as Nagrenia samylinae (Middle Jurassic) (27) and Nehvizdyella bipartita (Late Cretaceous) (28), there is no evidence of the umbrella-like structure seen in Umaltolepis. In all these taxa the single, terminal, erect seed on each branch of the seed-bearing structure is very different from the several pendulous seeds present in Umaltolepis and Vladimaria. More productive comparisons are with the seed-bearing organs of Peltaspermales and Umkomasiales (SI Appendix, Table S2).

Recent reviews of the Peltaspermales include Peltaspermaceae (e.g., Autunia, Peltaspermum), Angaropeltaceae (e.g., Angaropeltis), Vetlugospermaceae (e.g., Vetlugospermum), and Matatiellaceae (e.g., Matatiella) (29 ⇓⇓–32). In most cases, such as Autunia, Peltaspermum, Vetlugospermum, Matatiella, and other genera, there is no indication that the seeds are attached to a stalk. Instead, they appear to be naked on the lower surface of an open peltate, lobed, fan-shaped to disc-shaped structure (SI Appendix, Table S2). This is different from the situation in Umaltolepis and Vladimaria where the seeds are attached to the central column and almost completely enclosed.

Potentially more similar are the seed-bearing organs of Permian Angaropeltaceae, including Angaropeltis (formerly Cardiolepis), Permoxylocarpus, and Sylvocarpus, in which the seeds are more completely enclosed (32 ⇓⇓–35). In Angaropeltis the enclosing structure also appears resinous, and the associated leaves are simple, strap-shaped, and parallel-veined (29, 36) (SI Appendix, Table S2). Unfortunately, the preservation of Angaropeltis and similar genera means that the details of seed attachment are not well understood.

A further interesting comparison for the seed-bearing structures of Umaltolepis and Vladimaria is provided by the cupules of Umkomasiales (13, 14). In Umkomasiales, as in Umaltolepis, the seeds are also partially to completely enclosed within a “cupule,” which is formed by the stalk on which the seed is borne, together with a bilobed or multilobed flap of tissue (14, 30). In most Umkomasiales there is one seed in each cupule, but Umkomasia resinosa from the early Middle Triassic of Antarctica has resinous cupules like Umaltolepis, and when each cupule has two seeds, one flap of tissue corresponds to each seed (37). Umaltolepis and Vladimaria may reflect a situation in which four or eight corystosperm cupules are fused around a central column. Umkomasia uniramia from the Triassic of Antarctica, in which four to eight cupules are borne in a whorl on a single stalk, potentially approaches this condition (38). Each multicupule unit of U. uniramia is also borne at the tip of short shoots similar to those of Umaltolepis.

Both Peltaspermales and Umkomasiales commonly have pinnately compound leaves, which are often referred to the genera Lepidopteris or Dicroidium, respectively (7, 30). However, the leaves of Angaropeltis and Permoxylocarpus are simple, and referred to the genus Phylladoderma (32). Similarly, the fan-shaped basal elements seen in some pinnate Dicroidium leaves resemble Ginkgo foliage (39), and the leaves of some Umkomasia-like plants (e.g., Kannaskoppia) are very Ginkgo-like (30). The resin cells that occur in the mesophyll of Dicroidium leaves (40) also recall those of Ginkgo. Given the similarities between leaves of P. resinosa and P. palustris, it may be significant that preliminary data on patterns of cooccurrence suggest that P. palustris may be the leaf of the corystosperm reproductive structure Umkomasia mongolica (9).

Current phylogenetic analyses of seed plant relationships based on morphological data include only a small proportion of the potentially relevant extinct diversity and contain significant missing data as well as many uncertain homologies. However, inclusion of Umaltolepis in a previous published matrix (ref. 41, based mainly on ref. 42) places it in a polychotomy with several other groups (SI Appendix). Depending on exactly how key characters of Umaltolepis and other extinct taxa are scored, the taxa in the polychotomy include Glossopteris+Pentoxylon, Ginkgo+cordaites+conifers, corystosperms, peltasperms, the BEG group (Bennettitales+Erdmanthicales+Gnetales), and Caytonia+angiosperms. This relatively unresolved phylogenetic result is consistent with the observation that the Umaltolepis–Pseudotorellia plant is morphologically distinct from all previously recognized groups of seed plants.

Implications for Seed Plant Evolution.

