- Research article
- Open Access
Schmeissneria: A missing link to angiosperms?
© Wang et al; licensee BioMed Central Ltd. 2007
- Received: 23 November 2006
- Accepted: 07 February 2007
- Published: 07 February 2007
The origin of angiosperms has been under debate since the time of Darwin. While there has been much speculation in past decades about pre-Cretaceous angiosperms, including Archaefructus, these reports are controversial. The earliest reliable fossil record of angiosperms remains restricted to the Cretaceous, even though recent molecular phylogenetic studies suggest an origin for angiosperms much earlier than the current fossil record.
In this paper, after careful SEM and light microscopic work, we report fossils with angiospermous traits of the Jurassic age. The fossils were collected from the Haifanggou Formation (middle Jurassic) in western Liaoning, northeast China. They include two female structures and an associated leaf on the same slab. One of the female structures is physically connected to the apex of a short shoot. The female organs are borne in pairs on short peduncles that are arranged along the axis of the female structure. Each of the female organs has a central unit that is surrounded by an envelope with characteristic longitudinal ribs. Each central unit has two locules completely separated by a vertical septum. The apex of the central unit is completely closed. The general morphology places these fossils into the scope of Schmeissneria, an early Jurassic genus that was previously attributed to Ginkgoales.
Because the closed carpel is a character only found in angiosperms, the closed apex of the central unit suggests the presence of angiospermy in Schmeissneria. This angiospermous trait implies either a Jurassic angiosperm or a new seed plant group parallel to angiosperms and other known seed plants. As an angiosperm, the Liassic age (earliest Jurassic) of Schmeissneria microstachys would suggest an origin of angiosperms during the Triassic. Although still uncertain, this could have a great impact on our perspective of the history, diversity and systematics of seed plants and angiosperms.
- Central Unit
- Short Shoot
- Female Organ
- Winged Seed
- Female Structure
Angiosperms are the dominating plant group in current vegetation. They account for the majority of terrestrial primary production, demonstrate the highest diversity in the plant kingdom, and dominate highly diversified habitats [1–4]. The rapid radiation and diversification of angiosperms during the Cretaceous led to major ecological changes on the earth, the latter were a prerequisite for many critical evolutionary events  including the later evolution of human beings. However, the origin of this important plant group has remained obscure since the time of Darwin [3, 5–8]. Although palaeobotanists have been searching for pre-Cretaceous angiosperms and some speculate that the angiosperm line may extend back to the Triassic [8, 9], the earliest angiosperm fossil records are still restricted to the Cretaceous hitherto [3–5, 10–12]. Therefore, it is not surprising that whenever something related to the origin of angiosperms is discovered, such as Sanmiguelia  and Archaefructus [6, 7, 14], it not only receives attention but also triggers controversy within and beyond academic circles. Western Liaoning has been a focus of palaeontological research because of its wealth of fossil plants [7, 15–20] and animals [21, 22]. Pan's claims of Jurassic angiosperms [15–17] once raised great interest in fossil plants in this region, but they are currently not generally accepted [18, 23].
Schmeissneria was first identified as a member of the Ginkgoales , with a history dating back to 1838 . Schmeissneria (Stachyopitys) was once thought to be related to conifers [25, 26]. Its ginkgoalean affinity was initially proposed based on association: Schenk (1890) classified it as a premature male flower of Baiera, therefore placing Schmeissneria (Stachyopitys) in the Ginkgoales . Based on the data available now, Schenk's conclusion on Schmeissneria (Stachyopitys) has been proven erroneous. First, the male nature of Schmeissneria (Stachyopitys) has been disproved . Second, the connection between Baiera and Schmeissneria has been nullified [24, 29]. Third, Schmeissneria has been proven connected with Glossophyllum? sp. A , which is dissimilar to any known ginkgoalean leaf . All of this evidence refuted Schenk's initial proposal on the ginkgoalean affinity of Schmeissneria (Stachyopitys), and thus Schmeissneria lost its affinity. Apparently, Kirchner and Van Konijnenburg-Van Cittert did not realize what they had accomplished and conveniently put Schmeissneria in Ginkgoales . In addition, there are a few characters that make Schmeissneria even more mysterious: 1) the internal structure of the reproductive organ, which is important for systematics, is hitherto unknown; 2) its connected vegetative parts do not provide enough information to resolve its systematic position; and 3) its winged seeds are never found in other Ginkgoales.
