BACKGROUND
the extant gnetales, which are often classified into three monotypic families, namely, ephedraceae dumort., gnetaceae lindl., and welwitschiaceae markgr., have attracted extensive attention because of their enormous potential for understanding the origin of angiosperms and the phylogenetic relationships of seed plants due to the bisexual reproductive units that occasionally occur in ephedra l.  <cit> , vessels and broad leaves with reticulate venation present in gnetum l.  <cit> , ovules with multiple envelopes  <cit> , and double fertilization  <cit> .
this order now includes three relict genera ephedra, gnetum, and welwitschia hook.
f., with a mutually exclusive geographic distribution  <cit> .
each of three genera possesses compound female cones that comprise a main axis and  <dig> to multiple pairs of opposite and decussate bracts or  <dig> to multiple whorls of ternately arranged bracts which usually subtend a female reproductive unit .
to date, there are primarily two competing hypotheses on the early evolution and phylogeny of the gnetales  <cit>  .
one hypothesis places the gnetales into an anthophyte clade  <cit>  using morphological data, which implies that the compound female cones of the gnetales might be closely related to either flowers of angiosperms or fertile organs of bennettitales, erdtmanithecales, and other anthophytes  <cit>  .
the other hypothesis nests the gnetales within or closely related to conifers using molecular data, forming either gnepines or gnetifers or gnecups  <cit>  , which infers that the compound female cones of the gnetales and coniferophytes may be homologous.
therefore, the evolutionary origin and phylogenetic relationships of the gnetales within seed plants remain controversial, and macrofossils especially regarding compound female cones should be important to decipher the early evolution of the order and their relationship with other seed plants.
the extant ephedraceae  usually occupy a basal position in phylogenetic trees of the gnetales  while gnetum and welwitschia are more derived and are more closely related to each other than either is to ephedra <cit> .
ephedra has scale-like, linear and  <dig>  parallel-veined leaves which are often opposite and decussate at nodes and connate at the base into a sheath , and ternate phyllotaxis is also not rare   <cit>  .
in contrast, welwitschia bears two opposite, enormous strap-like leaves with numerous parallel primary veins   <cit>  , while gnetum possesses petiolate, broad-laminar and reticulate-veined leaves that are arranged in opposite and decussate manner in most cases  <cit>  , and ternate phyllotaxis is also present .
bracts and reproductive units of female cones of ephedra and welwitschia are opposite and decussate in most cases while those of gnetum are usually whorled at nodes with the fusion of bracts into cupules and occasionally they are spirally arranged  <cit> .
both gnetum and welwitschia bear female cones with many whorls of fertile bracts while living ephedra normally has only the uppermost whorl/pair of bracts fertile  <cit> , rarely the inferior bracts subtending female reproductive units  <cit> , or hermaphroditic cones with the lower whorls of bracts bearing male reproductive units but the uppermost whorl possessing female reproductive units  <cit> .
in addition, ovules of the gnetales have 1— <dig> outer envelopes and the inner integument upwardly extended into a characteristic micropylar tube.
therefore, well-preserved female reproductive organs of the gnetales may be easily recognized in the fossil record, and macrofossils of the basal family ephedraceae are especially important in understanding the origin and phylogenetic relationships of the extant gnetales.
so far, a variety of pre-cretaceous macrofossils have been attributed to or compared with extant gnetales , but their putative relationships to the gnetales are not unequivocal due to lacking of synapomorphies recognized from the clade  and other detail  as crane  <cit>  previously suggested.
hence, the extant genera ephedra, gnetum, and welwitschia, together with two cretaceous genera drewria crane et upchurch  <cit>  and eoantha krassilov  <cit> , were considered to form a crown group of the gnetales  <cit>  while those pre-cretaceous genera were assigned to either stem-gnetaleans  <cit>  or seed plants with uncertain affinities  <cit> .
recently, a wealth of additional early cretaceous macrofossils and mesofossils assignable to the crown-gnetaleans have been widely described from south europe, northeast china, mongolia, north america, south america, and australia  <cit> , suggesting that three families ephedraceae, gnetaceae, and welwitschiaceae of the extant gnetales existed and diversified during at least the early cretaceous.
of all, macrofossils closely related to welwitschia and gnetum are very rare  <cit> , but macrofossils and mesofossils  assignable to ephedraceae or even to the extant ephedra have been extensively reported  <cit> .
these members of the ephedraceae show a very high morphological diversity in both reproductive and vegetative organs across the world except for africa and antarctica.
according to characteristics of female reproductive organs, cretaceous ephedroid macrofossils can be classified into three groups, namely:  those with female cones bearing  <dig> pairs of bracts with only the uppermost pair fertile, e.g., ephedra carnosa yang et wang  <cit> , e. archaerhytidosperma yang et al.
<cit> , e. hongtaoi wang et zheng  <cit>  and e. verticillata cladera et al.