Reconstruction of the U. mongoliensis–Pseudotorellia resinosa plant (Fig. 4) together with improved information on the seed-bearing structures adds significantly to knowledge about extinct seed plants from the Mesozoic. This is important for understanding large-scale patterns of seed plant evolution, including the origin of angiosperms, and for attempts to harmonize information on the molecular phylogenetics of living seed plants with paleobotanical data. It is especially interesting that the leaves and short shoots of the Umaltolepis–Pseudotorellia plant are similar to those of living Ginkgo, whereas the seed-bearing structures are more similar to those of certain extinct Peltaspermales and Umkomasiales. The diversity of Peltaspermales includes several forms in which the seeds are almost fully enclosed by the umbrella-like peltate heads of the seed-bearing structures. Similarly, the possibility of a closer relationship between Umkomasiales and Ginkgo has been emphasized recently based on information on the corystosperm ovulate reproductive structures [e.g., Doylea (43) and Umkomasia (14)].

The emerging picture suggests that Ginkgo, and very closely related extinct genera, such as Yimaia (25) and Karkenia (44, 45), are part of a larger group of Ginkgo-like plants that also included simple-leaved forms, such Nagrenia (27) and Nehvizdyella (28). Corystosperms (Umkomasiales) and peltasperms may be closely related to this group. These ideas need to be tested in a new generation of seed plant phylogenetic analyses that include critical assessments of putative homologies among diverse reproductive structures and new information on other potentially relevant, but currently poorly understood, extinct forms (e.g., Angaropeltaceae, Toretzia). Nevertheless, indications so far recall the concept of the Ginkgoopsida, a large and very inclusive clade defined by Meyen (7, 8) based on similarities in short shoots, leaves, cuticles, seeds, and pollen morphology. Meyen’s concept of Ginkgoopsida included not only Ginkgoales, but also Peltaspermales, Umkomasiales, and other extinct plants. This idea, supported by the potential links highlighted here between Ginkgo, Peltaspermales, and Umkomasiales, suggests that G. biloba may be the sole surviving relict of a group of seed plants that was once even more diverse than has been commonly recognized.

Materials and Methods

Plant Locality.

Fossil plants described in this study were collected in central Mongolia from the Tevshiin Govi Formation, which comprises sandstones and siltstones with thick coal and lignite seams, at the Tevshiin Govi locality, a small open-cast lignite mine, ∼220 km southwest of Ulaanbaatar (45°58′5′′ N, 106°07′12′′ E; paleolatitude: ∼44° N; 55° E). The age of the Tevshiin Govi Formation is Aptian–Albian (ca. 125–100 Mya) based on analyses of palynomorphs (46, 47) and stratigraphic correlations with the Khukhteeg Formation (48). Thirty-five samples of siltstone and lignite were collected from the Tevshiin Govi mine, of which 27 are rich in mesofossils that are exquisitely preserved. The Tevshiin Govi lignites are composed of diverse macerals and a minimal amount of detrital sediment. We presume that these lignites are largely autochthonous in origin. The fossil taxon described in this paper is common to very abundant in the 27 lignite samples. Most of the specimens are isolated four-lobed cupules (∼500 specimens) (SI Appendix). However, many four-lobed cupules attached to short shoots have also been recovered (SI Appendix).

Fossil Preparation.

Lignite samples were prepared as previously described (16, 18). Fossil specimens were cleaned with dilute hydrochloric acid for half an hour, followed by concentrated hydrofluoric acid (50%) for 1 d. Specimens were then thoroughly washed and soaked in distilled water for 1 wk with changes of water every day. Fossils were picked from the disaggregated lignite under Leica stereomicroscopes using a small brush and insect forceps. Specimens were selected for further study using a Carl Zeiss EVO 60 scanning electron microscope at The Field Museum of Natural History in Chicago. Large specimens were photographed at the Chicago Botanic Garden using a Canon Rebel camera with 100-mm macrolens attached to a Stackshot system, and the digital photos were merged using Helicon Focus software. Several specimens were examined using a General Electric dual-tube X-ray computed tomography scanner in the Department of Organismal Biology and Anatomy at the University of Chicago. Tomographic sections were analyzed using Avizo 8.1. Cuticles were obtained by macerating shoots, leaves, cupules, and seeds in dilute household bleach (∼1% sodium hypochlorite solution) after removal of residual sediment. Maceration times varied from several seconds to several minutes, depending on the degree of lignification. Large pieces of cuticle were mounted on slides with glycerin jelly and sealed with nail polish. Fossils selected for anatomical study were soaked in 10% (wt/vol) hydrochloric acid followed by Aerosol OT [10% (wt/vol) solution of sodium dioctyl sulfosuccinate in alcohol]. Specimens were then taken through a series of ethanol concentrations (70% to absolute ethanol) and embedded in Technovit 7100 following the prescribed mounting protocol. Transverse and longitudinal sections ∼4–7 µm thick were made of the embedded material using a Leica 2030 microtome. Slides were mounted in Hydromount no. 17966.

