Opinion TRENDS in Science Vol.8 No.8 August 2003 369

Archaefructus – angiosperm precursor or specialized early angiosperm?

Else Marie Friis1, James A. Doyle2, Peter K. Endress3 and Qin Leng4

1Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden 2Section of Evolution and Ecology, University of California, Davis, CA 95616, USA 3Institute of Systematic Botany, University of Zurich, 8008 Zurich, Switzerland 4Nanjing Institute of Geology and Palaeontology, CAS, 39 East Beijing Road, 210008 Nanjing, The People’s Republic of China

With molecular analyses indicating that angiosperms Ovulate and microsporangiate organs are not closely related to any other extant seed plant Reproductive axes are elongate with ovulate organs borne group, information from might provide the only distally and microsporangiate organs borne proximally. basis for reconstructing their origin. Therefore the Some specimens apparently have unisexual (ovulate) axes. description of a new Early angiosperm, The organs are crowded in young specimens (Fig. 1a) but , placed as the sister of all extant angio- spaced out in more mature specimens (Fig. 1b). Ovulate sperms, has created much debate and optimism. organs are pedicellate and typically borne in pairs on each However, we question both the interpretation and the pedicel (Fig. 2). They are elongate with an acuminate apex analysis of Archaefructus, concluding that it might be a and enclose few (A. liaoningensis) or many (A. sinensis) crown-group angiosperm specialized for aquatic habit ovules or seeds. rather than a more primitive relative. Although ovulate organs of Archaefructus have not been shown to have all the features of carpels, in other The family Archaefructaceae [1] was established to respects they are more like angiosperm carpels than they accommodate two extinct , Archaefructus liaonin- are like the ovulate organs of other seed with gensis [2] and Archaefructus sinensis [1], from the Yixian enclosed ovules (Box 2). However, it is not clear that they Formation in northeastern China. In the initial report [2], were conduplicate (i.e. like a leaf folded lengthwise and A. liaoningensis was presented as the oldest known sealed along its margins), or that the fruits were follicles, angiosperm because the beds were dated as Late . as described by Sun et al. [1,2]. Follicles open long- However, radiometric dating strongly supports a mid- itudinally along the ventral side. No such open fruits and age for the [3], close to the age of the first records of angiosperms in other areas (Box 1). Box 1. Age and palaeoenvironment of Archaefructus The Archaefructaceae were defined as including small The Archaefructus fossils were all collected in the Yixian Formation, herbaceous water plants with axillary branches terminat- outcropping in the western part of Liaoning Province in northeastern ing in reproductive organs, and with strongly dissected China. The Yixian Formation is part of the Jehol Group, which has yielded a wealth of exquisitely preserved animals, most leaves. Reproductive axes were assumed to be exposed notably feathered theropod dinosaurs and a diversity of early above water level and were described as solitary flowers birds. The sediments were deposited in a low-energy lacustrine without perianth, with numerous borne in environment in a seasonally semiarid climate and are intercalated helically arranged pairs and numerous conduplicate with volcanic tuffs and basalts (the environment and biota are reviewed in Ref. [3]). Although the faunal elements of the Jehol biota carpels borne in a helical or whorled arrangement and exhibit exceptional preservation, the plant fossils rarely have cellular maturing into multi-seeded follicles. details intact, and tissues are often replaced or infilled with pyrite Ge Sun et al. [1] evaluated the phylogenetic position of framboids and microcrystallines [33]. However, some fossil plants Archaefructus by including its morphological characters in have been preserved with many of the organs (roots, stems, leaves) still in organic connection. This is unusual for Cretaceous plant a combined three-gene molecular and morphological fossils and provides unique information about growth form in early analysis, which placed Archaefructus as the sister to angiosperms. The only contemporaneous flora with whole-plant extant angiosperms. We will discuss the characters of preservation is the Crato flora from the Early Cretaceous of Brazil, Archaefructus in detail and question aspects of their deposited in a similar low-energy lake system [34]. The thickness of the Yixian Formation reaches 4700 m, with plant interpretation. Our conclusions are based on published and animal fossils occurring throughout. The age of the Yixian descriptions and illustrations [1,2,4] and our own studies Formation has been much debated [35] but there is now strong of additional specimens housed in the Institute of evidence from radiometric dating that it is Early Cretaceous [3,36–38]. Vertebrate Paleontology and Paleoanthropology, CAS, The oldest Archaefructus is from the Jianshangou Bed, which is in the lower part of the Yixian Formation and dated radiometrically to Beijing, China. ,125 million years, corresponding to the Barremian stage [3], close to the age of the first well-known angiosperm floras Corresponding author: Else Marie Friis ([email protected]). elsewhere [31,39]. http://plants.trends.com 1360-1385/03/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00161-4 370 Opinion TRENDS in Plant Science Vol.8 No.8 August 2003