<cit>  as well as alloephedra xingxuei tao et yang  <cit>  and two species of gurvanella krassilov  <dig>  <cit>  ;  those with female cones possessing multiple whorls of fertile bracts each subtending a female reproductive unit, e.g., numerous species of liaoxia cao et wu  <dig>  <cit>  ; and  those that have ovules surrounded by envelopes lacking supporting bracts and directly attached on the peduncles, e.g., siphonospermum simplex rydin et friis  <cit> .
therefore, the basal gnetalean family ephedraceae, including the extant genus ephedra, was demonstrated to have considerable diversity by the early cretaceous.
in this paper, we study a new ephedroid macrofossil from the early cretaceous yixian formation of western liaoning province, northeast china, and name it chengia laxispicata gen. et sp.
nov.. our new plant bears a comparatively complete, leafy shooting system with loose female spikes that allow us to discuss the evolution of female cones of the ephedraceae.
we also consider the taxonomic and biogeographic implications of our findings on the basis of abundant ephedroid macrofossils from the early cretaceous jehol biota of northeast china and adjacent areas.
RESULTS
description of the specimens
the macrofossils presented here based on information from the part and counterpart of a single well-preserved and articulated specimen  that represents part of a leafy shooting system with reproductive organs attached .
the shooting system represents the distal part of the plant and is preserved at least  <dig>  cm long, and the shoot is ca.
<dig> — <dig>   mm wide.
the main shoot is slightly curved, with nodes and internodes.
nodes are swollen, from which the lateral branches arise oppositely .
internodes are 2— <dig>  cm long or more, taper toward the distal region and have numerous fine, longitudinal striations, in which ridges and furrows are discernible .
the main shoot branches at least  <dig> times.
lateral branches are stretched upwards at 15—70° and do not ramify or dichasially ramify once to twice.
leaves, which subtend lateral branches, are linear, about  <dig>  cm long, but the venation is indiscernible .
foliar structures at the base of spikes are specialized into involucres which are linear, about  <dig>  mm long, approximately perpendicular to the shoot at the proximal part and slightly curved inward at the distal part .
spikes are terminal to twigs or are axillary to leaves, 1— <dig>  cm long and 2— <dig> mm wide, and mature acropetally .
spikes are loosely arranged at the distal end of the main shoot, but more compact on the basal lateral branches .
those loosely arranged spikes are noticeable in having prominent nodes and internodes .
nodes are swollen, and each node gives rise to two opposite and spreading bracts.
internodes are approximately 1— <dig> mm long, acropetally becoming successively shorter and shorter .
bracts of spikes are decussately opposite and comprise 4— <dig> pairs that are linear in lateral view .
each bract subtends an ellipsoid seed, about  <dig> — <dig>  mm long and  <dig> — <dig>  mm wide.
seeds are sessile, with a thin outer envelope and a distal, hollow micropylar tube, about  <dig> — <dig>  mm long .
spikes of this plant are all female, which are oriented toward one side of the shooting system and appear to have been flexible rather than rigid.
a reconstruction of this plant is given here .
discussion
identity and affinity
the fossil specimens studied here obviously possess opposite organographic features, including opposite lateral branches, leaves as well as decussately opposite bracts and enveloped seeds, all of which conform to the diagnostic and synapomorphic features of the gnetales  <cit> .
hence this plant can be readily classified into the gnetales, and its linear leaves and decussately opposite bracts that comprise female spikes resemble those of the ephedroids.
however, the decussately opposite bracts and loose female spikes with clear nodes and internodes are noticeably different from all known ephedroid fossils  <cit>  and extant ephedra that bears female cones usually having 2— <dig> pairs/whorls of cone bracts but with only the uppermost pairs/whorls of bracts being fertile  <cit> .
therefore, the fossils presented here do not conform to the generic circumscription of ephedra and require a new name for which we institute chengia laxispicata gen. et sp.
nov. and place it within the ephedroid gnetales .
the evolution of female cones in ephedraceae
previous morphological, anatomical, ontogenetic, and molecular studies supported a reduction hypothesis that female cones of the extant ephedraceae may have stemmed from a loosely arranged, multi-axial, reproductive organs homologous to the late palaeozoic cordaitales and permian—triassic coniferophytes  <cit> , <cit> .
with shortening of internodes of the reproductive multi-axial shoot system, both the primary and secondary shoots of ephedraceae, to some extent, may have experienced a series of structural reductions and finally given rise to compact female cones in extant ephedra <cit> .
hence, female cones similar to laxly arranged reproductive shooting systems would represent more primitive organizations than those resembling to compact reduced female cones of the extant ephedraceae.
our new fossil chengia laxispicata gen. et sp.
nov. bearing loose female spikes appears to be a missing link to the extant ephedraceae with compact cones.
early cretaceous macrofossils have provided diverse characteristics of female reproductive structures.
ovulate cones of ephedra carnosa <cit> , e. archaeorhytidosperma <cit> , e. hongtaoi <cit> , gurvanella dictyoptera krassilov and g. exquisita sun et al.