Phylogenetic Analyses.

We analyzed the relationships of U. mongoliensis–P. resinosa with respect to other seed plants by adding it to a published morphological matrix (41, 42). Character scoring for Umaltolepis–Pseudotorellia is available in SI Appendix. The matrix used includes 51 taxa and 102 morphological characters. Tetraxylopteris was used as the outgroup. Parsimony analyses were conducted using Winclada (49). All characters were treated as equally weighted and unordered. A combination of ratchet searches (to detect islands of trees) followed by a heuristic search was used. An initial set of most parsimonious trees was generated using the “Ratchet” option (200 iterations/replicate; hold 1 tree/iteration; random constraint level = 10; three sequential ratchet runs). Trees obtained from the ratchet analysis were submitted to the tree bisection-reconnection branch swapping with the maximum number of trees saved set to 5,000 (hold = 5,000). The analysis yielded 2,573 most parsimonious trees [length = 318, consistency index (CI) = 44, retention index (RI) = 79].

Acknowledgments

We thank T. Gombosuren and O. Nyamsambuu for assistance with fieldwork in Mongolia; I. Glasspool and S. Grant for curatorial assistance; B. Strack for assistance with scanning electron microscopy; Z.-X. Luo and A. I. Neander for permission and assistance with X-ray tomography; G. Bedoya for nomenclatural suggestions; P. von Knorring for the plant reconstruction; P. Knopf, A. B. Leslie, and S. Carlquist for comments on the fossils; and J. M. Hilton and S. McLoughlin for valuable comments on the manuscript. Funding for this work was provided by National Science Foundation Grant DEB-1348456 (to P.S.H. and P.R.C.) and by Grants-in-Aid for Scientific Research (21405010 and 24405015) from the Japan Society for the Promotion of Science (to M.T.).

Footnotes

↵¹To whom correspondence should be addressed. Email: peter.crane{at}yale.edu.

Author contributions: F.H., M.T., P.S.H., and P.R.C. designed research; F.H., G.S., N.I., E.V.B., and P.S.H. performed research; F.H. and P.R.C. analyzed data; and F.H., P.S.H., and P.R.C. wrote the paper.
Reviewers: J.M.H., University of Birmingham; and S.M., Swedish Museum of Natural History.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1621409114/-/DCSupplemental.

Freely available online through the PNAS open access option.