Box 2. Reproductive structures of Caytonia and angiosperms

Several non-angiospermous Mesozoic seed plants resemble Archae- fructus and extant angiosperms in having enclosed ovules, but their enclosing structures clearly differ from carpels or are poorly under- stood. The best examples are Caytonia (Caytoniales, a ‘Mesozoic pteridosperm’ [16]), Irania (related to Czekanowskiales? [40]), and Leptostrobus (Czekanowskiales [41]). Caytoniales were first described by Hamshaw Thomas [42] from Yorkshire (UK) as Jurassic angiosperms, but later Tom Harris [16] documented that Caytonia had gymnospermous reproduction, with pollen germinating inside the micropyles of the ovules. Subsequently, the homology of the ovule-bearing structures (‘cupules’) with carpels was questioned. The cupules appear to be borne in two rows on a bilateral axis, like leaflets on the rachis of a compound leaf, unlike carpels, which are borne like leaves on a radial stem. Caytonia cupules are circinately curved toward the axis; their plane of symmetry is perpendicular to the axis, and ovules form an arc perpendicular to this plane of symmetry. By contrast, the ovulate structures of Archaefructus are elongate and acuminate, their plane of symmetry is parallel to the axis, and ovules are attached parallel to the plane of symmetry – typical features of carpels. Leptostrobus also has ovulate organs arranged along an axis. They consist of two valves, but each valve seems to differ from a carpel in its symmetry and in bearing ovules in an arc perpendicular to its plane of symmetry [41]. Irania also has paired ovulate organs borne along an axis [40], but the detailed structure of the organs is unknown and a more detailed comparison is not possible. Fig. 1. Line drawings showing details of the reproductive organs of Archaefructus The ovules of Caytonia have only one integument, rather than two, sp. (a) and Archaefructus liaoningensis (b,c) from the Early Cretaceous Yixian For- the ancestral state in angiosperms [17]. Sun et al. [2] described ovules mation of northeastern China. (a) Immature reproductive axis with densely spaced of Archaefructus as bitegmic and anatropous (with two integuments ovulate organs (carpels). (b) Mature reproductive axes with carpels above (ovulate and a reflexed orientation), but unfortunately their structure is zone) and microsporangiate organs (stamens) below (staminate zone). (c) Basal part of a mature reproductive axis showing clustering of the stamens in the stami- uncertain. Even in well-preserved specimens (B0112, Fig. 2) we failed nate zone; a few carpels of the ovulate zone are also shown. The paired arrange- to establish the number of integuments, nature of internal structures, ment of both the carpels and stamens is evident in several places (arrow heads). or orientation and attachment of ovules. Scale bar ¼ 1 cm. (a) Redrawn from Plate 32, Fig. 6, in Ref. [4]; (b) redrawn from Because they both have four microsporangia, stamens of Plate 32, Fig. 3 in Ref [4]; (c) redrawn from Plate 31, Fig. 1, in Ref [4]. angiosperms have often been compared with the synangia of Caytoniales (Caytonanthus) [42]. These are borne in groups on lateral stalks along an axis. The stalks often branch several times, but occasionally there are only two or three synangia grouped closely on an unbranched stalk, suggesting the arrangement in Archaefructus. However, Caytonanthus synangia are radial structures with four equally spaced microsporangia, rather than bilateral structures with (a) (b) two pairs of sporangia on either side of a sterile connective, like angiosperm stamens. Ovulate zone Caytonia has figured in discussions of angiosperm origin, but with the cupules interpreted as homologous with the bitegmic ovules of angiosperms, not with the carpels [12,14,43–46].