<cit>  from the early cretaceous jehol biota of northeast china and adjacent areas bear either  <dig> pairs or  <dig> whorl of bracts enclosing 1— <dig> seeds, effectively demonstrating the same pattern as modern ephedra that possesses only the uppermost one pair/whorl of fertile bracts.
siphonospermum simplex has linear leaves, opposite phyllotaxis, and ovules with exposed micropylar tubes and surrounded by envelopes, which are attached directly on the peduncles, so these ephedroid features may be plesiomorphic in the gnetales  <cit> .
female spikes of liaoxia have multiple whorls of fertile bracts each subtending a female reproductive unit  , which provide palaeobotanical evidence for the previous morphological—evolutionary interpretation that the archetypal female cone of ephedraceae may be compound, with multiple-whorled fertile bracts.
our new ephedroid fossil-genus chengia markedly differs from both extant and fossil species of ephedra by the female cone bearing multiple  pairs of fertile bracts.
it is different from siphonospermum by the female reproductive unit possessing subtending bracts.
chengia also differs from liaoxia in having loosely arranged female cones.
the female spikes of chengia have evident nodes and internodes showing similarity to the supposed laxly arranged reproductive shoot system of ancient ancestors, so such female cones in ephedraceae are more primitive than those of liaoxia and other ephedroid fossils .
chengia together with other macrofossils from the early cretaceous yixian formation of northeast china give instrumental clues to the morphological transformation of cone bracts in ephedraceae.
according to current phylogenetic trees of the gnetales  <cit>  , the ancestral form of the order is far more likely to bear compound female cones regardless of the anthophyte hypothesis or gnetifer hypothesis.
here, we propose a reduction and sterilization hypothesis that the female cone of ephedra is derived from that of siphonospermum, chengia, and liaoxia by a series of changes that include reduction and sterilization of lower fertile bracts, shortenings of internodes and peduncles, loss of reproductive units in all inferior bracts, and retains only the uppermost pair/whorl of bracts fertile .
CONCLUSIONS
this ephedroid plant chengia laxispicata gen. et sp.
nov. described from the early cretaceous yixian formation of northeast china provides a missing link between archetypal fertile organs of the crown lineage of the gnetales and compound female cones of the extant ephedraceae.
based upon a plethora of ephedra and ephedroid macrofossils from the early cretaceous, we propose a reduction and sterilization hypothesis that the female cone of the extant ephedraceae may have stemmed from archetypal fertile organs of the crown lineage of the gnetales, which have undergone sequentially intermediate links similar to female cones of cretaceous siphonospermum, chengia, and liaoxia by a series of transformations that include reduction and sterilization of the lower fertile bracts, shortenings of internodes and peduncles, loss of reproductive units in all inferior bracts.
the basal family ephedraceae including ephedra of the extant gnetales was demonstrated to have considerable diversity by the early cretaceous, so an emended familial diagnosis is given here.
the jehol biota in northeast china and adjacent areas contains a plethora of well-preserved macrofossils of ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of ephedraceae, so northeast china and adjacent areas may represent either the centre of origination for the family or its centre of early diversification.
systematics
gnetales luerss.
1879
ephedraceae dumort.
<dig>  emend.
type:ephedra l.  <dig>  sp.
pl.
<dig>
familial diagnosis emended
dioecious  shrubs, sub-shrubs, small tree, climbers, or sometimes perennial herbs.
shoots are profusely and dichasially branched and have many nodes; nodes are usually swollen, sometimes branches are whorled at nodes due to extremely reduction of internodes or alternate on account of suppression of the opposite branch; internodes of twigs possess many fine striations.
leaves are opposite and decussate or ternately whorled at nodes, linear and free to basally connate into a sheath but apices acute and triangular.
leaves are parallel veined, with  <dig>  veins.
reproductive organs are usually unisexual but hermaphroditic cones occasionally occur.
male cones are terminal to twigs, or pedunculate, or sessile and axillary to leaves, or clustered at nodes, bear multiple pairs/whorls of bracts each of which enclose an axillary male reproductive unit.
the male reproductive unit is a shortened shoot and usually consists of a pair of bracteoles enclosing  <dig> microsporangiophore.
the microsporangiophore is fused or distally furcated, and terminated by 2— <dig> synangia.
the synangium is sessile to pedicellate, consists of 2— <dig> microsporangia, the latter opening by horizontal slits.
at maturity, the microsporangiophore is elongated outside the bracteoles and terminated by a few free or fused synangia which produce polyplicate pollen bearing longitudinal ridges and furrows.
the female reproductive units  or compound female cones are directly terminal to twigs, or pedunculate or sub-sessile or sessile at nodes.
the compound female cones if present are trimerous or bimerous, bear  <dig> to multiple whorls/pairs of leaf-like or specialized bracts, each subtending a female reproductive unit, or only the uppermost whorl/pair of bracts being fertile and the inferior whorls/pairs of bracts becoming sterile.
cone bracts are sometimes modified into dry and membranous, or dry and coriaceous, or fleshy and colourful.
seeds bear an outer envelope and an inner integument which usually extends upward and passes through the opening of the outer envelope, forming a thin and hollow micropylar tube.
micropylar tubes varying in length and shape,  <dig> — <dig> mm long, straight, curved or coiled.
remarks
in  <dig>  the family ephedraceae was instituted by the belgian botanist barthélemy-charles dumortier   <cit> , who only gave a brief familial diagnosis “ovaire supère stylifère; écailles opposes; ovaire monogyne”.
in modern plant taxonomy, the ephedraceae are usually characterized by features of the sole extant ephedra <cit> .
however, abundant ephedroid fossil plants from the early cretaceous have increasingly broadened our understanding of the circumscription and character variation of the family, so an emended familial diagnosis is provided here.
the key diagnoses  of ephedraceae include enveloped ovules with extruded micropylar tubes , linear leaves opposite and decussate or ternately whorled and having 2— <dig> parallel veins.
in light of the present study, ephedraceae sensu lato contain ephedra l. with ca.