Here new specimens of Schmeissneria, S. sinensis Wang sp. nov., are reported from the Haifanggou Formation (middle Jurassic) in western Liaoning, China. The new information from these materials allowed us to re-examine the affinity of Schmeissneria.
Description of the specimens
Only the apex of a short shoot was organically connected to a female structure (Figs. 1a,c). It was about 2.4 mm long and 2.3 mm wide, with leaf cushions (Fig. 1c). The leaf cushion was about 0.56 mm high and 1.8 mm wide (Fig. 1c).
The female organs were about 1.6–4.6 mm long, about 1.2–4 mm in diameter, widest at the base and constricted at the apex (Figs. 2a–f, 3a, 4a,c). They had an onion-like appearance, including a central unit and a sheathing envelope (Figs. 2b,e, 3a,d, 4c,d). The envelope was longitudinally ribbed internally and externally (Figs. 2a–b,f, 3a,j, 4a,c,d). The apices of the female organs pointed away from the axis of the female structure (Figs. 2a–b, 4a,d). The envelope apex of a large female organ (Figs. 2a–b, 2e–f) was more extended than that of a smaller one (Figs. 2c–d, 3d). The envelope, sheathing around the central unit, was of multiple parts (Fig. 3c), and inflated (Figs. 2a–b, 3a). The surface of the envelope was smooth locally with elongated epidermal cells (Fig. 3b). The cells within the envelope were elongated: 18–33 μm long and 6–12 μm wide (Fig. 3b). The rugulate pollen grains found on the internal surface of the envelope apex were about 26 μm in diameter (Figs. 3j–o). The central units were about 1.5 to 3.3 mm long and 1 to 3.2 mm in diameter, widest basally and constricted apically (Figs. 2a–b,e, 3a,d, 4a,c). The central unit was attached to a receptacle by a wide base about 1.6 mm in diameter (Fig. 3a), with its apex approaching that of the envelope (Figs. 3d–f, 4c). The distal part of the central unit wall was longitudinally ribbed internally and externally (Figs. 3a,e). No elaborated pollen reception site was observed (Figs. 3d–f,i). The central unit was bilocular, completely separated by a 9 to 19 μm thick vertical septum (Figs. 2f–h, 3d–i, 4b–c). The central unit internal walls were smooth (Figs. 2g, 4b) and flat at the base and rough in the upper part (Figs. 2g, 3e,f, 4b). The septum was complete, extending from the base (Figs. 2g, 4b), through the middle part (Figs. 3g–h) to the apex (Figs. 2h, 3e–f,i, 4c) of the central unit. The septum was papillate (Fig. 2h and its inset).
Remarks: Although two rugulate pollen grains (Figs. 3j–o) were found on the internal surface of the envelope apex, their relationship to S. sinensis was tentative and subject to further validation. Stachyopitys preslii (possible male organ of Schmeissneria ) was only associated with but never connected to Schmeissneria microstachys , and may also be related to other Ginkgoalean plants .
The specimens studied here were generally identical to Schmeissneria , especially the holotype of S. microstachys (pl. I, fig. 1) . The latter closely resembled S. sinensis in spicate structure, paired female organs, female organ morphology, longitudinally ribbed axes of female structures, and the insertion of a female structure on the apex of a short shoot, even though the specimens described here and S. microstachys were from different continents and geological epochs, and S. sinensis had more densely clustered female organs and much shorter peduncles of female organ pairs (0.5 mm rather than 2 mm long). Fortunately, the internal structure was preserved in S. sinensis and thus shed new light on its affinity.