References

↵
1. Crane PR
(2013) Ginkgo: The Tree That Time Forgot (Yale University Press, New Haven, CT), p 408.
.
↵
1. Zhou ZY
(2009) An overview of fossil Ginkgoales. Palaeoworld 18(1):1–22.
.
OpenUrl CrossRef
↵
1. Zhou ZY
(1991) Phylogeny and evolutionary trends of Mesozoic ginkgoaleans: A preliminary assessment. Rev Palaeobot Palynol 68(3-4):203–216.
.
OpenUrl CrossRef
↵
1. Krassilov VA
(1972) Mesozoic Flora from the Bureja River (Ginkgoales and Czekanowskiales) (Nauka, Moscow), p 115 (in Russian).
.
↵
1. Stanislavsky FA
(1973) The new genus Toretzia from the Upper Triassic of the Donetz basin and its relation to the genera of the order Ginkgoales. Paleont Zh 1:88–96 (in Russian).
.
OpenUrl
↵
1. Harris TM
(1935) The fossil flora of Scoresby Sound, East Greenland, Part 4. Medd Gronl 112(1):1–176.
.
OpenUrl
↵
1. Meyen SV
(1984) Basic features of gymnosperm systematics and phylogeny as shown by the fossil record. Bot Rev 50(1):1–111.
.
OpenUrl CrossRef
↵
1. Meyen SV
(1987) Fundamentals of Palaeobotany (Chapman & Hall, London), p 432.
.
↵
1. Shi G, et al.
(January 24, 2017) Leaves of Podozamites and Pseudotorellia from the Early Cretaceous of Mongolia: Stomatal patterns and implications for relationships. J Syst Paleontol doi:10.1080/14772019.2016.1274343.
.
OpenUrl CrossRef
↵
1. Schweitzer HJ,
2. Kirchner M
(1995) Die Rhäto-Jurassischen Floren des Iran und Afghanistans. 8. Ginkgophyta. Palaeontographica B 237:1–58.
.
OpenUrl
↵
1. Wang ZQ
(1984) Plant kingdom. Palaeontological Atlas of North China II Mesozoic, eds Tianjin Institute of Geology and Mineral Resources (Geological Publishing House, Beijing), pp 223–296, 367–384 (in Chinese).
.
↵
1. Chen F,
2. Meng XY,
3. Ren SQ,
4. Wu CL
(1988) The Early Cretaceous Flora of Fuxin Basin and Tiefa Basin, Liaoning Province (Geological Publishing House, Beijing), p 180 (in Chinese).
.
↵
1. Gordenko NV
(2010) Vladimariales ordo nov. (Gymnospermae) from the Middle Jurassic (Kursk Region, European Russia). Paleontol J 44(10):1281–1307.
.
OpenUrl
↵
1. Shi G, et al.
(2016) Early Cretaceous Umkomasia from Mongolia: Implications for homology of corystosperm cupules. New Phytol 210(4):1418–1429.
.
OpenUrl
↵
1. Herrera F, et al.
(2015) A new voltzian seed cone from the Early Cretaceous of Mongolia and its implications for the evolution of ancient conifers. Int J Plant Sci 176(8):791–809.
.
OpenUrl
↵
1. Leslie AB, et al.
(2013) Pinaceae-like reproductive morphology in Schizolepidopsis canicularis sp. nov. from the Early Cretaceous (Aptian-Albian) of Mongolia. Am J Bot 100(12):2426–2436.
.
OpenUrl Abstract/FREE Full Text
↵
1. Herrera F, et al.
(2016) New fossil Pinaceae from the Early Cretaceous of Mongolia. Botany 94:885–915.
.
OpenUrl
↵
1. Shi G, et al.
(2014) Whole-plant reconstruction and phylogenetic relationships of Elatides zhoui sp. nov. (Cupressaceae) from the Early Cretaceous of Mongolia. Int J Plant Sci 175(8):911–930.
.
OpenUrl CrossRef
↵
1. Herrera F, et al.
(2017) Cupressaceae conifers from the Early Cretaceous of Mongolia. Int J Plant Sci 178(1):19–41.
.
OpenUrl
↵
1. Leslie AB,
2. Beaulieu JM,
3. Crane PR,
4. Knopf P,
5. Donoghue MJ
(2015) Integration and macroevolutionary patterns in the pollination biology of conifers. Evolution 69(6):1573–1583.
.
OpenUrl
↵
1. Thomas HH
(1925) The Caytoniales, a new group of angiospermous plants from the Jurassic rocks of Yorkshire. Philos Trans R Soc Lond B Biol Sci 213(402-410):299–363.
.
OpenUrl FREE Full Text
↵
1. Thomas HH
(1933) On some pteridospermous plants from the Mesozoic rocks of South Africa. Philos Trans R Soc Lond B Biol Sci 222(483-493):193–265.
.
OpenUrl
↵
1. Harris TM
(1940) Caytonia Ann Bot (Lond) 4(16):713–734.
.
OpenUrl
↵
1. Hori T, et al.
1. Zhou ZY
(1997) Mesozoic ginkgoalean megafossils: A systematic review. Ginkgo biloba—A Global Treasure—From Biology to Medicine, ed Hori T, et al. (Springer, Tokyo), pp 183–206.
.
↵
1. Zhou ZY,
2. Zhang BL
(1988) Two new ginkgoalean female reproductive organs from the Middle Jurassic of Henan Province. Sci Bull 33(4):1201–1203.
.
OpenUrl
↵
1. Zhou ZY,
2. Zhang BL