<dig> living species,  <dig> macrofossil-species , and  <dig> seed fossil-species  as well as ephedroid macrofossils alloephedra tao et yang  <cit> , gurvanella krassilov  <cit> , liaoxia cao et wu  <cit> , siphonospermum rydin et friis  <cit> , leongathia krassilov et al.
<cit> , amphiephedra miki  <cit> , and chengia gen. nov. presented herein, indicating higher generic diversity through time.
early cretaceous strata of northeast china contain a plethora of well-preserved macrofossils  of ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of ephedraceae, and in this respect northeast china and adjacent areas that yield the famous jehol biota  <cit>  might represent either the centre of origination or one of centres for early diversification of the family.
chengia laxispicata y.yang, l.b.lin et q.wang gen. et sp.
nov. .
etymology
the generic name “chengia” is dedicated to the late eminent botanist cheng wan-chun   who has made enormous contributions to the taxonomy of gymnosperms; the specific epithet “laxispicata”, stemming from the latin “laxus” + “spicatus”, refers to the loosely arranged female spike which is a conspicuous feature of this fossil-species.
generic and specific diagnosis
reproductive shoots branch oppositely at swollen nodes.
internodes bear numerous longitudinal striations.
leaves that subtend lateral branches are long and linear.
female spikes are terminal to twigs or are subtended by the leaf, possessing multiple pairs of loosely arranged female reproductive units.
nodes and internodes of female spikes prominent.
female reproductive units consist of decussately opposite seeds and subtending bracts.
seeds enveloped, with distal micropylar tube.
description: .
holotype
pe 2012041619a, b  .
type locality
dawangzhangzi village, songzhangzi town, lingyuan city, chaoyang district, liaoning province, china .
stratigraphic horizon and age
dawangzhangzi bed in the middle part of the yixian formation or xinfangzi bed in the lower part of the yixian formation  .
repository
chinese national herbarium , institute of botany, chinese academy of sciences, beijing, china.
remarks
the plant-bearing beds at dawangzhangzi village , lingyuan city, chaoyang district, liaoning province, northeast china have been known since the 1930s.
fossil fish lycoptera jeholensis grabau, monocotyledonous plants potamogeton jeholensis yabe et endô, potamogeton ?
sp., gymnosperms schizolepis jeholensis yabe et endô and czekanowskia rigida heer were first reported from this early cretaceous locality  <cit> .
subsequently, potamogeton jeholensis was reclassified as another angiosperm ranunculus jeholensis  miki  <cit>  or an ephedroid plant ephedrites chenii  guo et x.w.
wu  <cit>  , which is synonymous with liaoxia cheniae  cao et s. q. wu  <cit> .
moreover, miki  <cit>  described a new ephedroid plant amphiephedra rhamnoides miki from this locality, which is different from our new plant chengia laxispicata gen. et sp.
nov. in bearing “verticillate, scaly leaves on the lateral branches that look more like short shoots” .
adjacent to dawangzhangzi village of lingyuan city, an ephedroid plant ephedrites?
elegans sun et zheng  <cit>  was described from the jianshangou bed in the lower part of the yixian formation of huangbanjigou village , beipiao city, chaoyang district, liaoning province, northeast china.
ephedrites?
elegans  also bears loosely arranged spikes with clear nodes and internodes, but it differs from our new plant chengia laxispicata gen. et sp.
nov. in having possibly 3— <dig> bracts per whorl in spikes   <cit> .
another superficially similar specimen was also reported from the early cretaceous lycoptera beds of manlaj, eastern gobi in mongolia, which krassilov called “potamogeton-like spike” bearing  <dig> or  <dig> nutlets per node   <cit> .