Structure and Interpretation
In all non-angiospermous seed plants, there is an opening at the nucellar apices to allow the pollen grains to approach the ovules [31, 32]. The dimension of the opening has to be large enough to let pollen grains pass through. Unlike seed ferns or other gymnosperms, no opening was found at the apex of the central unit in S. sinensis (Figs. 3d–f). In the view from the interior of the central unit to its apex (Fig. 3f), any opening larger than 20 μm (the normal size of an average pollen grain) should be visible if present on the central unit wall. Although the preservation of the fossils reported here was not perfect, the female organs had both the cellular details (Fig. 3b) and a septum only about 10 μm thick (Fig. 3i) preserved. The preservation of such fine details suggested that preservation fidelity was high enough for structures above the cellular level. Therefore the central unit apex of S. sinensis was physically closed, at least to pollen grains. This was essentially different from the situation in Caytonia, in which there are numerous ovules within a cupule that has an opening for pollen grain entry before pollination [33, 34]. There were two alternative interpretations for the absence of pollen entry in Schmeissneria: one was that the pollen entry did not exist at all; the other was that the pollen entry had been obliterated. The latter situation has been seen in Gnetum [32, 35], Ephedra, Pinus, Cedrus, Cephalotaxus , and possibly in Caytonia [33, 34], in all of which the pollen canals were plugged or obliterated by tissue outgrowth or cell proliferation after pollination. This tissue growth or cell proliferation is concomitant with morphological changes [35, 36]. However, in the case of Schmeissneria this alternative appeared unlikely for the following reasons: 1) the female organs in Figs. 3d–f were in their early stages (pre-pollination), suggested by their smaller sizes and morphology different from winged seeds ; 2) there was neither any trace of abnormal tissue outgrowth nor sudden changes in the wall at the apex of the central unit (Figs. 3d–f), unlike what is observed in Gnetum , Cephalotaxus, and Ephedra . Consequently, the other alternative was more reasonable and acceptable. This was the major reason that the authors correlated the structures of Schmeissneria's central unit, envelope, female organ and female structure with an angiosperm's gynoecium, perianth, flower and inflorescence.
A septum extended from the base (Figs. 2g, 4b), through the middle (Figs. 3g–h), to the apex (Figs. 2h, 3e,f,i, 4c) of the central unit. The septum separated the central unit into two independent locules (Figs. 2f–h, 3h–i, 4b–c). The latter were suggestive of two carpels in a central unit (equivalent to gynoecium in angiosperm) . The septum appeared as a ridge raised above the smooth wall of the central unit in the longitudinal view (Fig. 2g). Its smooth connections to the side walls (Figs. 3h–i) and base (Fig. 2g) of the central units suggested that the septum represented an original structure rather than an artefact or alteration. The repeated presence of a septum of various poses in four individual female organs (Figs. 2g–h, 3d–i) also strongly suggested its truthful existence. Up until now there has been no report of a complete septum in a seed or ovule in any gymnosperm. Sometimes paired ovules in Ginkgo may appear to have a membraneous division in between. However, their ovules have never been completely enclosed before pollination, the tips of the paired ovules point to different directions, and there is no empty interior space within any ovule. Therefore the paired ovules of Ginkgo were distinct from the central unit of Schmeissneria.
Schmeissneria sinensis had female organs of various ontogenetic stages, from small premature ones at the top to large mature ones at the base of the female structures (Figs. 1, 2, 3, 4). Considering the slight morphological difference between the topmost (most immature) and bottommost (most mature) female organs, it was reasonable to assume that the female organs reported here, especially the smaller ones, were not yet pollinated. The rough internal surface in the upper portion of the central unit (Fig. 2g and Fig. 4b(g)) and the longitudinal ribs on it (Fig. 3e), in contrast to the smooth surface in the lower portion of the internal surface of the central unit (Fig. 2g and Fig. 4b(a,c)), suggested that the upper portion of the central unit was empty, while the lower part was occupied by another inherent substructure (probably an ovule). This situation was unlikely in ovules or seeds, which rarely, if ever, have an empty interior space. It was also unlikely to be a result of differentiated preservation related to histological differences because the presence or absence of tissues is a morphological rather than histological character. The winged seeds connected to vegetative parts reported by Kirchner and Van Konijnenburg-Van Cittert (Fig. 1b, ) were distinct from the female organs reported here, implying the immaturity of S. sinensis. Considering the aforementioned details, since Wcislo-Luraniec  and Kirchner and Van Konijnenburg-Van Cittert  have proven the female nature of Schmeissneria, the immature central unit with two locules and a closed apex sheathed by an envelope can be interpreted as a gynoecium of two carpels surrounded by a perianth. This suggested that the carpels (gynoecium) in Schmeissneria were closed before pollination, a situation quite different from the "angiospermy" after pollination in gymnosperms .
