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Opinion TRENDS in Plant 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 1 Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden Section of Evolution and Ecology, University of California, Davis, CA 95616, USA 3 Institute of Systematic Botany, University of Zurich, 8008 Zurich, Switzerland 4 Nanjing Institute of Geology and Palaeontology, CAS, 39 East Beijing Road, 210008 Nanjing, The People’s Republic of China 2 With molecular analyses indicating that angiosperms are not closely related to any other extant seed plant group, information from fossils might provide the only basis for reconstructing their origin. Therefore the description of a new Early Cretaceous angiosperm, Archaefructus, placed as the sister of all extant angiosperms, has created much debate and optimism. However, we question both the interpretation and the analysis of Archaefructus, concluding that it might be a crown-group angiosperm specialized for aquatic habit rather than a more primitive relative. The family Archaefructaceae [1] was established to accommodate two extinct species, Archaefructus liaoningensis [2] and Archaefructus sinensis [1], from the Yixian Formation in northeastern China. In the initial report [2], A. liaoningensis was presented as the oldest known angiosperm because the beds were dated as Late Jurassic. However, radiometric dating strongly supports a midEarly Cretaceous age for the Yixian Formation [3], close to the age of the first records of angiosperms in other areas (Box 1). The Archaefructaceae were defined as including small herbaceous water plants with axillary branches terminating in reproductive organs, and with strongly dissected leaves. Reproductive axes were assumed to be exposed above water level and were described as solitary flowers without perianth, with numerous stamens borne in helically arranged pairs and numerous conduplicate carpels borne in a helical or whorled arrangement and maturing into multi-seeded follicles. Ge Sun et al. [1] evaluated the phylogenetic position of Archaefructus by including its morphological characters in a combined three-gene molecular and morphological analysis, which placed Archaefructus as the sister to extant angiosperms. We will discuss the characters of Archaefructus in detail and question aspects of their interpretation. Our conclusions are based on published descriptions and illustrations [1,2,4] and our own studies of additional specimens housed in the Institute of Vertebrate Paleontology and Paleoanthropology, CAS, Beijing, China. Corresponding author: Else Marie Friis ([email protected]). Ovulate and microsporangiate organs Reproductive axes are elongate with ovulate organs borne distally and microsporangiate organs borne proximally. Some specimens apparently have unisexual (ovulate) axes. The organs are crowded in young specimens (Fig. 1a) but spaced out in more mature specimens (Fig. 1b). Ovulate organs are pedicellate and typically borne in pairs on each pedicel (Fig. 2). They are elongate with an acuminate apex and enclose few (A. liaoningensis) or many (A. sinensis) ovules or seeds. Although ovulate organs of Archaefructus have not been shown to have all the features of carpels, in other respects they are more like angiosperm carpels than they are like the ovulate organs of other seed plants with enclosed ovules (Box 2). However, it is not clear that they were conduplicate (i.e. like a leaf folded lengthwise and sealed along its margins), or that the fruits were follicles, as described by Sun et al. [1,2]. Follicles open longitudinally along the ventral side. No such open fruits and Box 1. Age and palaeoenvironment of Archaefructus The Archaefructus fossils were all collected in the Yixian Formation, outcropping in the western part of Liaoning Province in northeastern China. The Yixian Formation is part of the Jehol Group, which has yielded a wealth of exquisitely preserved fossil animals, most notably feathered theropod dinosaurs and a diversity of early birds. The sediments were deposited in a low-energy lacustrine environment in a seasonally semiarid climate and are intercalated with volcanic tuffs and basalts (the environment and biota are reviewed in Ref. [3]). Although the faunal elements of the Jehol biota exhibit exceptional preservation, the plant fossils rarely have cellular details intact, and tissues are often replaced or infilled with pyrite framboids and microcrystallines [33]. However, some fossil plants have been preserved with many of the organs (roots, stems, leaves) still in organic connection. This is unusual for Cretaceous plant fossils and provides unique information about growth form in early angiosperms. The