 the extant gnetales, which are often classified into three monotypic families, namely, ephedraceae dumort., gnetaceae lindl., and welwitschiaceae markgr., have attracted extensive attention because of their enormous potential for understanding the origin of angiosperms and the phylogenetic relationships of seed plants due to the bisexual reproductive units that occasionally occur in ephedra l., vessels and broad leaves with reticulate venation present in gnetum l., ovules with multiple envelopes, and double fertilization. this order now includes three relict genera ephedra, gnetum, and welwitschia hook. f., with a mutually exclusive geographic distribution. each of three genera possesses compound female cones that comprise a main axis and to multiple pairs of opposite and decussate bracts or to multiple whorls of ternately arranged bracts which usually subtend a female reproductive unit. to date, there are primarily two competing hypotheses on the early evolution and phylogeny of the gnetales. one hypothesis places the gnetales into an anthophyte clade using morphological data, which implies that the compound female cones of the gnetales might be closely related to either flowers of angiosperms or fertile organs of bennettitales, erdtmanithecales, and other anthophytes. the other hypothesis nests the gnetales within or closely related to conifers using molecular data, forming either gnepines or gnetifers or gnecups, which infers that the compound female cones of the gnetales and coniferophytes may be homologous. therefore, the evolutionary origin and phylogenetic relationships of the gnetales within seed plants remain controversial, and macrofossils especially regarding compound female cones should be important to decipher the early evolution of the order and their relationship with other seed plants. the extant ephedraceae usually occupy a basal position in phylogenetic trees of the gnetales while gnetum and welwitschia are more derived and are more closely related to each other than either is to ephedra. ephedra has scale-like, linear and parallel-veined leaves which are often opposite and decussate at nodes and connate at the base into a sheath, and ternate phyllotaxis is also not rare. in contrast, welwitschia bears two opposite, enormous strap-like leaves with numerous parallel primary veins, while gnetum possesses petiolate, broad-laminar and reticulate-veined leaves that are arranged in opposite and decussate manner in most cases, and ternate phyllotaxis is also present. bracts and reproductive units of female cones of ephedra and welwitschia are opposite and decussate in most cases while those of gnetum are usually whorled at nodes with the fusion of bracts into cupules and occasionally they are spirally arranged. both gnetum and welwitschia bear female cones with many whorls of fertile bracts while living ephedra normally has only the uppermost whorl/pair of bracts fertile, rarely the inferior bracts subtending female reproductive units, or hermaphroditic cones with the lower whorls of bracts bearing male reproductive units but the uppermost whorl possessing female reproductive units. in addition, ovules of the gnetales have 1— outer envelopes and the inner integument upwardly extended into a characteristic micropylar tube. therefore, well-preserved female reproductive organs of the gnetales may be easily recognized in the fossil record, and macrofossils of the basal family ephedraceae are especially important in understanding the origin and phylogenetic relationships of the extant gnetales. so far, a variety of pre-cretaceous macrofossils have been attributed to or compared with extant gnetales, but their putative relationships to the gnetales are not unequivocal due to lacking of synapomorphies recognized from the clade and other detail as crane previously suggested. hence, the extant genera ephedra, gnetum, and welwitschia, together with two cretaceous genera drewria crane et upchurch and eoantha krassilov, were considered to form a crown group of the gnetales while those pre-cretaceous genera were assigned to either stem-gnetaleans or seed plants with uncertain affinities. recently, a wealth of additional early cretaceous macrofossils and mesofossils assignable to the crown-gnetaleans have been widely described from south europe, northeast china, mongolia, north america, south america, and australia, suggesting that three families ephedraceae, gnetaceae, and welwitschiaceae of the extant gnetales existed and diversified during at least the early cretaceous. of all, macrofossils closely related to welwitschia and gnetum are very rare, but macrofossils and mesofossils assignable to ephedraceae or even to the extant ephedra have been extensively reported. these members of the ephedraceae show a very high morphological diversity in both reproductive and vegetative organs across the world except for africa and antarctica. according to characteristics of female reproductive organs, cretaceous ephedroid macrofossils can be classified into three groups, namely: those with female cones bearing pairs of bracts with only the uppermost pair fertile, e.g., ephedra carnosa yang et wang, e. archaerhytidosperma yang et al., e. hongtaoi wang et zheng and e. verticillata cladera et al. as well as alloephedra xingxuei tao et yang and two species of gurvanella krassilov; those with female cones possessing multiple whorls of fertile bracts each subtending a female reproductive unit, e.g., numerous species of liaoxia cao et wu; and those that have ovules surrounded by envelopes lacking supporting bracts and directly attached on the peduncles, e.g., siphonospermum simplex rydin et friis. therefore, the basal gnetalean family ephedraceae, including the extant genus ephedra, was demonstrated to have considerable diversity by the early cretaceous. in this paper, we study a new ephedroid macrofossil from the early cretaceous yixian formation of western liaoning province, northeast china, and name it chengia laxispicata gen. et sp. nov.. our new plant bears a comparatively complete, leafy shooting system with loose female spikes that allow us to discuss the evolution of female cones of the ephedraceae. we also consider the taxonomic and biogeographic implications of our findings on the basis of abundant ephedroid macrofossils from the early cretaceous jehol biota of northeast china and adjacent areas.  