In 1838, Presl (pl. 33, fig. 12 only) reported fructifications from Keuper Sandstone (actually Liassic age ) of Reundorf near Bamberg, Germany . He considered them male flowers of Pinites microstachys (Conifers). Schenk (pl. XLIV, figs. 11, 12 only, 1867) investigated similar fossils from Veitlahm near Kulmbach, describing them as female flowers of Stachyopitys preslii, which was associated with Schizolepis (a coniferous genus) . Later Schenk (fig. 180b only, 1890) assigned Stachyopitys preslii as male fructifications of Baiera münsteriana (Ginkgoales), and interpreted the formerly "female fructifications" as male flowers in an early stage . This association between Baiera and Stachyopitys proposed by Schenk  was later widely accepted (taf. 29, abb. 4 ; fig. 239c ; fig. 375d ; abb. 303h ; fig. 198B ; taf. 1, fig. lower left ; fig. 35d ). Actually, fossils of various affinities had been lumped into Stachyopitys preslii . Wcislo-Luraniec (pl. 1 and textfigs. 1, 2, 1992) cast doubt on the male nature of Stachyopitys preslii because of the discovery of "cupules," thereby proving the female nature of the fossil . At the same time, Stachyopitys preslii was found connected with Weber's (p58, taf. 5, fig. 51 ) Glossophyllum? sp. A . With more complete fossil materials available, a new genus, Schmeissneria (Ginkgoales), was established for the female Stachyopitys and officially separated from the male Stachyopitys (Figure 1 and pls. I-III, pl. IV, fig. 1, ). It appeared that Kirchner and Van Konijnenburg-Van Cittert did not realize that they had undermined the ground for the ginkgoalean affinity of the fossil and uncritically accepted the previous conclusion as true . Furthermore, they did not give any valid reason for why they put the genus in Ginkgoales except for comparing the paired "ovules" of Schmeissneria and the paired ovules of Ginkgo in two sentences (p.207) . Apparently, their comparison was not sufficient to place the fossil in Ginkgoales with confidence because the characteristic collar at the base of Ginkgo seed was absent in all specimens of Schmeissneria and the winged seeds of Schmeissneria were never seen in any Ginkgoales. However, re-examining the references indicated that 1) the discovery of the connection between Stachyopitys (Schmeissneria) preslii and Weber's Glossophyllum? sp. A disproved the relationship between Stachyopitys (Schmeissneria) preslii and Baiera münsteriana proposed by Schenk ; and 2) Glossophyllum? sp. A did not belong to the ginkgoalean Glossophyllum . Therefore, Schmeissneria was dangling phylogenetically. Since the connected vegetative organs could not resolve its affinity, the affinity of Schmeissneria had to be resolved based on the internal structure of its own female reproductive organs.
Comparison of Schmeissneria to Ginkgoales, Gnetales, and angiosperms.
Spiral on short shoot
Opposite, whorled, spiral
Slender-cuneiform, obtuse apex
Fan-shaped, or cuneiform
Strap-like, triangular, linear or oval-shaped
Parallel or reticulate
Reproductive axis articulate
-(? bract scale seed complex)
Whorled, paired, or N/A
Ovuliferous unit position
On peduncle tip, in pair
On peduncle tip, single, pair or more in group
In bract axil, one to many in a group
Ovuliferous unit with septum
Completely enclosed by central unit wall
Exposed through micropyle
Exposed through micropylar tube
Completely enclosed by carpel or secretion
Several characters are used to distinguish angiosperms and gymnosperms, including enclosed ovules/seeds, double fertilization, vessel elements, reticulate venation, and tectate-columellate pollen wall structure. However, it is harder to draw a line between these two groups than it might appear: neither of the above characters is a touchstone for angiosperms [1, 3]. None of the above characters is unique to angiosperms. All the ovules in gymnosperms are exposed when pollination occurs, but at least some of the ovules/seeds are enclosed after fertilization (Caytoniales ; Gnetales ; Coniferales and Gnetales ; Coniferales ). Angiosperms have completely closed carpels. However, in some basal groups this closure is by secretion, and not by postgenital fusion (e.g., Amborellaceae, Schisandraceae, Austrobaileyaceae, Trimeniaceae ). Double fertilization has been reported in non-angiosperms, as in Ephedra [31, 50] and Abies . Vessel elements are also present in various non-angiosperms, such as Selaginella, Equisetum, Pteridium , Gigantopteriales , and Gnetales [1, 4, 31, 32]. Reticulate venation has been reported in non-angiosperms, including Dipteridaceae [52–55], Gigantopteriales [56, 57], Caytoniales [33, 58], Glossopteridales [5, 40, 46, 58], Bennettitales , and Gnetales [31, 32]. Pollen grains with an angiosperm-like wall structure have been reported in many pre-Cretaceous plants [59–61] that are regarded as non-angiosperms by others . According to Tomlinson and Takaso , the only consistent difference between angiosperms and gymnosperms is that the ovules at pollination are exposed in gymnosperms, but enclosed in angiosperms. Fortunately, the closed carpel at or before pollination is a character that is sufficient to identify an angiosperm alone. This was one of the characters used here to resolve the affinity of Schmeissneria.