only contemporaneous flora with whole-plant preservation is the Crato flora from the Early Cretaceous of Brazil, deposited in a similar low-energy lake system [34]. The thickness of the Yixian Formation reaches 4700 m, with plant and animal fossils occurring throughout. The age of the Yixian Formation has been much debated [35] but there is now strong evidence from radiometric dating that it is Early Cretaceous [3,36–38]. The oldest Archaefructus is from the Jianshangou Bed, which is in the lower part of the Yixian Formation and dated radiometrically to , 125 million years, corresponding to the Barremian stage [3], close to the age of the first well-known angiosperm floras 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 Opinion 370 TRENDS in Plant Science Vol.8 No.8 August 2003 Box 2. Reproductive structures of Caytonia and angiosperms Fig. 1. Line drawings showing details of the reproductive organs of Archaefructus sp. (a) and Archaefructus liaoningensis (b,c) from the Early Cretaceous Yixian Formation of northeastern China. (a) Immature reproductive axis with densely spaced ovulate organs (carpels). (b) Mature reproductive axes with carpels above (ovulate zone) and microsporangiate organs (stamens) below (staminate zone). (c) Basal part of a mature reproductive axis showing clustering of the stamens in the staminate zone; a few carpels of the ovulate zone are also shown. The paired arrangement of both the carpels and stamens is evident in several places (arrow heads). Scale bar ¼ 1 cm. (a) Redrawn from Plate 32, Fig. 6, in Ref. [4]; (b) redrawn from Plate 32, Fig. 3 in Ref [4]; (c) redrawn from Plate 31, Fig. 1, in Ref [4]. (a) (b) Ovulate zone Staminat zone 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 small, dissected leaves and several reproductive axes attached to the stem. Most 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 carpels (arrows). Scale bar ¼ 1 cm. http://plants.trends.com Several non-angiospermous Mesozoic seed plants resemble Archaefructus and extant angiosperms in having enclosed ovules, but their enclosing structures clearly differ from carpels or are poorly understood. 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. The ovules of Caytonia have only one integument, rather than two, the ancestral state in angiosperms [17]. Sun et al. [2] described ovules of Archaefructus as bitegmic and anatropous (with two integuments and a reflexed orientation), but unfortunately their structure is uncertain. Even in well-preserved specimens (B0112, Fig. 2) we failed to establish the number of integuments, nature of internal structures, or orientation and attachment of ovules. Because they both have four microsporangia, stamens of 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 two pairs of sporangia on either side of a sterile connective, like angiosperm stamens. 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 it is often difficult to see whether carpels are conduplicate, 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 with several ovules arranged in two rows [7]. Microsporangiate organs of Archaefructus are borne in pairs or several together on a short common stalk (Fig. 1b,c). Sun et al. [1] described these organs as typical Opinion TRENDS in Plant Science bilateral angiosperm stamens with two pairs of microsporangia. This is not entirely clear from their figures or the material we have examined, although some do seem to show a connective between lateral pollen sacs, like typical angiosperm stamens, and unlike the radial synangia of Caytonanthus (Box 2). Flower or inflorescence? If Archaefructus is related to the angiosperms, how are its reproductive axes best interpreted? Both carpels and stamens are usually borne in pairs or several together (Figs 1,2). Similar paired carpels and stamens are unknown in multiparted angiosperm flowers. This strongly suggests that the reproductive axes are not flowers, but rather inflorescences consisting of male flowers towards the base, each with two (sometimes one or more) stamens, and female flowers consisting of one or two carpels (or unicarpellate flowers borne singly or in pairs) at the top. Furthermore, the arrangement of the organs seems to vary from opposite to subopposite or helical, which is also more typical of inflorescences than it is of flowers. Sun et al. [1] rejected the inflorescence interpretation because of the absence of bracts or bract scars below the individual organs. However, flowers in living angiosperms do not always have a subtending bract (i.e. a bract on the axis of the next lower order, in the axil of which the flower is formed). Examples include Hedyosmum (Chloranthaceae) [8] and especially some members of the largely aquatic