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Plant Divers
Plant Divers
Plant Diversity
2096-2703
2468-2659
Kunming Institute of Botany, Chinese Academy of Sciences

S2468-2659(24)00022-2
10.1016/j.pld.2024.03.002
Report
A new gnetalean macrofossil from the Lower Cretaceous of the Laiyang Basin, eastern China
Jin Peihong a
Zhang Mingzhen zhangmzh08@lzb.ac.cn
a⁎
Du Baoxia b
Zhang Jing b
Sun Bainian b
a Key Laboratory of Petroleum Resources, Northwest Institute of Eco–Environment and Resources, Chinese Academy of Sciences, Gansu Province, Lanzhou 730000, China
b Key Laboratory Western China's Mineral Resources of Gansu Province, Lanzhou University, Lanzhou 730000, China
⁎ Corresponding author. zhangmzh08@lzb.ac.cn
14 3 2024
9 2024
14 3 2024
46 5 678682
7 8 2023
22 2 2024
5 3 2024
© 2024 Kunming Institute of Botany, Chinese Academy of Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.
2024
Kunming Institute of Botany, Chinese Academy of Sciences
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Highlights

• A new species Laiyangia compacta gen. et sp. nov. with unusual female spikes was described from the Laiyang Formation.

• This species shows transitional morphology between early ephedroid and modern gnetoid.

• The epidermal microstructural character of this species provides a driver paleoclimate of Laiyang area in Early Cretaceous.
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pmcGnetophytes are a key group of plant for understanding seed plant phylogeny, partly because of their unique and elusive morphology, such as xylem with vessels, phloem with chaperones, reticular veins, and double fertilization (Endress, 1996). In particular, the ovule bears a membranous integument, the upper part of which extends beyond the seed envelope to form a micropylar tube. Therefore, gnetophytes occupy a unique evolutionary position in the phylogeny of seed plants and apparently represent a transition between angiosperms and other gymnosperms (Ran et al., 2018). Modern gnetophytes consist of only three families: Ephedraceae, Gnetaceae, and Welwitschiaceae, and each family contains only one genus. Ephedraceae (Ephedra L.) are the earliest diverging group of Gnetales, with a total of 70 extant species, and usually occur in cold and arid places in Asia, Europe, northern Africa, western North America and South America (Price, 1996; Yang et al., 2017b).

The earliest reliable fossil records of gnetophytes can be traced back to at least the Late Permian, but they are mostly preserved as fragmented twigs, leaves, and seed fossils (Wu et al., 1986; Wang, 2004). During the Early Cretaceous, gnetophytes were most abundant, and many gnetalean mega-fossils have been reported in Australia, Europe, North America, South America, Mongolia and particularly in northeastern China (Liaoning). These reported gnetophyte fossils show higher diversity of gnetophytes in Cretaceous than today, providing significant clues for studying the origin, evolution, and geological distribution patterns of this plant group. However, currently, there is no effective hypothesis or evidence on how the unique morphological features of gnetophytes have arisen or on the relationships between living and fossil species. Therefore, any fossil material related to gnetophyte plants is highly valuable and meaningful.

Here, we describe a new macrofossil plant of Ephedraceae from the Lower Cretaceous Laiyang Formation in Shandong Province, eastern China. This new reproductive shoot is well preserved and possesses unusual female spikes that distinguish it from all other known gnetophyte species. The new fossils may improve our understanding of the relationships and evolution of the divergent morphology within the gnetophytes, and help to understand the diversity and biogeography of modern species. The detail of geological setting and fossil preparation and illustration are provided in Appendix A.

1 Systematic description

Order—Gnetales Luerssen, 1879

Family—Ephedraceae Dumortier, 1829

Genus—Laiyangia P.H. Jin, gen. nov.

Etymology—The generic name “Laiyangia” is derived from the Laiyang localities where the specimens were collected.