Two characters separated Schmeissneria from known gymnosperms: the vertical complete septum and the closed apex of the central unit. Considering all available information and the definitions of plant groups, there were two alternatives left to us: 1) accepting that Schmeissneria as a new angiosperm in the Jurassic, or 2) proposing Schmeissneria as a new gymnosperm. Although the specialized features of the early Cretaceous angiosperm Archaefructus  and other data [8, 9] may imply the possible existence of angiosperms before the Cretaceous, Schmeissneria did not look like any known typical angiosperm. However, this dissimilarity was conceivable and understandable since 1) "angiophytes" had not evolved any typical identifiable angiospermous character , and 2) many angiospermous taxa were much more diversified then and much of that diversification had since become extinct . Extreme caution should be exercised when a Jurassic angiosperm, along with their relatives of which we know very little, is compared with the extant angiosperms.
If accepted as an angiosperm, because of its early Jurassic age in Europe, Schmeissneria would push the origin of angiospermy back to the Triassic. This would make the claims of Triassic angiosperms [13, 59–61], [63, 64] less surprising, and also help to bridge the gap between the fossil record [3, 5, 10–12, 65] and molecular data [66–72]. However, it should be kept in mind that Schmeissneria might well represent early angiosperms still sporadic in the vegetation dominated by gymnosperms, that it might bear no direct relationship with any known angiosperm, and that the presence of Schmeissneria in the flora was still far different from the radiation and diversification of angiosperms.
Schmeissneria is an interesting Jurassic plant that bears a trait of angiosperms (two separated locules in a central unit with a closed apex). This feature has a counterpart in angiosperms (two carpels in the gynoecium). Based on the current definition of angiosperms, Schmeissneria could be classified as an angiosperm. Otherwise, a new group, Schmeissneriales, would have to be established for Schmeissneria. The bottom line is that in whatever position Schmeissneria is placed in the future, it increases the diversity of seed plants and challenges people regarding the systematics of seed plants. Undoubtedly, Schmeissneria requires further study.
Schmeissneria Kirchner et Van Konijnenburg-Van Cittert 1994, emend.
Type species: Schmeissneria microstachys (Presl 1838) Kirchner and Van Konijnenburg-Van Cittert 1994.
Emended diagnosis (based on previous work and present observation)
Plants with long- and short-shoots. Leaves inserted helically on short shoots. Short shoots with leaf cushions. Leaf slender, slightly cuneiform, apex obtuse. Veins parallel, more than two in the proximal part of the leaf, branching in the lower third of the lamina.
Female structures spicate, with a slender axis. Axis of the female structure longitudinally ribbed. Female organ pairs connated basally, borne on a peduncle, arranged along the axis of the female structure. Female organ with a central unit and a sheathing envelope. Envelope of undetermined number of parts, inflated, longitudinally ribbed internally and externally. Central unit bilocular, astylous, with a vertical septum, with longitudinal ribs distally both internally and externally. Seed winged (?).
Type locality: Reundorf near Bamberg, Germany.