monocot order Alismatales. Flowers of Alismatales provide special analogies for delimiting flowers in Archaefructus. In some alismatalian families that flower underwater, flowers are unisexual and have few organs; for example, in Cymodoceaceae, male flowers have two stamens (as in Archaefructus), and in Najas (Hydrocharitaceae) and Zosteraceae they have only a single stamen, and female flowers have a single carpel. Furthermore, in some of these taxa, subtending floral bracts are missing (e.g. Ruppiaceae [9] and Zosteraceae [10]). From the perspective of living aquatic angiosperms with underwater flowers, the most straightforward interpretation is that Archaefructus had unisexual flowers: the male flowers usually with two stamens, the female flowers with one or two carpels. An underwater flowering habit could also provide a functional explanation for the lack of a perianth in Archaefructus. Most extant angiosperm groups with underwater flowers have lost their perianth. The best examples are in Alismatales, in which several taxa with flowers borne above the water have a normal perianth, whereas other, related taxa have underwater flowers without a perianth (Cymodoceaceae, some Juncaginaceae, some Hydrocharitaceae, Posidoniaceae, Ruppiaceae, Zannichelliaceae, some Zosteraceae). Examples from other orders include Ceratophyllaceae (which have structures that resemble perianth parts but are interpreted as bracts because they sometimes have flowers in their axils [11]), and Callitriche (Veronicaceae). Loss of perianth in underwater-flowering plants can easily be understood on functional grounds: such flowers do not need protection against water loss in young stages, so neither sepals nor http://plants.trends.com Vol.8 No.8 August 2003 371 subtending floral bracts are necessary, and they do not need to be optically attractive, so showy parts are not necessary. It is therefore likely that there is something wrong in the original interpretation of Archaefructus, either lack of consideration of the possibility that Archaefructus was a completely submerged water plant, or the interpretation of the flowers as completely lacking a perianth and bracts. If the flowers had an underwater habit, it would resolve the puzzle of some of the more unusual features of Archaefructus: unisexual flowers, absence of a perianth and subtending floral bracts, and low organ number. Sister group or crown-group angiosperm? These arguments might not hold if Archaefructus is more basal than all living angiosperms (i.e. below the crown group – the most recent common ancestor of all living angiosperms and its derivatives), which is what Sun et al. [1] argued based on a cladistic analysis of six modern outgroups, Archaefructus, 167 living angiosperm species, molecular sequences of three genes, and 16 morphological characters, scored in Archaefructus and living groups. However, the four features that supported the basal position of Archaefructaceae [1], as ancestral character states shared with other seed plants, are problematical. Three of these characters (numbered as in [1]) involve leaves: (6) vein orders one, (7) laminar vein form dichotomous, and (8) vein fusion nonanastomosing. Characters 7 and 8 appear redundant, and three fossil taxa often proposed as closer outgroups of angiosperms, glossopterids, Gigantopteris and Caytonia [12 –15], have the angiosperm state of reticulate venation. Furthermore, the finely dissected leaf morphology of Archaefructus is unlike that of living outgroups. Such fine dissection occurred in the earliest Palaeozoic seed plants (the Sphenopteris leaf type). However, it is rare in Mesozoic seed plants, with a few exceptions such as Stenopteris [16]. However, similar leaf dissection is common in aquatic angiosperms, such as Cabomba (not included in the analysis of [1]) in the near-basal order Nymphaeales, Ceratophyllum, and some Ranunculaceae, where phylogenetic analyses imply it is derived [17,18]. The ancestral status of the fourth feature, (15) perianth absent, depends on scoring the perianth as absent in the outgroups (except Ephedra, scored 0/1). However, independent of our argument that a perianth is commonly lost in aquatic plants, we question whether it is valid to score presence or absence of a perianth in gymnospermous taxa that lack flowers. A less biased scoring would be ‘unknown’, for not applicable. Conversely, perianth-like sterile appendages do occur in at least one potential fossil outgroup, Bennettitales [19]. To test whether omission of Cabomba and the treatment of the perianth character influenced the inferred basal position of Archaefructus, we added Cabomba to the matrix (with no molecular characters and with leaves scored as