Generic diagnosis—Reproductive shoots having swollen nodes and internodes; leaves opposite, triangular, the lower part ca. 2/3 fused into a sheath; female spikes compact with no observable nodes and internodes, axillary to leaves or terminal to twigs, shortly pedunculate and narrowly elongate, with 5–8 pairs of fertile bracts; bracts decussately opposite, triangular and incurved, with each subtending 1 axillary sessile seed; seeds ellipsoid and plump with a distal and hollow micropylar tube.

Type Species—Laiyangia compacta P.H. Jin, sp. nov.

Species—L. compacta P.H. Jin, sp. nov.

Holotype—SDLY–2020–41A, B (Figs. 1A (a, b, d-i) and 1B)Fig. 1 A, Laiyangia compacta gen. et sp. nov. a–c, Part and counterpart displaying the general morphology of the species; scale bars = 2 cm; a, b, Specimen no. SDLY–2020–41A, B; c, Specimen no. SDLY–2021–47A; d-h, Female spikes under stereo microscopy, Specimen no. SDLY–2020–41A, B.; d, Female spikes showing their position and decussately opposite fertile bracts, scale bars = 2 mm; e, the uppermost bract of the female spike displaying 4 seeds in the adaxial part and the hollow and straight micropylar tubes, scale bars = 1 mm; f, g, individual fertile bract displaying one seed in the adaxial part and the hollow and straight micropylar tube, scale bars = 1 mm; h, Straight internode of reproductive shoot displaying longitudinal striations, scale bars = 1 mm; i, Details of epidermal features in the outer epidermis of the seed envelope under fluorescence microscopy, showing epidermal cells and stomatal complexes (white arrow), Specimen no. SDLY–2020–41A; b = bract; s = seed; mt = micropylar tube. B, Reconstruction of Laiyangia compacta gen. et sp. nov., abbreviations: in = internode; n = node; l = leaf; b = bract; s = seed; mt = micropylar tube. C, Phylogenetic relationships of Laiyangia compacta gen. et sp. nov. (bold type) with illustrations based on constrained Parsimony analysis of morphological characters for extinct species plus living species (∗) conducted under TNT v.1.5 software, showing the most parsimonious position of L. compacta are within the family Ephedraceae. a, Siphonospermum; b, Prognetella; c, The compact female spikes type of Chengia–Liaoningia–Liaoxia group and Laiyangia compacta gen. et sp. nov.; d, Jianchangia; e, Female cone types of fossil and modern Gurvanella–Beipiaoa–Ephedra group.

Fig. 1

Other illustrated material—SDLY–2021–47A (Fig. 1A (c))

Type locality—Hangyadi Country, Laiyang City, Shandong Province, China (Fig. S1A, B)

Stratigraphy—Laiyang Formation, Lower Cretaceous (Hauterivian–Barremian) (Fig. S1A–C)

Repository—Key Laboratory of Petroleum Resources, Northwest Institute of Eco–Environment and Resources, Chinese Academy of Sciences, Gansu Province, China.

Etymology—The species name ‘compacta’ refers to the compactness of the female spikes of the fossil species.

Specific diagnosis—The same as for the genus.

Description—The studied material include several articulated reproductive branches of L. compacta, and two were preserved well enough to be described in detail. The most completely preserved specimen is, ca. 5.13–9.53 cm long and ca. 3.52–4.66 cm wide (Fig. 1A (a, b)). The main shoot is slightly curved, with nodes and internodes. Nodes are swollen; internodes are straight, 2.97–3.27 cm long, ca. 0.58–1.72 mm wide, with many fine longitudinal striations (Fig. 1A (h)). The main shoot branches at least 4 times. Lateral branches are spreading upwards at 30–80° and monopodial or dichasially ramifying once to twice. Leaves subtend lateral branches, are triangular, approximately 0.83–0.87 mm long and 0.46–0.51 mm wide at the widest point of the base, 2–3 opposite at nodes and fused into a sheath in the ca. 2/3 lower part, but their venation is indiscernible.