no dehiscence line were observed. Even in living material

Staminat it is often difficult to see whether carpels are conduplicate, zone and it might be impossible in these fossils. Microtome serial sections would be necessary, but the preservation does not allow such studies. In Brasenia (Cabombaceae) and Zannichellia (Zannichelliaceae) (two extant aquatics belonging to near-basal angiosperm clades, one with above-water flowers, the other with underwater flowers), carpels look superficially like those of Archaefructus. However, they are not conduplicate but completely ascidiate (i.e. developing like a tube from a ring-like primordium) [5,6]. Brasenia and Zannichellia have only one or a few ovules per carpel, but Austrobaileya, another extant basal angiosperm, has completely ascidiate carpels Fig. 2. A well-preserved specimen (B0112) of Archaefructus sinensis from the Early Cretaceous Yixian Formation of northeastern China. (a) Portion of the plant with with several ovules arranged in two rows [7]. small, dissected leaves and several reproductive axes attached to the stem. Most Microsporangiate organs of Archaefructus are borne axes are young with densely spaced reproductive organs, but one is mature with the organs spaced out. (b) Details of the mature axis showing distinctly paired car- in pairs or several together on a short common stalk pels (arrows). Scale bar ¼ 1 cm. (Fig. 1b,c). Sun et al. [1] described these organs as typical http://plants.trends.com Opinion TRENDS in Plant Science Vol.8 No.8 August 2003 371 bilateral angiosperm stamens with two pairs of micro- subtending floral bracts are necessary, and they do not sporangia. This is not entirely clear from their figures or need to be optically attractive, so showy parts are not the material we have examined, although some do seem to necessary. show a connective between lateral pollen sacs, like typical It is therefore likely that there is something wrong in angiosperm stamens, and unlike the radial synangia of the original interpretation of Archaefructus, either lack of Caytonanthus (Box 2). consideration of the possibility that Archaefructus was a completely submerged water plant, or the interpretation of or inflorescence? the flowers as completely lacking a perianth and bracts. If If Archaefructus is related to the angiosperms, how are its the flowers had an underwater habit, it would resolve the reproductive axes best interpreted? Both carpels and puzzle of some of the more unusual features of Archae- stamens are usually borne in pairs or several together fructus: unisexual flowers, absence of a perianth and (Figs 1,2). Similar paired carpels and stamens are subtending floral bracts, and low organ number. unknown in multiparted angiosperm flowers. This strongly suggests that the reproductive axes are not Sister group or crown-group angiosperm? flowers, but rather inflorescences consisting of male These arguments might not hold if Archaefructus is more flowers towards the base, each with two (sometimes one basal than all living angiosperms (i.e. below the crown or more) stamens, and female flowers consisting of one or group – the most recent common ancestor of all living two carpels (or unicarpellate flowers borne singly or in angiosperms and its derivatives), which is what Sun et al. pairs) at the top. Furthermore, the arrangement of the [1] argued based on a cladistic analysis of six modern organs seems to vary from opposite to subopposite or outgroups, Archaefructus, 167 living angiosperm species, helical, which is also more typical of inflorescences than it molecular sequences of three genes, and 16 morphological is of flowers. characters, scored in Archaefructus and living groups. Sun et al. [1] rejected the inflorescence interpretation However, the four features that supported the basal because of the absence of bracts or bract scars below the position of Archaefructaceae [1], as ancestral character individual organs. However, flowers in living angiosperms states shared with other seed plants, are problematical. do not always have a subtending bract (i.e. a bract on the Three of these characters (numbered as in [1]) involve axis of the next lower order, in the axil of which the flower leaves: (6) vein orders one, (7) laminar vein form is formed). Examples include Hedyosmum (Chlorantha- dichotomous, and (8) vein fusion nonanastomosing. Char- ceae) [8] and especially some members of the largely acters 7 and 8 appear redundant, and three fossil taxa aquatic monocot order Alismatales. of Alismatales often proposed as closer outgroups of angiosperms, provide special analogies for delimiting flowers in Archae- glossopterids, Gigantopteris and Caytonia [12–15], have fructus. In some alismatalian families that flower under- the angiosperm state of reticulate venation. Furthermore, water, flowers are unisexual and have few organs; for the finely dissected leaf morphology of Archaefructus is example, in Cymodoceaceae, male flowers have two unlike that of living outgroups. Such fine dissection stamens (as in Archaefructus), and in Najas (Hydrochar- occurred in the earliest Palaeozoic seed plants (the itaceae) and Zosteraceae they have only a single , Sphenopteris leaf type). However, it is rare in Mesozoic and female flowers have a single carpel. Furthermore, in seed plants, with a few exceptions such as Stenopteris [16]. some of these taxa, subtending floral bracts are missing However, similar leaf dissection is common in aquatic (e.g. Ruppiaceae [9] and Zosteraceae [10]). From the angiosperms, such as Cabomba (not included in the perspective of living aquatic angiosperms with under- analysis of [1]) in the near-basal order , water flowers, the most straightforward interpretation is Ceratophyllum, and some Ranunculaceae, where phylo- that Archaefructus had unisexual flowers: the male genetic analyses imply it is derived [17,18]. flowers usually with two stamens, the female flowers The ancestral status of the fourth feature, (15) perianth with one or two carpels. absent, depends on scoring the perianth as absent in the An underwater flowering habit could also provide a outgroups (except Ephedra, scored 0/1). However, inde- functional explanation for the lack of a perianth in pendent of our argument that a perianth is commonly lost Archaefructus. Most extant angiosperm groups with in aquatic plants, we question whether it is valid to score underwater flowers have lost their perianth. The best presence or absence of a perianth in gymnospermous taxa examples are in Alismatales, in which several taxa with that lack flowers. A less biased scoring would be flowers borne above the water have a normal perianth, ‘unknown’, for not applicable. Conversely, perianth-like whereas other, related taxa have underwater flowers sterile appendages do occur in at least one potential fossil without a perianth (Cymodoceaceae, some Juncaginaceae, outgroup, Bennettitales [19]. some Hydrocharitaceae, Posidoniaceae, Ruppiaceae, Zan- To test whether omission of Cabomba and the treatment nichelliaceae, some Zosteraceae). Examples from other of the perianth character influenced the inferred basal orders include Ceratophyllaceae (which have structures position of Archaefructus, we added Cabomba to the that resemble perianth parts but are interpreted as bracts matrix (with no molecular characters and with leaves because they sometimes have flowers in their axils [11]), scored as dissected) and scored the outgroups as unknown and Callitriche (Veronicaceae). Loss of perianth in under- for perianth. With these changes, it is more parsimonious water-flowering plants can easily be understood on to associate Cabomba with Archaefructus than with functional grounds: such flowers do not need protection Brasenia, the one member of Nymphaeales in the matrix against water loss in young stages, so neither nor and its sister group based on molecular and morphological http://plants.trends.com 372 Opinion TRENDS in Plant Science Vol.8 No.8 August 2003