(1989) A Middle Jurassic Ginkgo with ovule-bearing organs from Henan, China. Palaeontographica B 211(4-6):113–133.
.
OpenUrl
↵
1. Nosova NV
(2013) Revision of the genus Grenana Samylina from the Middle Jurassic of Angren, Uzbekistan. Rev Palaeobot Palynol 197(1-4):226–252.
.
OpenUrl
↵
1. Kvaček J,
2. Falcon-Lang HJ,
3. Dasková J
(2005) A new Late Cretaceous ginkgoalean reproductive structure Nehvizdyella gen. nov. from the Czech Republic and its whole-plant reconstruction. Am J Bot 92(12):1958–1969.
.
OpenUrl Abstract/FREE Full Text
↵
1. Doweld AB
(2001) Prosyllabus Tracheophytorum. Tentamen Systematis Plantarum Vascularium (Tracheophyta) (Geos, Moscow), p 110.
.
↵
1. Anderson JM,
2. Anderson HM
(2003) Heyday of the gymnosperms: Systematics and biodiversity of the Late Triassic Molteno fructifications. Strelitzia 15:1–398.
.
OpenUrl
↵
1. Bomfleur B, et al.
(2011) Systematics and paleoecology of a new peltaspermalean seed fern from the Triassic polar vegetation of Gondwana. Int J Plant Sci 172(6):807–835.
.
OpenUrl CrossRef
↵
1. Naugolnykh SV
(2012) Vetlugospermum and Vetlugospermaceae: A new genus and family of peltasperms from the Lower Triassic of Moscow syneclise (Russia). Geobios 45(5):451–462.
.
OpenUrl
↵
1. Naugolnykh SV
(2007) Permian floras of the Urals. Transactions of Geological Institute of Russian Academy of Sciences, vol. 524 (Geos, Moscow).
.
↵
1. Naugolnykh SV
(2008) A new gymnosperm Sylvocarpus armatus gen. et sp. nov. from the Lower Permian of the Ural Mountains. Paleontol J 42(4):431–439.
.
OpenUrl
↵
1. Naugolnykh SV,
2. Oskolski AA
(2010) An advanced peltasperm Permoxylocarpus trojanus Naug. from the Lower Permian of the Urals (Russia): An ancient case of entomophily in gymnosperms? Wulfenia 17:29–43.
.
OpenUrl
↵
1. Meyen SV
(1977) The Cardiolepidaceae, a new Permian conifer family from north Eurasia. Paleontol J 3:128–138.
.
OpenUrl
↵
1. Klavins SD,
2. Taylor TN,
3. Taylor EL
(2002) Anatomy of Umkomasia (corystospermales) from the triassic of antarctica. Am J Bot 89(4):664–676.
.
OpenUrl Abstract/FREE Full Text
↵
1. Axsmith BJ,
2. Taylor EL,
3. Taylor TN,
4. Cuneo NR
(2000) New perspectives on the Mesozoic seed fern order Corystospermales based on attached organs from the Triassic of Antarctica. Am J Bot 87(6):757–768.
.
OpenUrl Abstract/FREE Full Text
↵
1. Bomfleur B,
2. Escapa IH,
3. Taylor EL,
4. Taylor TN
(2012) Modified basal elements in Dicroidium fronds (Corystospermales). Rev Palaeobot Palynol 170:15–26.
.
OpenUrl
↵
1. Pigg KB
(1990) Anatomically preserved Dicroidium foliage from the central Transantarctic Mountains. Rev Palaeobot Palynol 66(1-2):129–145.
.
OpenUrl CrossRef
↵
1. Friis EM, et al.
(2007) Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature 450(7169):549–552.
.
OpenUrl CrossRef PubMed
↵
1. Hilton J,
2. Bateman RM
(2006) Pteridosperms are the backbone of seed plant phylogeny. J Torrey Bot Soc 133(1):119–168.
.
OpenUrl CrossRef
↵
1. Rothwell GW,
2. Stockey RA
(2016) Phylogenetic diversification of Early Cretaceous seed plants: The compound seed cone of Doylea tetrahedrasperma. Am J Bot 103(5):923–937.
.
OpenUrl Abstract/FREE Full Text
↵
1. Archangelsky S
(1965) Fossil Ginkgoales from the Ticó flora, Santa Cruz Province, Argentina. Bull Br Mus (Nat Hist). Geol 10(5):121–137.
.
OpenUrl
↵
1. Del Fueyo GM,
2. Archangelsky S
(2001) New studies on Karkenia incurva Archang. from the Early Cretaceous of Argentina. Evolution of the seed cone in Ginkgoales. Palaeontographica B 256:111–121.
.
OpenUrl
↵
1. Ichinnorov N
(2003) Palynocomplex of the Lower Cretaceous sediments of eastern Mongolia. Geosci 22:12–16.
.
OpenUrl
↵
1. Nichols DJ,
2. Matsukawa M,
3. Ito M
(2006) Palynology and age of some Cretaceous nonmarine deposits in Mongolia and China. Cretac Res 27(2):241–251.
.
OpenUrl
↵
1. Erdenetsogt B-O,
2. Lee I,
3. Bat-Erdene D,
4. Jargal L
(2009) Mongolian coal-bearing basins: geological settings, coal characteristics, distribution, and resources. Int J Coal Geol 80(2):87–104.
.
OpenUrl
↵
1. Nixon KC
(1999) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15(4):407–414.
.
OpenUrl CrossRef