Female spikes are compact with no observable nodes and internodes, shortly pedunculate and narrowly elongate, axillary to leaves or terminal to twigs, ca. 1.36–2.70 cm long and 0.22–0.29 cm wide. Each female spike bears 5–8 pairs of fertile bracts (Fig. 1A (d)). Bracts are decussate and opposite and close to the axis, narrowly triangular with an acute apex, incurved, ca. 1.33–3.23 mm long and 0.35–0.52 mm wide. Each bract subtends one seed on the adaxial side, while in one specimen, it was observed that there may be four seeds on the adaxial side of the uppermost bract of the female spike (Fig. 1A (e–g)) (this feature is only an isolated occurrence). Seeds are ellipsoid and plump, approximately 1.73–2.42 mm long and 1.03–1.60 mm wide, and probably have an oval to cuspidate apex, a smooth surface, and fine longitudinal grooves. Each seed bears a thin outer envelope and a distal, hollow micropylar tube, approximately 0.70–0.86 mm long and ca. 0.04–0.07 mm in diam. (Fig. 1A (e–g)).

Fortunately, some epidermal features were observed in the outer epidermis of the seed envelope under fluorescence microscopy. Epidermal cells are irregular, polygonal or elongate rectangular with straight anticlinal walls, regularly arranged in longitudinal files, approximately 40–60 μm long and 10–20 μm wide (Fig. 1A (i)). Stomata are sparsely distributed and irregularly arranged in longitudinal files (Fig. 1A (i)). Stomatal complexes are rounded to elliptical in outline, haplocheilic, monocyclic, approximately 60–80 μm long and 40–50 μm wide. The guard cells are slightly sunken and generally surrounded by five to seven subsidiary cells, which form a ring (Fig. 1A (i)).

2 Comparison with other gnetalean plants

Laiyangiacompacta bears a reproductive shoot with nodes and internodes, a monopodial or dichasially branching pattern and opposite triangular leaves. Female spikes are narrowly elongate with short pedicels, straight or slightly curved, and relatively compact with no observable nodes or internodes. The female spikes consist of 5–8 pairs of decussate and opposite fertile bracts, each bract usually subtends one axillary sessile seed. All of these characteristics conform to the circumscription of the Ephedraceae. The integument in seeds of L. compacta is elongated to form long micropore tubes. This feature appears only in extant and extinct gnetalean plants, and in Bennettitales and some extinct members that are closely related to Gnetales, such as the Erdtmanithecales and some genera for which only scattered seed fossils are preserved that are not clearly classified (Mendes et al., 2008, 2010; Friis et al., 2009). Our new fossils clearly differ from Bennettitales the reproductive structure of which is a bisexual cone. Only dispersed reproductive structures (seeds, male cones, and pollen) are seen in the Erdtmanithecales, and the seeds have a three–valved seed envelope. Other characteristics of the female spikes cannot be further compared.

Over 54 fossil species of Gnetales have been reported from the Mesozoic of southern Europe, Australia, North America, South America, and Asia, especially in the Yixian Formation of northeastern China, which has the richest diversity. However, most of these fossil species can be distinguished from our fossils by morphology of their leaves, bracts and seeds, and a comparison between Laiyangia compacta and related fossils is provided in Tables 1 and S2.Table 1 Morphological comparison of Laiyangia compacta gen. et sp. nov. with closest extinct gnetalean fossils.