Crown group angiosperms

Extant outgroups Archaefructus Amborella Archaefructus Cabomba Brasenia Illicium Schisandra Austrobaileya Ceratophyllum Chloranthaceae Eumagnoliids Monocots

Fig. 4. Line drawing of Vitiphyllum – an Early Cretaceous leaf type characterized by a ternate pattern of dissection (Baltimore, lower Potomac Group, Aptian). This pattern is generally similar to that of Archaefructus, although the lobes are much wider and the lamina has reticulate venation. Reproduced, with permission, from [23].

and Caspiocarpus have been related to Ranunculales based on leaf architecture and fruit type [24,25]. TRENDS in Plant Science These observations raise the possibility that Archae- fructus is an early eudicot. Eudicots are characterized by Fig. 3. Cladogram of Sun et al. [1], simplified, with Cabomba added, showing two equally parsimonious positions for Archaefructus after scoring non-angiosper- tricolpate pollen (with three longitudinal germination mous outgroups as unknown (inapplicable) for perianth. furrows), which appears globally in the Albian, but extends back to the Barremian–Aptian [26–28], the age data [18,20]. However, if Cabomba is kept with Brasenia, of Archaefructus. A eudicot affinity could be consistent as supported by a great body of data, it is equally with the paired arrangement of stamens and carpels in parsimonious to place Archaefructus either with Cabomba Archaefructus: dimerous floral organization is common or below the angiosperms (Fig. 3). It is only one step less in basal eudicots (e.g. Papaveraceae, Proteaceae, Tetra- parsimonious to link it with Ceratophyllum. Thus, judging centron, Buxaceae), and phylogenetic analyses are con- from this exercise, it is possible that Archaefructus is on the sistent with the hypothesis that it is ancestral in the group stem lineage to angiosperms, but the evidence for this is [17,29]. The presence of eudicots in the Yixian Formation ambiguous. Proper exploration of this problem will require a is also suggested by the discovery of another fossil plant more comprehensive morphological analysis including more with features suggesting a position among near-basal characters and fossil as well as living outgroups. eudicots (e.g. syncarpous ) [30]. It could be objected that leaves of Archaefructus differ Pollen grains are usually valuable systematic markers. from those of Cabomba, which have several segments Unfortunately, although Sun et al. [1,4] isolated material radiating from one point, in having a ternate structure from the anthers that they described as monosulcate (dividing into threes). However, in this respect Archae- pollen, the organic preservation is poor and the pollen fructus is like the basal eudicot order Ranunculales, in grains are not convincing. They are unusual in their which some members have highly dissected leaves irregular and angular shape (shown in Refs [1,4]) and their (e.g. some Papaveraceae, aquatic species of Ranunculus). wide size range (17–36 mm). Furthermore, no details are A similar ternate pattern is also known in Early known about the pollen wall structure. Cretaceous (Aptian) leaves called Vitiphyllum [21–23], although these are less finely dissected, with several Conclusions veins per lobe and reticulations among them (Fig. 4). Although Archaefructus provides important new data on Hence it is possible that Archaefructus is not as the early diversification of angiosperms, it is premature to isolated in the Early Cretaceous as it seems. Leaves conclude that it is relevant to their origin. Our interpret- compared with Vitiphyllum, although less well pre- ation of Archaefructus as a totally submerged water plant served and more problematical, have been described with small, simple and unisexual flowers is in accordance from the Albian of Kazakhstan, attached to stems with with inferences from molecular analyses that aquatic inflorescences called Caspiocarpus [24],whichwere lineages evolved early in the radiation of angiosperms, described as bearing few-seeded follicles. Vitiphyllum both in the near-basal orders Nymphaeales and http://plants.trends.com Opinion TRENDS in Plant Science Vol.8 No.8 August 2003 373

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