Article Alerts

Email Article

Citation Tools

Request Permissions

Article Classifications

Biological Sciences
Evolution

Proceedings of the National Academy of Sciences: 114 (12)

Table of Contents

Submit

[1] ↵
Crane PR
(2013) Ginkgo: The Tree That Time Forgot (Yale University Press, New Haven, CT), p 408.
.

[2] Crane PR

[3] ↵
Zhou ZY
(2009) An overview of fossil Ginkgoales. Palaeoworld 18(1):1–22.
.
OpenUrl CrossRef

[4] Zhou ZY

[5] ↵
Zhou ZY
(1991) Phylogeny and evolutionary trends of Mesozoic ginkgoaleans: A preliminary assessment. Rev Palaeobot Palynol 68(3-4):203–216.
.
OpenUrl CrossRef

[6] Zhou ZY

[7] ↵
Krassilov VA
(1972) Mesozoic Flora from the Bureja River (Ginkgoales and Czekanowskiales) (Nauka, Moscow), p 115 (in Russian).
.

[8] Krassilov VA

[9] ↵
Stanislavsky FA
(1973) The new genus Toretzia from the Upper Triassic of the Donetz basin and its relation to the genera of the order Ginkgoales. Paleont Zh 1:88–96 (in Russian).
.
OpenUrl

[10] Stanislavsky FA

[11] ↵
Harris TM
(1935) The fossil flora of Scoresby Sound, East Greenland, Part 4. Medd Gronl 112(1):1–176.
.
OpenUrl

[12] Harris TM

[13] ↵
Meyen SV
(1984) Basic features of gymnosperm systematics and phylogeny as shown by the fossil record. Bot Rev 50(1):1–111.
.
OpenUrl CrossRef

[14] Meyen SV

[15] ↵
Meyen SV
(1987) Fundamentals of Palaeobotany (Chapman & Hall, London), p 432.
.

[16] Meyen SV

[17] ↵
Shi G, et al.
(January 24, 2017) Leaves of Podozamites and Pseudotorellia from the Early Cretaceous of Mongolia: Stomatal patterns and implications for relationships. J Syst Paleontol doi:10.1080/14772019.2016.1274343.
.
OpenUrl CrossRef

[18] Shi G, et al.

[19] ↵
Schweitzer HJ,
Kirchner M
(1995) Die Rhäto-Jurassischen Floren des Iran und Afghanistans. 8. Ginkgophyta. Palaeontographica B 237:1–58.
.
OpenUrl

[20] Schweitzer HJ,

[21] Kirchner M

[22] ↵
Wang ZQ
(1984) Plant kingdom. Palaeontological Atlas of North China II Mesozoic, eds Tianjin Institute of Geology and Mineral Resources (Geological Publishing House, Beijing), pp 223–296, 367–384 (in Chinese).
.

[23] Wang ZQ

[24] ↵
Chen F,
Meng XY,
Ren SQ,
Wu CL
(1988) The Early Cretaceous Flora of Fuxin Basin and Tiefa Basin, Liaoning Province (Geological Publishing House, Beijing), p 180 (in Chinese).
.

[25] Chen F,

[26] Meng XY,

[27] Ren SQ,

[28] Wu CL

[29] ↵
Gordenko NV
(2010) Vladimariales ordo nov. (Gymnospermae) from the Middle Jurassic (Kursk Region, European Russia). Paleontol J 44(10):1281–1307.
.
OpenUrl

[30] Gordenko NV

[31] ↵
Shi G, et al.
(2016) Early Cretaceous Umkomasia from Mongolia: Implications for homology of corystosperm cupules. New Phytol 210(4):1418–1429.
.
OpenUrl

[32] Shi G, et al.

[33] ↵
Herrera F, et al.
(2015) A new voltzian seed cone from the Early Cretaceous of Mongolia and its implications for the evolution of ancient conifers. Int J Plant Sci 176(8):791–809.
.
OpenUrl

[34] Herrera F, et al.

[35] ↵
Leslie AB, et al.
(2013) Pinaceae-like reproductive morphology in Schizolepidopsis canicularis sp. nov. from the Early Cretaceous (Aptian-Albian) of Mongolia. Am J Bot 100(12):2426–2436.
.
OpenUrl Abstract/FREE Full Text

[36] Leslie AB, et al.

[37] ↵
Herrera F, et al.
(2016) New fossil Pinaceae from the Early Cretaceous of Mongolia. Botany 94:885–915.
.
OpenUrl

[38] Herrera F, et al.