Table 1Species	Branch	Leaf shape	Leaf position	Female cone shape	Female cone pedunculate	Bract shape	Bract position	Seed number per cone	Seed number per bract	MT length (cm)	Age	
Laiyangia compacta gen. et sp. nov.	monopodial or dichasially	triangular	opposite, 2/3FS	narrowly elongate	yes	long triangular	5–8 pairs, decussately opposite,	multiple, ≥20	4	0.70–0.86, straight	K1	
Siphonospermum simplex	–	linear	opposite	narrowly ovoid	yes	no	no	1	1	2.5–3.5, straight	K1	
Prognetella minuta	–	–	–	deltoid	yes	linear to lanceolate	2–3 whorls	1–3	1	0.2–1, straight	K1	
Jianchangia verticillata	opposite	linear	verticellate	–	no	linear	>2 whorls, verticillate	2	1, UPF	short	K1	
Liaoxia cheniae	opposite-decussate	linear	opposite	obovate, spicate	no	ovoid to triangular-ovoid	2–6 pairs, decussate	multiple	1	–	K1	
Liaoxia changii	opposite-decussate	–	–	obovate to elongate, spicate	no	ovoid to triangular-ovoid	6–10 pairs, decussate	multiple	1	–	K1	
Liaoxia acutiformis	opposite-decussate	linear	opposite	elongate, spicate	no	ovoid to triangular-ovoid	6–12 pairs, decussate	multiple	1	–	K1	
Liaoxia elongata	opposite	–	–	narrowly elongate, spicate	no	ovoid to triangular-ovoid	8–12 pairs, decussate	multiple	1	–	K1	
Liaoxia robusta	opposite	linear	opposite	rounded to ellipsoid, spicate	no	ovoid to triangular-ovoid	4–10 pairs, decussate	multiple	1	–	K1	
Liaoxia longivractea	opposite	–	–	rounded, spicate	no	ovoid to triangular-ovoid	1–2 pairs, decussate	2–4	1	–	K1	
Chengia laxispicata	opposite	linear	opposite	elongate, spicate	–	ovoid	4–8 pairs, opposite- decussate	multiple	1	0.34–0.75, straight	K1	
Liaoningia decussata	dichasial	linear	opposite	elongate, spicate	no	triangular	5–12 pairs, opposite	multiple	1	–	K1	
Abbreviations: MT = Micropylar tube, 2/3FS = the lower part ca. 2/3 fused into a sheath, UPF = only the uppermost pair/whorl is fertile.

Data from Yang et al. (2013, 2017a, 2020), Rydin et al. (2006), Rydin and Friis (2010), Yang and Ferguson (2015).

Constrobilus ovata Y. Yang et L.B. Lin, Latibractea divisa Liu et al., and Spinobractea lanceolata Liu et al. are reported from the Lower Cretaceous of the Yixian Formation in Liaoning, northeastern China (Liu et al., 2013). Laiyangia compacta differs from all three species in that those three species bear pinnately veined broad leaves and reduced female cones with 2–3 seeds (C. ovata) or 1–2 seeds (S. lanceolata). Siphonospermum Rydin et Friis from the Early Cretaceous of northeastern China bears a loosely organized female shoot with pedunculate ovules and no associated bracts, which is also different from L. compacta (Rydin and Friis, 2010). Daohugoucladus sinensis Yang et al., recently reported from the Middle-Late Jurassic Daohugou bed, Inner Mongolia, bears decurrent, long and linear leaves with a prominent midvein and reduced female cones with one seed, making it significantly different from our new macrofossils (Yang et al., 2023).

Gnetum L. differs from the new genus from Laiyang in possessing broad leaves, female spikes with multiple whorls of seeds, each whorl subtended by a collar of bracts. Welwitschia Hook. f. can be distinguished from Laiyangia compacta by its giant and strap–shaped leaves and female spikes with multiple pairs of fertile bracts, each subtending an axillary seed. Drewria potomacensis Crane et Upchurch (Welwitschiaceae) also differs from our new fossils in these aspects. Protognetum jurassicum Y. Yang et al. from the Middle-Late Jurassic of the Inner Mongolian, northeastern China can also be easily distinguished from L. compacta by the ovulate spikes, linear and leaf–like bracts, two bracts subtending 4–6 whorled seeds and shorter micropylar tube (Yang et al., 2017c).