description of the specimens the macrofossils presented here based on information from the part and counterpart of a single well-preserved and articulated specimen that represents part of a leafy shooting system with reproductive organs attached. the shooting system represents the distal part of the plant and is preserved at least cm long, and the shoot is ca. — mm wide. the main shoot is slightly curved, with nodes and internodes. nodes are swollen, from which the lateral branches arise oppositely. internodes are 2— cm long or more, taper toward the distal region and have numerous fine, longitudinal striations, in which ridges and furrows are discernible. the main shoot branches at least times. lateral branches are stretched upwards at 15—70° and do not ramify or dichasially ramify once to twice. leaves, which subtend lateral branches, are linear, about cm long, but the venation is indiscernible. foliar structures at the base of spikes are specialized into involucres which are linear, about mm long, approximately perpendicular to the shoot at the proximal part and slightly curved inward at the distal part. spikes are terminal to twigs or are axillary to leaves, 1— cm long and 2— mm wide, and mature acropetally. spikes are loosely arranged at the distal end of the main shoot, but more compact on the basal lateral branches. those loosely arranged spikes are noticeable in having prominent nodes and internodes. nodes are swollen, and each node gives rise to two opposite and spreading bracts. internodes are approximately 1— mm long, acropetally becoming successively shorter and shorter. bracts of spikes are decussately opposite and comprise 4— pairs that are linear in lateral view. each bract subtends an ellipsoid seed, about — mm long and — mm wide. seeds are sessile, with a thin outer envelope and a distal, hollow micropylar tube, about — mm long. spikes of this plant are all female, which are oriented toward one side of the shooting system and appear to have been flexible rather than rigid. a reconstruction of this plant is given here. discussion identity and affinity the fossil specimens studied here obviously possess opposite organographic features, including opposite lateral branches, leaves as well as decussately opposite bracts and enveloped seeds, all of which conform to the diagnostic and synapomorphic features of the gnetales. hence this plant can be readily classified into the gnetales, and its linear leaves and decussately opposite bracts that comprise female spikes resemble those of the ephedroids. however, the decussately opposite bracts and loose female spikes with clear nodes and internodes are noticeably different from all known ephedroid fossils and extant ephedra that bears female cones usually having 2— pairs/whorls of cone bracts but with only the uppermost pairs/whorls of bracts being fertile. therefore, the fossils presented here do not conform to the generic circumscription of ephedra and require a new name for which we institute chengia laxispicata gen. et sp. nov. and place it within the ephedroid gnetales. the evolution of female cones in ephedraceae previous morphological, anatomical, ontogenetic, and molecular studies supported a reduction hypothesis that female cones of the extant ephedraceae may have stemmed from a loosely arranged, multi-axial, reproductive organs homologous to the late palaeozoic cordaitales and permian—triassic coniferophytes,. with shortening of internodes of the reproductive multi-axial shoot system, both the primary and secondary shoots of ephedraceae, to some extent, may have experienced a series of structural reductions and finally given rise to compact female cones in extant ephedra. hence, female cones similar to laxly arranged reproductive shooting systems would represent more primitive organizations than those resembling to compact reduced female cones of the extant ephedraceae. our new fossil chengia laxispicata gen. et sp. nov. bearing loose female spikes appears to be a missing link to the extant ephedraceae with compact cones. early cretaceous macrofossils have provided diverse characteristics of female reproductive structures. ovulate cones of ephedra carnosa, e. archaeorhytidosperma, e. hongtaoi, gurvanella dictyoptera krassilov and g. exquisita sun et al. from the early cretaceous jehol biota of northeast china and adjacent areas bear either pairs or whorl of bracts enclosing 1— seeds, effectively demonstrating the same pattern as modern ephedra that possesses only the uppermost one pair/whorl of fertile bracts. siphonospermum simplex has linear leaves, opposite phyllotaxis, and ovules with exposed micropylar tubes and surrounded by envelopes, which are attached directly on the peduncles, so these ephedroid features may be plesiomorphic in the gnetales. female spikes of liaoxia have multiple whorls of fertile bracts each subtending a female reproductive unit, which provide palaeobotanical evidence for the previous morphological—evolutionary interpretation that the archetypal female cone of ephedraceae may be compound, with multiple-whorled fertile bracts. our new ephedroid fossil-genus chengia markedly differs from both extant and fossil species of ephedra by the female cone bearing multiple pairs of fertile bracts. it is different from siphonospermum by the female reproductive unit possessing subtending bracts. chengia also differs from liaoxia in having loosely arranged female cones. the female spikes of chengia have evident nodes and internodes showing similarity to the supposed laxly arranged reproductive shoot system of ancient ancestors, so such female cones in ephedraceae are more primitive than those of liaoxia and other ephedroid fossils. chengia together with other macrofossils from the early cretaceous yixian formation of northeast china give instrumental clues to the morphological transformation of cone bracts in ephedraceae. according to current phylogenetic trees of the gnetales, the ancestral form of the order is far more likely to bear compound female cones regardless of the anthophyte hypothesis or gnetifer hypothesis. here, we propose a reduction and sterilization hypothesis that the female cone of ephedra is derived from that of siphonospermum, chengia, and liaoxia by a series of changes that include reduction and sterilization of lower fertile bracts, shortenings of internodes and peduncles, loss of reproductive units in all inferior bracts, and retains only the uppermost pair/whorl of bracts fertile.  this ephedroid plant chengia laxispicata gen. et sp. nov. described from the early cretaceous yixian formation of northeast china provides a missing link between archetypal fertile organs of the crown lineage of the gnetales and compound female cones of the extant ephedraceae. based upon a plethora of ephedra and ephedroid macrofossils from the early cretaceous, we propose a reduction and sterilization hypothesis that the female cone of the extant ephedraceae may have stemmed from archetypal fertile organs of the crown lineage of the gnetales, which have undergone sequentially intermediate links similar to female cones of cretaceous siphonospermum, chengia, and liaoxia by a series of transformations that include reduction and sterilization of the lower fertile bracts, shortenings of internodes and peduncles, loss of reproductive units in all inferior bracts. the basal family ephedraceae including ephedra of the extant gnetales was demonstrated to have considerable diversity by the early cretaceous, so an emended familial diagnosis is given here. the jehol biota in northeast china and adjacent areas contains a plethora of well-preserved macrofossils of ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of ephedraceae, so northeast china and adjacent areas may represent either the centre of origination for the family or its centre of early diversification. systematics gnetales luerss. 