[39] ↵
Shi G, et al.
(2014) Whole-plant reconstruction and phylogenetic relationships of Elatides zhoui sp. nov. (Cupressaceae) from the Early Cretaceous of Mongolia. Int J Plant Sci 175(8):911–930.
.
OpenUrl CrossRef

[40] Shi G, et al.

[41] ↵
Herrera F, et al.
(2017) Cupressaceae conifers from the Early Cretaceous of Mongolia. Int J Plant Sci 178(1):19–41.
.
OpenUrl

[42] Herrera F, et al.

[43] ↵
Leslie AB,
Beaulieu JM,
Crane PR,
Knopf P,
Donoghue MJ
(2015) Integration and macroevolutionary patterns in the pollination biology of conifers. Evolution 69(6):1573–1583.
.
OpenUrl

[44] Leslie AB,

[45] Beaulieu JM,

[46] Crane PR,

[47] Knopf P,

[48] Donoghue MJ

[49] ↵
Thomas HH
(1925) The Caytoniales, a new group of angiospermous plants from the Jurassic rocks of Yorkshire. Philos Trans R Soc Lond B Biol Sci 213(402-410):299–363.
.
OpenUrl FREE Full Text

[50] Thomas HH

[51] ↵
Thomas HH
(1933) On some pteridospermous plants from the Mesozoic rocks of South Africa. Philos Trans R Soc Lond B Biol Sci 222(483-493):193–265.
.
OpenUrl

[52] Thomas HH

[53] ↵
Harris TM
(1940) Caytonia Ann Bot (Lond) 4(16):713–734.
.
OpenUrl

[54] Harris TM

[55] ↵
Hori T, et al.
Zhou ZY
(1997) Mesozoic ginkgoalean megafossils: A systematic review. Ginkgo biloba—A Global Treasure—From Biology to Medicine, ed Hori T, et al. (Springer, Tokyo), pp 183–206.
.

[56] Hori T, et al.

[57] Zhou ZY

[58] ↵
Zhou ZY,
Zhang BL
(1988) Two new ginkgoalean female reproductive organs from the Middle Jurassic of Henan Province. Sci Bull 33(4):1201–1203.
.
OpenUrl

[59] Zhou ZY,

[60] Zhang BL

[61] ↵
Zhou ZY,
Zhang BL
(1989) A Middle Jurassic Ginkgo with ovule-bearing organs from Henan, China. Palaeontographica B 211(4-6):113–133.
.
OpenUrl

[62] Zhou ZY,

[63] Zhang BL

[64] ↵
Nosova NV
(2013) Revision of the genus Grenana Samylina from the Middle Jurassic of Angren, Uzbekistan. Rev Palaeobot Palynol 197(1-4):226–252.
.
OpenUrl

[65] Nosova NV

[66] ↵
Kvaček J,
Falcon-Lang HJ,
Dasková J
(2005) A new Late Cretaceous ginkgoalean reproductive structure Nehvizdyella gen. nov. from the Czech Republic and its whole-plant reconstruction. Am J Bot 92(12):1958–1969.
.
OpenUrl Abstract/FREE Full Text

[67] Kvaček J,

[68] Falcon-Lang HJ,

[69] Dasková J

[70] ↵
Doweld AB
(2001) Prosyllabus Tracheophytorum. Tentamen Systematis Plantarum Vascularium (Tracheophyta) (Geos, Moscow), p 110.
.

[71] Doweld AB

[72] ↵
Anderson JM,
Anderson HM
(2003) Heyday of the gymnosperms: Systematics and biodiversity of the Late Triassic Molteno fructifications. Strelitzia 15:1–398.
.
OpenUrl

[73] Anderson JM,

[74] Anderson HM

[75] ↵
Bomfleur B, et al.
(2011) Systematics and paleoecology of a new peltaspermalean seed fern from the Triassic polar vegetation of Gondwana. Int J Plant Sci 172(6):807–835.
.
OpenUrl CrossRef

[76] Bomfleur B, et al.

[77] ↵
Naugolnykh SV
(2012) Vetlugospermum and Vetlugospermaceae: A new genus and family of peltasperms from the Lower Triassic of Moscow syneclise (Russia). Geobios 45(5):451–462.
.
OpenUrl

[78] Naugolnykh SV

[79] ↵
Naugolnykh SV
(2007) Permian floras of the Urals. Transactions of Geological Institute of Russian Academy of Sciences, vol. 524 (Geos, Moscow).
.