Gurvanella Krassilov, Beipiaoa Dilcher et al. and some Ephedra macrofossil species from the Early Cretaceous of Liaoning, e.g. Ephedra hongtaoi Wang et Zheng, Ephedra archaeorhytidosperma Yang et al., Ephedra carnosa Yang et Wang and Ephedra multinervia Yang et Lin, have extremely reduced female spikes with only one (uppermost) pair/whorl of fertile bracts, each subtending an axillary and sessile seed, which are markedly different from those in Laiyangia compacta (Wang and Zheng, 2010; Yang et al., 2005, 2013, 2015). Gurvanella bear specially shaped bracts possessing an unusual furcate venation. The female spikes of modern Ephedra are usually ovate, with multiple pairs/whorls bracts, and only the uppermost pair/whorl is fertile, while the lower bracts are sterile, and each modified fertile bract subtends an axillary and sessile seed with a longer and curved micropylar tube. All of these characteristics are obviously different from those of L. compacta.

Similar to Gurvanella and Beipiaoa, the female spikes of Jianchangia Y. Yang, Y.W. Wang & D.K. Ferguson from the Lower Cretaceous Jiufotang Formation of Liaoning, have reduced female spikes with only one (uppermost) pair/whorl of fertile bracts subtending two seeds, but the bracts are linear, ascending and inserted in whorls. In these features Jianchangia are different from Laiyangia compacta (Yang et al., 2020).

Our new species Laiyangia compacta is more similar to Prognetella Krassilov, Chengia Y. Yang & al., Liaoningia Y. Yang & L.B. Lin and Liaoxia Cao & Wu (Ephedraceae) from western Liaoning, China, in having multiple pairs of fertile bracts with axillary, sessile seeds (Rydin et al., 2006; Yang et al., 2013, 2015, 2017a). However, the female spikes of L. compacta are more compact than those of Prognetella, Chengia (loosely arranged), Liaoningia and Liaoxia, with no observable nodes and internodes, and each bract is closer to the axis (Rydin et al., 2006; Yang and Ferguson, 2015; Yang et al., 2013, 2017a). Prognetella possess linear or strap–like bracts, with 2 or 4 parallel veins on the bract, subtending one axillary seed, with a noticeable gap between the two seeds (Yang and Ferguson, 2015). The leaves of Chengia, Liaoningia and Liaoxia are opposite, linear and elongated (longer than in L. compacta), and each bract subtends one ellipsoid seed with shorter micropylar tube (Yang and Ferguson, 2015; Yang et al., 2013, 2017a). All of these characteristics differ from those of our new species L. compacta.

3 Phylogenetic analysis

We conducted a new phylogenetic analysis based on 14 morphological characters for 28 fossil and extant gnetalean species in which morphology was well known, and the characters included branch arrangement, leaf morphology, and reproductive characters. All the morphological characters were coded and recorded in a matrix. The matrix yielded one most parsimonious tree of 36 steps (consistency index [CI] = 0.528, retention index [RI] = 0.785). The detail setting of constrained parsimony analysis is provided in Appendix A.

The phylogenetic results suggested that the most parsimonious position of Laiyangia compacta is within the family Ephedraceae (Fig. 1C). Siphonospermum is clearly distinct from other gnetalean species possessing very primitive female reproductive organs. Gurvanella, Beipiaoa and fossil Ephedra converged to form a secondary clade with modern Ephedra, representing a relatively new reduced female cone form (with the uppermost pair/whorl of bracts are fertile). Jianchangia is also closely related to the Gurvanella–Beipiaoa–Ephedra group. Our new fossil L. compacta is closely related to the Chengia, Liaoningia and Liaoxia changii, all of which possess compact female spikes with multiple pairs of fertile bracts, and possibly represent transitional forms in the evolution of gnetalean plants (Fig. 1C).