Further locality: Oberwaiz, Unternschreez (Lautner) and Schnabelwaid (Creußen) near Bayreuth, Veitlahm, Pechgraben near Kulmbach, Großbellhofen, Rollhofen (Wolfshöhe) northeast of Nuremberg (all in Germany); Odrowaz, Holy Cross Mounts, Poland; western Liaoning, China.
Stratigraphic horizon: Liassic, lower Jurassic (Germany and Poland); middle Jurassic (China).
Comparison between Schmeissneria and other possibly related fossil taxa.
No. appendages per peduncle
Appendage opening orientation
Seed/central unit position
Ovule completely enclosed
No. ovules/seeds per cupule/central unit
Peduncle connects to
Globose, in pair
Away from axis
More or less extended
Within the sheathing envelope
Away from axis
Below the wing, enclosed (?)
More or less extended
Axil of scale
Axil of scale
1 (2 valves)
Away from axis
Round, thickened margin
Within capsule, axil of valves
Schmeissneria sinensis Wang sp. nov.
Diagnosis: The same as that of the genus, except that female organs are densely clustered along the axis of the female structure and the peduncles of the female organ pairs are short in this new species.
Description (see Results)
Paratype: 8604b, 8604c.
Etymology: sinensis referring to China, for specimens found in China.
Type locality: Sanjiaochengcun, Jinxi, western Liaoning, China.
Stratigraphic horizon: the Haifanggou Formation, middle Jurassic; equivalent to Aalenian-Bajocian.
Depository: Institute of Botany, the Chinese Academy of Sciences, Beijing, China.
Remarks: The specimens described here and S. microstachys were from different continents and geological epochs, and S. sinensis had more densely clustered female organs and much shorter peduncles of female organ pairs (0.5 mm rather than 2 mm long). Therefore, a new species, S. sinensis, was established for the specimens from Liaoning, China.
The studied specimens included two weakly coalified compressions of female structures and one associated leaf. Coaly membranes were found only on the surface of the specimens (Fig. 3a), while most parts of the specimens were replaced by unidentified minerals. The fossils were exposed by trimming away the fine matrix. They were observed under a Zeiss stereomicroscope, photographed with a Nikon 4500 and a Nikon Stereomicroscope SMZ1000 with digital camera DMX1200F. Some of the specimens (Figs. 3b–f, 3j–o) were coated with gold and observed under a Hitachi S800 SEM at Institute of Botany, the Chinese Academy of Sciences. After SEM observations, a piece of specimen (Fig. 3d–f) was embedded in an Epon 812 resin, ground into a thin section, and observed with the light microscope (Fig. 3i). One of the trimmed fragments was embedded in Epon 812 resin, ground, coated with gold, and observed with the SEM again (Figs. 3g–h). The SEM images were recorded on black-white negatives. All photographs were later scanned, processed, and pieced together for publication using Photoshop 7.0.
The authors thank Dr. Zhiyan Zhou, Dr. James A. Doyle, Dr. Walter S. Judd, Dr. Peter Stevens, Dr. Dennis W. Stevenson, Dr. Shijun Wang, Dr. Meizhen Cao, Dr. Zhenyu Li, Dr. Jianan Zhu, Dr. Liangqian Li, Dr. Catarina Rydin, Dr. Steven Manchester, Dr. David Dilcher for their discussions and help during this research, Dr. Ye Chen for collecting the specimens, Mr. Yinhou Xiao for help with SEM, Dr. Min Feng, Ms. Jie Wen, Mr. Zhi Du, Mr. Xuejian Yang, and Mr. Zhaoyi Meng for help with the photography, Ms. Xin Xu for help with the drawings, and Dr. Douglas McKinnon, Dr. Williams Rose and Ms. Margaret Joyner for help with English. Finally, we want to thank the two anonymous reviewers for their kind and constructive help with this manuscript. This research was supported by the Jiangsu Planned Project for Postdoctoral Research Funds (XW), Royal Society K. C. Wong Fellowships (XW), China Postdoctoral Science Foundation (No. 2005037746) (XW), State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS, No. 053103) (XW), the Laboratory of Systematics and Evolutionary Botany and Herbarium at the Institute of Botany (BG), NSFC Programs (No. 40632010, No. J0630967, No. 39170058 and No. 49402018), and Deep Time RCN (XW).
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