[80] Naugolnykh SV

[81] ↵
Naugolnykh SV
(2008) A new gymnosperm Sylvocarpus armatus gen. et sp. nov. from the Lower Permian of the Ural Mountains. Paleontol J 42(4):431–439.
.
OpenUrl

[82] Naugolnykh SV

[83] ↵
Naugolnykh SV,
Oskolski AA
(2010) An advanced peltasperm Permoxylocarpus trojanus Naug. from the Lower Permian of the Urals (Russia): An ancient case of entomophily in gymnosperms? Wulfenia 17:29–43.
.
OpenUrl

[84] Naugolnykh SV,

[85] Oskolski AA

[86] ↵
Meyen SV
(1977) The Cardiolepidaceae, a new Permian conifer family from north Eurasia. Paleontol J 3:128–138.
.
OpenUrl

[87] Meyen SV

[88] ↵
Klavins SD,
Taylor TN,
Taylor EL
(2002) Anatomy of Umkomasia (corystospermales) from the triassic of antarctica. Am J Bot 89(4):664–676.
.
OpenUrl Abstract/FREE Full Text

[89] Klavins SD,

[90] Taylor TN,

[91] Taylor EL

[92] ↵
Axsmith BJ,
Taylor EL,
Taylor TN,
Cuneo NR
(2000) New perspectives on the Mesozoic seed fern order Corystospermales based on attached organs from the Triassic of Antarctica. Am J Bot 87(6):757–768.
.
OpenUrl Abstract/FREE Full Text

[93] Axsmith BJ,

[94] Taylor EL,

[95] Taylor TN,

[96] Cuneo NR

[97] ↵
Bomfleur B,
Escapa IH,
Taylor EL,
Taylor TN
(2012) Modified basal elements in Dicroidium fronds (Corystospermales). Rev Palaeobot Palynol 170:15–26.
.
OpenUrl

[98] Bomfleur B,

[99] Escapa IH,

[100] Taylor EL,

[101] Taylor TN

[102] ↵
Pigg KB
(1990) Anatomically preserved Dicroidium foliage from the central Transantarctic Mountains. Rev Palaeobot Palynol 66(1-2):129–145.
.
OpenUrl CrossRef

[103] Pigg KB

[104] ↵
Friis EM, et al.
(2007) Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature 450(7169):549–552.
.
OpenUrl CrossRef PubMed

[105] Friis EM, et al.

[106] ↵
Hilton J,
Bateman RM
(2006) Pteridosperms are the backbone of seed plant phylogeny. J Torrey Bot Soc 133(1):119–168.
.
OpenUrl CrossRef

[107] Hilton J,

[108] Bateman RM

[109] ↵
Rothwell GW,
Stockey RA
(2016) Phylogenetic diversification of Early Cretaceous seed plants: The compound seed cone of Doylea tetrahedrasperma. Am J Bot 103(5):923–937.
.
OpenUrl Abstract/FREE Full Text

[110] Rothwell GW,

[111] Stockey RA

[112] ↵
Archangelsky S
(1965) Fossil Ginkgoales from the Ticó flora, Santa Cruz Province, Argentina. Bull Br Mus (Nat Hist). Geol 10(5):121–137.
.
OpenUrl

[113] Archangelsky S

[114] ↵
Del Fueyo GM,
Archangelsky S
(2001) New studies on Karkenia incurva Archang. from the Early Cretaceous of Argentina. Evolution of the seed cone in Ginkgoales. Palaeontographica B 256:111–121.
.
OpenUrl

[115] Del Fueyo GM,

[116] Archangelsky S

[117] ↵
Ichinnorov N
(2003) Palynocomplex of the Lower Cretaceous sediments of eastern Mongolia. Geosci 22:12–16.
.
OpenUrl

[118] Ichinnorov N

[119] ↵
Nichols DJ,
Matsukawa M,
Ito M
(2006) Palynology and age of some Cretaceous nonmarine deposits in Mongolia and China. Cretac Res 27(2):241–251.
.
OpenUrl

[120] Nichols DJ,

[121] Matsukawa M,

[122] Ito M

[123] ↵
Erdenetsogt B-O,
Lee I,
Bat-Erdene D,
Jargal L
(2009) Mongolian coal-bearing basins: geological settings, coal characteristics, distribution, and resources. Int J Coal Geol 80(2):87–104.
.
OpenUrl

[124] Erdenetsogt B-O,

[125] Lee I,

[126] Bat-Erdene D,

[127] Jargal L

[128] ↵
Nixon KC
(1999) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15(4):407–414.
.
OpenUrl CrossRef

[129] Nixon KC

Main menu

User menu

Search

The presumed ginkgophyte Umaltolepis has seed-bearing structures resembling those of Peltaspermales and Umkomasiales

Significance

Abstract

Results