4 Evolution of female cones of the gnetophytes

Among the living gnetophytes, the Ephedraceae are more basal group, while the Gnetaceae and Welwitschiaceae are sister (Yang, 2010; Yang et al., 2015). Modern Ephedraceae bear rather reduced female spikes that possess only one apical pair/whorl of fertile bracts and multiple pairs/whorls of sterile bracts (Rydin et al., 2010). Recent palaeobotanical studies generally agree that the reduced female spikes of modern Ephedraceae originated from a spike with multiple pairs/whorls of fertile bracts (Rydin and Korall, 2009; Yang, 2004, 2014; Yang et al., 2013, 2015). Siphonospermum seems to represent the primitive form of modern gnetophytes in the evolutionary process. It has loosely organized female shoots with pedunculate ovules and no associated bracts (Rydin and Friis, 2010; Yang and Ferguson, 2015; Yang et al., 2013, 2017b). In the early ephedroid plants Prognetella, Chengia, Liaoningia, and Liaoxia, with losses of pedicles of the female reproductive units and shortening of the internodes of the cone axis, the female spike became increasingly compact (Rydin et al., 2006; Yang and Ferguson, 2015; Yang et al., 2013, 2017a). During the evolutionary process, these early female spikes, which had multiple pairs of fertile bracts, eventually became modified into the reduced female spikes of modern Ephedraceae via shortening of the internodes and a reduction in the number of fertile bracts in the lower parts (Yang and Ferguson, 2015; Yang et al., 2013).

It has been suggested that the common ancestor of the Gnetaceae and Welwitschiaceae had an ephedroid morphology (Yang et al., 2015). For example, Protognetum has vegetative organs similar to those of Ephedraceae, such as swollen nodes and striated internodes and opposite linear leaves with parallel venation. The female reproductive organs are similar to those of Gnetaceae, such as the lax spikes with verticillate and complicated female reproductive units at the nodes (Yang et al., 2017c). Within the modern gnetophytes, Laiyangia compacta is most similar to Ephedraceae in its vegetative organs, such as the dichasially branched shoot with swollen nodes, and the triangular leaves opposite at nodes and normally fused into a sheath. However, the female reproductive organs of L. compacta were different from those of modern Ephedra, but similar to those of extant Gnetaceae and fossil Liaoningia, Chengia and Liaoxia. The ovulate structure of L. compacta organized into increasingly compact spikes having multiple pairs/whorls of bracts and multiple seeds (vs. only the uppermost pair/whorl is fertile in female spikes of Ephedraceae). Thus, the L. compacta appears intermediate in between the ephedroid and gnetoid in morphology is very likely one of the early transitional forms between ephedroids and gnetoids.

5 Ecology

Modern Ephedra plants generally grow in arid regions, Gobi-type deserts, cliffs, or stony crevices. They are distributed from the Mediterranean region eastwards to Siberia and northern China and in the southwestern United States, northwestern Mexico, and the Andes Mountains in South America (Musaev, 1978). Early Ephedra plants may have occupied a broader range of habitats than they do today, possibly including wetlands or swamps and even aquatic environments (Wang and Zheng, 2010; Yang and Ferguson, 2015; Yang et al., 2020). For instance, the frequent presence of cystiform chlamydosperms in Prognetella may facilitate the dissemination of diaspores in lacustrine environments (Yang and Ferguson, 2015). Jianchangia exhibits a unique morphology of fine linear bracts, different from other fossil species and extant representatives, which may also suggest an ecological adaptation to aquatic environments (Yang et al., 2020). The evolution of plants is closely related to the environment and climate, and their form, structure and function must be able to adapt to the external climate and environmental conditions, which will ultimately be recorded in plant structure. Features of the plant epidermis also vary in similar ways. Anatomical studies of the modern gnetophytes show that stomata are usually absent in the seed envelope. However, in a few species adapted to arid environments, stomata are common but only found in the outer epidermis and in upper parts of the seed envelope, such as in Ephedra alata and Ephedra californica (Rydin et al., 2010). In this study, multiple stomata were clearly observed in the outer epidermis of the seed envelope from Laiyangia compacta under a fluorescence microscope.