1879 ephedraceae dumort. emend. type:ephedra l. sp. pl. familial diagnosis emended dioecious shrubs, sub-shrubs, small tree, climbers, or sometimes perennial herbs. shoots are profusely and dichasially branched and have many nodes; nodes are usually swollen, sometimes branches are whorled at nodes due to extremely reduction of internodes or alternate on account of suppression of the opposite branch; internodes of twigs possess many fine striations. leaves are opposite and decussate or ternately whorled at nodes, linear and free to basally connate into a sheath but apices acute and triangular. leaves are parallel veined, with veins. reproductive organs are usually unisexual but hermaphroditic cones occasionally occur. male cones are terminal to twigs, or pedunculate, or sessile and axillary to leaves, or clustered at nodes, bear multiple pairs/whorls of bracts each of which enclose an axillary male reproductive unit. the male reproductive unit is a shortened shoot and usually consists of a pair of bracteoles enclosing microsporangiophore. the microsporangiophore is fused or distally furcated, and terminated by 2— synangia. the synangium is sessile to pedicellate, consists of 2— microsporangia, the latter opening by horizontal slits. at maturity, the microsporangiophore is elongated outside the bracteoles and terminated by a few free or fused synangia which produce polyplicate pollen bearing longitudinal ridges and furrows. the female reproductive units or compound female cones are directly terminal to twigs, or pedunculate or sub-sessile or sessile at nodes. the compound female cones if present are trimerous or bimerous, bear to multiple whorls/pairs of leaf-like or specialized bracts, each subtending a female reproductive unit, or only the uppermost whorl/pair of bracts being fertile and the inferior whorls/pairs of bracts becoming sterile. cone bracts are sometimes modified into dry and membranous, or dry and coriaceous, or fleshy and colourful. seeds bear an outer envelope and an inner integument which usually extends upward and passes through the opening of the outer envelope, forming a thin and hollow micropylar tube. micropylar tubes varying in length and shape, — mm long, straight, curved or coiled. remarks in the family ephedraceae was instituted by the belgian botanist barthélemy-charles dumortier, who only gave a brief familial diagnosis “ovaire supère stylifère; écailles opposes; ovaire monogyne”. in modern plant taxonomy, the ephedraceae are usually characterized by features of the sole extant ephedra. however, abundant ephedroid fossil plants from the early cretaceous have increasingly broadened our understanding of the circumscription and character variation of the family, so an emended familial diagnosis is provided here. the key diagnoses of ephedraceae include enveloped ovules with extruded micropylar tubes, linear leaves opposite and decussate or ternately whorled and having 2— parallel veins. in light of the present study, ephedraceae sensu lato contain ephedra l. with ca. living species, macrofossil-species, and seed fossil-species as well as ephedroid macrofossils alloephedra tao et yang, gurvanella krassilov, liaoxia cao et wu, siphonospermum rydin et friis, leongathia krassilov et al., amphiephedra miki, and chengia gen. nov. presented herein, indicating higher generic diversity through time. early cretaceous strata of northeast china contain a plethora of well-preserved macrofossils of ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of ephedraceae, and in this respect northeast china and adjacent areas that yield the famous jehol biota might represent either the centre of origination or one of centres for early diversification of the family. chengia laxispicata y.yang, l.b.lin et q.wang gen. et sp. nov.. etymology the generic name “chengia” is dedicated to the late eminent botanist cheng wan-chun who has made enormous contributions to the taxonomy of gymnosperms; the specific epithet “laxispicata”, stemming from the latin “laxus” + “spicatus”, refers to the loosely arranged female spike which is a conspicuous feature of this fossil-species. generic and specific diagnosis reproductive shoots branch oppositely at swollen nodes. internodes bear numerous longitudinal striations. leaves that subtend lateral branches are long and linear. female spikes are terminal to twigs or are subtended by the leaf, possessing multiple pairs of loosely arranged female reproductive units. nodes and internodes of female spikes prominent. female reproductive units consist of decussately opposite seeds and subtending bracts. seeds enveloped, with distal micropylar tube. description:. holotype pe 2012041619a, b. type locality dawangzhangzi village, songzhangzi town, lingyuan city, chaoyang district, liaoning province, china. stratigraphic horizon and age dawangzhangzi bed in the middle part of the yixian formation or xinfangzi bed in the lower part of the yixian formation. repository chinese national herbarium, institute of botany, chinese academy of sciences, beijing, china. remarks the plant-bearing beds at dawangzhangzi village, lingyuan city, chaoyang district, liaoning province, northeast china have been known since the 1930s. fossil fish lycoptera jeholensis grabau, monocotyledonous plants potamogeton jeholensis yabe et endô, potamogeton? sp., gymnosperms schizolepis jeholensis yabe et endô and czekanowskia rigida heer were first reported from this early cretaceous locality. subsequently, potamogeton jeholensis was reclassified as another angiosperm ranunculus jeholensis miki or an ephedroid plant ephedrites chenii guo et x.w. wu, which is synonymous with liaoxia cheniae cao et s. q. wu. moreover, miki described a new ephedroid plant amphiephedra rhamnoides miki from this locality, which is different from our new plant chengia laxispicata gen. et sp. nov. in bearing “verticillate, scaly leaves on the lateral branches that look more like short shoots”. adjacent to dawangzhangzi village of lingyuan city, an ephedroid plant ephedrites? elegans sun et zheng was described from the jianshangou bed in the lower part of the yixian formation of huangbanjigou village, beipiao city, chaoyang district, liaoning province, northeast china. ephedrites? elegans also bears loosely arranged spikes with clear nodes and internodes, but it differs from our new plant chengia laxispicata gen. et sp. nov. in having possibly 3— bracts per whorl in spikes. another superficially similar specimen was also reported from the early cretaceous lycoptera beds of manlaj, eastern gobi in mongolia, which krassilov called “potamogeton-like spike” bearing or nutlets per node. 