dissected) and scored the outgroups as unknown for perianth. With these changes, it is more parsimonious to associate Cabomba with Archaefructus than with Brasenia, the one member of Nymphaeales in the matrix and its sister group based on molecular and morphological Opinion 372 TRENDS in Plant Science Vol.8 No.8 August 2003 Monocots Eumagnoliids Chloranthaceae Ceratophyllum Eudicots Austrobaileya Schisandra Illicium Brasenia Cabomba Archaefructus Amborella Archaefructus Extant outgroups Crown group angiosperms 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]. TRENDS in Plant Science Fig. 3. Cladogram of Sun et al. [1], simplified, with Cabomba added, showing two equally parsimonious positions for Archaefructus after scoring non-angiospermous outgroups as unknown (inapplicable) for perianth. data [18,20]. However, if Cabomba is kept with Brasenia, as supported by a great body of data, it is equally parsimonious to place Archaefructus either with Cabomba or below the angiosperms (Fig. 3). It is only one step less parsimonious to link it with Ceratophyllum. Thus, judging from this exercise, it is possible that Archaefructus is on the stem lineage to angiosperms, but the evidence for this is ambiguous. Proper exploration of this problem will require a more comprehensive morphological analysis including more characters and fossil as well as living outgroups. It could be objected that leaves of Archaefructus differ from those of Cabomba, which have several segments radiating from one point, in having a ternate structure (dividing into threes). However, in this respect Archaefructus is like the basal eudicot order Ranunculales, in which some members have highly dissected leaves (e.g. some Papaveraceae, aquatic species of Ranunculus). A similar ternate pattern is also known in Early Cretaceous (Aptian) leaves called Vitiphyllum [21 – 23], although these are less finely dissected, with several veins per lobe and reticulations among them (Fig. 4). Hence it is possible that Archaefructus is not as isolated in the Early Cretaceous as it seems. Leaves compared with Vitiphyllum, although less well preserved and more problematical, have been described from the Albian of Kazakhstan, attached to stems with inflorescences called Caspiocarpus [24], which were described as bearing few-seeded follicles. Vitiphyllum http://plants.trends.com and Caspiocarpus have been related to Ranunculales based on leaf architecture and fruit type [24,25]. These observations raise the possibility that Archaefructus is an early eudicot. Eudicots are characterized by tricolpate pollen (with three longitudinal germination furrows), which appears globally in the Albian, but extends back to the Barremian – Aptian [26 – 28], the age of Archaefructus. A eudicot affinity could be consistent with the paired arrangement of stamens and carpels in Archaefructus: dimerous floral organization is common in basal eudicots (e.g. Papaveraceae, Proteaceae, Tetracentron, Buxaceae), and phylogenetic analyses are consistent with the hypothesis that it is ancestral in the group [17,29]. The presence of eudicots in the Yixian Formation is also suggested by the discovery of another fossil plant with features suggesting a position among near-basal eudicots (e.g. syncarpous gynoecium) [30]. Pollen grains are usually valuable systematic markers. Unfortunately, although Sun et al. [1,4] isolated material from the anthers that they described as monosulcate pollen, the organic preservation is poor and the pollen grains are not convincing. They are unusual in their irregular and angular shape (shown in Refs [1,4]) and their wide size range (17 – 36 mm). Furthermore, no details are known about the pollen wall structure. Conclusions Although Archaefructus provides important new data on the early diversification of angiosperms, it is premature to conclude that it is relevant to their origin. Our interpretation of Archaefructus as a totally submerged water plant with small, simple and unisexual flowers is in accordance with inferences from molecular analyses that aquatic lineages evolved early in the radiation of angiosperms, both in the near-basal orders Nymphaeales and Opinion TRENDS in Plant Science Ceratophyllales and among basal monocots. Our interpretation is also in good agreement with the fossil record of Early Cretaceous floral structures from Europe and North America [31,32] where small, simple flowers are predominant. However, whatever its phylogenetic position, Archaefructus is significant in our understanding of the early morphological and ecological radiation of angiosperms, especially the existence of multiple early trends toward an aquatic habit. 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