Moreover, the sedimentary characteristics of the Laiyang Formation clearly represent a fluvial-lacustrine depositional environment in the Laiyang Basin (Luo et al., 1990). A rich gymnospermous flora is found in the present locality, which included genera of Pararaucaria, Elatides, Podozamites, Cupressinocladus, Pagiophyllum, Brachyphyllum and Pseudofrenelopsis, many of which belong to Cheirolepidiaceae, such as the species of the genera Pseudofrenelopsis, Pagiophyllum, Brachyphyllum and Pararaucaria, which indicate relatively arid and water-stressed environments (Jin, 2018). Therefore, we infer that the palaeoclimate of the Laiyang area in the Early Cretaceous may have been drier than previously imagined.

In this study, we describe Laiyangia compacta P.H. Jin as a new ephedroid species from the Lower Cretaceous of eastern Shandong in China. This new genus shows transitional morphology between early Ephedraceae and modern Gnetaceae, and potentially signifying an important clade within the ancestor of the Gnetaceae. It may provide clues regarding the relationships of gnetophyte plants with other seed plants. Furthermore, a driver palaeoclimate of the Laiyang area in the Early Cretaceous is inferred based on the appearance of L. compacta.

CRediT authorship contribution statement

Peihong Jin: Writing – original draft, Conceptualization. Mingzhen Zhang: Writing – original draft, Resources, Funding acquisition. Baoxia Du: Writing – review & editing, Investigation. Jing Zhang: Visualization, Software, Data curation. Bainian Sun: Writing – review & editing.

Declaration of competing interest

There is no conflict of interest.

Appendix A Supplementary data

The following is/are the supplementary data to this article:Multimedia component 1

Multimedia component 1

Acknowledgments

We are very grateful to Yong Yang (College of Biology and the Environment, Nanjing Forestry University) for his many useful suggestions. We would also like to acknowledge the editor and the anonymous reviewers for their useful comments that significantly improved the manuscript. This study was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (STEP) (Grant No. 2019QZKK0704 ), the National Natural Science Foundation of China (Grant No. 42272029 ).

Peer review under responsibility of Editorial Office of Plant Diversity.

Appendix A Supplementary data to this article can be found online at https://doi.org/10.1016/j.pld.2024.03.002.
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References