seeds are sessile, with a thin outer envelope and a distal micropylar tube. the extant gnetales include three monotypic families, namely, ephedraceae, gnetaceae, and welwitschiaceae, all of which possess compound female cones that comprise a main axis and to multiple pairs/whorls of bracts subtending a female reproductive unit or having lower pairs/whorls of bracts sterile. the basal family ephedraceae including ephedra of the extant gnetales was demonstrated to have considerable diversity by the early cretaceous, so an emended familial diagnosis is given here. the jehol biota in northeast china and adjacent areas contains a plethora of well-preserved macrofossils of ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of ephedraceae, so northeast china and adjacent areas may represent either the centre of origination or one of the centres for early diversification of the family. combined with a wealth of ephedra and ephedroid macrofossils from the early cretaceous, we propose a reduction and sterilization hypothesis that the female cone of the extant ephedraceae may have stemmed from archetypal fertile organs in the crown lineage of the gnetales. biogeographychengiaearly cretaceousephedraceaeephedroidevolutionfemale conegnetalesjehol biotareduction and sterilization hypothesisyixian formation the main shoot bears internodes and swollen nodes, from which lateral branches arise oppositely. nov. is described from the early cretaceous yixian formation of western liaoning, northeast china. nov. provides a missing link between archetypal fertile organs in the crown lineage of the gnetales and compound female cones of the extant ephedraceae. the fossil represents a part of a leafy shooting system with reproductive organs attached. reproductive organs consist of female spikes terminal to twigs or axillary to linear leaves. hence, macrofossils demonstrating the structure of compound female cones of the gnetales should be important to decipher the early evolution of the order. these have undergone sequentially intermediate links similar to female cones of cretaceous siphonospermum, chengia, and liaoxia by reduction and sterilization of the lower fertile bracts, shortenings of internodes and peduncles as well as loss of reproductive units in all inferior bracts. each bract subtends an ellipsoid seed. spikes are loosely arranged, having prominent nodes and internodes. however, the evolutionary origin of such a reproductive architecture in gnetales is controversial in the light of the competing anthophyte versus gnetifer hypotheses of seed plant relationships. a new ephedroid plant chengia laxispicata gen. et sp.
 the extant gnetales include three monotypic families, namely, ephedraceae, gnetaceae, and welwitschiaceae, all of which possess compound female cones that comprise a main axis and to multiple pairs/whorls of bracts subtending a female reproductive unit or having lower pairs/whorls of bracts sterile. however, the evolutionary origin of such a reproductive architecture in gnetales is controversial in the light of the competing anthophyte versus gnetifer hypotheses of seed plant relationships. hence, macrofossils demonstrating the structure of compound female cones of the gnetales should be important to decipher the early evolution of the order.  a new ephedroid plant chengia laxispicata gen. et sp. nov. is described from the early cretaceous yixian formation of western liaoning, northeast china. the fossil represents a part of a leafy shooting system with reproductive organs attached. the main shoot bears internodes and swollen nodes, from which lateral branches arise oppositely. reproductive organs consist of female spikes terminal to twigs or axillary to linear leaves. spikes are loosely arranged, having prominent nodes and internodes. bracts of the spikes are decussately opposite and comprise 4— pairs of bracts. each bract subtends an ellipsoid seed. seeds are sessile, with a thin outer envelope and a distal micropylar tube.  chengia laxispicata gen. et sp. nov. provides a missing link between archetypal fertile organs in the crown lineage of the gnetales and compound female cones of the extant ephedraceae. combined with a wealth of ephedra and ephedroid macrofossils from the early cretaceous, we propose a reduction and sterilization hypothesis that the female cone of the extant ephedraceae may have stemmed from archetypal fertile organs in the crown lineage of the gnetales. these have undergone sequentially intermediate links similar to female cones of cretaceous siphonospermum, chengia, and liaoxia by reduction and sterilization of the lower fertile bracts, shortenings of internodes and peduncles as well as loss of reproductive units in all inferior bracts. the basal family ephedraceae including ephedra of the extant gnetales was demonstrated to have considerable diversity by the early cretaceous, so an emended familial diagnosis is given here. the jehol biota in northeast china and adjacent areas contains a plethora of well-preserved macrofossils of ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of ephedraceae, so northeast china and adjacent areas may represent either the centre of origination or one of the centres for early diversification of the family. biogeographychengiaearly cretaceousephedraceaeephedroidevolutionfemale conegnetalesjehol biotareduction and sterilization hypothesisyixian formation 