Endress P.K. Structures and function of female and bisexual organ complexes in Gnetales Int. J. Plant Sci. 157 1996 S113 S125
Friis E.M. Pedersen K.R. Crane P.R. Early cretaceous mesofossils from Portugal and eastern North America related to the Bennettitales–Erdtmanithecales–Gnetales group Am. J. Bot. 96 2009 252 283 21628188
Jin P.H. Early Cretaceous Plant Fossils from the Laiyang Basin of Shandong and Their Paleoecological Characteristics 2018 Lanzhou University Lanzhou, thesis 109 127 (in Chinese with English Abstract)
Liu H.F. David K. Wang Y. New plants of Gnetales from early cretaceous of China, and its bearing on the early evolution of Ephedraceae and Welwitschiaceae in Gnetales Chin. Sci. Bull. 58 2013 200 209
Luo S.L. Liu M.W. Sha Y.X. The Stratigraphy and Palaeontology of Laiyang Basin, Shandong Province 1990 Geological Publishing House Beijing
Mendes M.M. Pais J. Friis E.M. Raunsgaardispermum lusitanicum gen. et sp. nov., a new seed with in situ pollen from the Early Cretaceous (probably Berriasian) of Portugal: further support for the Bennettitales-Erdtmanithecales-Gnetales link Grana 47 2008 211 219
Mendes M.M. Pais J. Pedersen K.R. Erdtmanitheca portucalensis, a new pollen organ from the Early Cretaceous (Aptian–Albian) of Portugal with Eucommiidites–type pollen Grana 49 2010 26 36
Musaev I.F. On geography and phylogeny of some representatives of the genus Ephedra L Bot. Zh. (St. Petersbg.). 63 1978 523 543
Price R.A. Systematics of the Gnetales: a review of morphological and molecular evidence Int. J. Plant Sci. 157 1996 S40 S49
Ran J.H. Shen T.T. Wang M.M. Phylogenomics resolves the deep phylogeny of seed plants and indicates partial convergent or homoplastic evolution between Gnetales and angiosperms Proc. R. Soc. B-Biol. Sci. 285 2018 20181012
Rydin C. Friis E.M. A new Early Cretaceous relative of Gnetales: Siphonospermum simplex gen. et sp. nov. from the Yixian Formation of Northeast China BMC Evol. Biol. 10 2010 1 6 20044934
Rydin C. Khodabandeh A. Endress P.K. The female reproductive unit of Ephedra (Gnetales): comparative morphology and evolutionary perspectives Bot. J. Linn. Soc. 163 2010 387 430 20799438
Rydin C. Korall P. Evolutionary relationships in Ephedra (Gnetales), with implications for seed plant phylogeny Int. J. Plant Sci. 170 2009 1031 1043
Rydin C. Wu S. Friis E. Liaoxia Cao et SQ Wu (Gnetales): ephedroids from the Early Cretaceous Yixian Formation in Liaoning, northeastern China Plant Syst. Evol. 262 2006 239 265
Wang X. Zheng S. Whole fossil plants of Ephedra and their implications on the morphology, ecology and evolution of Ephedraceae (Gnetales) Chin. Sci. Bull. 55 2010 1511 1519
Wang Z.Q. A new Permian gnetalean cone as fossil evidence for supporting current molecular phylogeny Ann. Bot. 94 2004 281 288 15229124
Wu X. He Y.L. Mei S.W. Discovery of Ephedrites from the lower jurassic Xiaomeigou formation, Qinghai Acta Palaeobot. Palynol. Sin. 1 1986 13 21
Yang Y. Ontogeny of triovulate cones of Ephedra intermedia and origin of the outer envelope of ovules of Ephedraceae Am. J. Bot. 91 2004 1 8 21653357
Yang Y. A systematic classification of Ephedraceae: living and fossil Phytotaxa 158 2014 83 90
Yang Y. A review on gnetalean megafossils: problems and perspectives Taiwania 55 2010 46 54
Yang Y. Ferguson D.K. Macrofossil evidence unveiling evolution and ecology of early Ephedraceae Perspect. Plant Ecol. Evol. Syst. 17 2015 31 46
Yang Y. Geng B.Y. Dilcher D.L. Morphology and affinities of an early cretaceous Ephedra (Ephedraceae) from China Am. J. Bot. 92 2005 31 41
Yang Y. Lin L. Ferguson D.K. Parallel evolution of leaf morphology in gnetophytes Org. Divers. Evol. 15 2015 51 62
Yang Y. Lin L. Wang Q. Chengia laxispicata gen. et sp. nov., a new ephedroid plant from the Early Cretaceous Yixian Formation of western Liaoning, Northeast China: evolutionary, taxonomic, and biogeographic implications BMC Evol. Biol. 13 2013 1 13 23279962
Yang Y. Lin L.B. Ferguson D.K. A new gnetalean macrofossil from the Early Cretaceous and its evolutionary significance Cretac. Res. 74 2017 56 64
Yang Y. Wang Y. Ferguson D.K. A new macrofossil ephedroid plant with unusual bract morphology from the Lower Cretaceous Jiufotang Formation of northeastern China BMC Evol. Biol. 20 2020 1 12 31906845
Yang Y. Wang Z. Xu X. Taxonomy and Distribution of Global Gymnosperms 2017 China Scientific Books
Yang Y. Xie L. Ferguson D.K. Protognetaceae: a new gnetoid macrofossil family from the Jurassic of northeastern China Perspect. Plant Ecol. Evol. Systemat. 28 2017 67 77
Yang Y. Yang Z. Lin L. A new gnetalean macrofossil from the Mid-Jurassic Daohugou formation Plants 12 2023 1749 37176807
