Proc. Natd. Acad. Sci. USA Vol. 89, pp. 11495-11497, December 1992 Plant Biology Reproductive biology of the Permian Glossopteridales and their suggested relationship to flowering plants (Gndwan/seed fen/p d peat/phogy) EDITH L. TAYLOR AND THOMAS N. TAYLOR Byrd Polar Research Center and Department of Plant Biology, Ohio State University, Columbus, OH 43210 Communicated by Henry N. Andrews, August 27, 1992 ABSTRACT The discovery of pn rid reproductive organs fm Le ard- mr Glacier regV_io Antarctica proides anato l eidene for the ada iat- tachment of the seeds to the megasporophyll in this Impant group of Late Paeooic seed plants. The position of the seeds is in direct contradiction to many earlier Pbs predominantly on impression/compressIon remains. The at- tachment of the ovules on the adaxial surface of a leaf-like megasftiorophyfl, combinedwithotherfetre, suchasm g- metophyte development, sugs a sler reproductive biology in this group than has prev been hypothesized. These findings confirm the of the Glessopteridales as seed ferns and are important coider- FIG. 1. Cross section of megasporophyll (below) showing three ato in dc ons f the of the group, cldg ovules attached to the adaxial (upper) surface. Arrow points to ovule phylogey that has been broken off and is reoriented with the micropyle facing their suggestd role as close relatives or possible c of the megasporophyll. Note circular pads of resistant tissue around the a osperms. micropyle. Arrowheads delimit outer edge of megasporophyll. (x15.) The Glossopteridales are a group of extinct gymnospermous plants that dominated many terrestrial habitats in Gondwana locality along Skaar Ridge in the Beardmore Glacier region of during Permian times. In fact, the presence of Glkssopteris the central Transantarctic Mountains (8447' S, 163'15' E) leaves on various southern continents, including South Amer- (13, 14). The fossils occur within the Upper Buckley Forma- ica, South Africa, India, Australia, and Antarctica, provided tion and are probably Late Permian in age. The plants are some of the first evidence for continental drift. Although preserved in silica and can be studied by utilizing cellulose glossopterid leaves are one of the most common plant fossils acetate peels after etching in hydrofluoric acid. The flora of known from the Permian of Gondwana, the affinities of the the peat deposit can be compared to many other Gondwana group have been debated for many years. They are now most sites of similar age in that it is dominated by Glossopteris com nly classified as seed ferns, based on the documenta- remains (15), including two different species of leaves (16), tion of leaf-borne reproductive parts in permineralized spec- Vertebraria underground organs, and wood of the Araucar- imens from the Bowen Basin of Queensland, Australia (1). ioxylon type. A small, well-preserved moss, Merceria au- However, their evolutionary origin and relationships to other gustica, has also been described from this site (17). groups continue to remain unresolved, even though several The glossopterid reproductive organs consist of several authors have proposed glossopterids to be potential an- small, leaf-like megasporophylls that are 6 mm wide and -1.0 giosperm ancestors (2-5). Along with other Paleozoic and mm thick (Figs. 1 and 2). The adaxial surface of each Mesozoic seed fern groups, they have been included in cla- megasporophyll is uneven and bears a number of platysper- distic analyses on the origin of the flowering plants (e.g., see mic ovules that are aligned with their long axes along the refs. 6 and 7). The emergence of an integrated understanding length of the sporophyll (Fig. 2). Since the specimens are of the phylogenetic position of the glossopterids continues to incomplete, the total length of the sporophyll is not known. be hampered by varying interpretations ofthe basic morphol- The edges of the megasporophyll are partially inrolled, so ogy of the reproductive organs, especially the seed-bearing that the ovules attached near the outer edge are partly (ovulate) fructifications (8-11). Some authors suggest that the covered (Fig. 1, arrowheads). group is polyphyletic (e.g., see refs. 8 and 12), while cladistic The sporophyll is leaf-like in its organization and exhibits analyses have treated the glossopterids as monophyletic (6, 7). an epidermis with thickened walls and a hypodermis that The problem is further exacerbated by the generally very poor contains large lacunae; many ofthese are often crushed. The preservation of most of the fossils. Only one example of a vascular bundles include a mass of primary xylem with pernineralized ovulate fructification is known (from the Bo- scalariform thickenings; a space is present in the position that wen Basin ofQueensland, Australia) (1), and most ofthe other was once occupied by the phloem (Fig. 3). The orientation of fructifications described to date represent impression fossils the sporophyll surfaces (adaxial versus abaxial) was deter- with no cuticle preserved. mined by the consistent arrangement of the vascular bundles The present material consists of specimens ofglossopterid (xylem positioned closest to the surface with the ovules). The reproductive organs preserved in permineralized peat from a anatomy of the megasporophyll is similar to that of Glosso- pteris schopfii, one of the two leaf types described from the The publication costs of this article were defrayed in part by page charge same site (16). payment. This article must therefore be hereby marked "advertisement" Three orthotropous, platyspermic ovules are attached to in accordance with 18 U.S.C. §1734 solely to indicate this fact. the adaxial surface of one of the megasporophylls (Fig. 1). 11495 Downloaded by guest on September 26, 2021 114% Plant Biology: Taylor and Taylor Proc. Natl. Acad. Sci. USA 89 (1992) FIG. 2. Suggested reconstruction of megasporophyll showing vascular bundles (black, xylem; white, position of phloem), undu- lating surface, and winged ovules. Four ovules are present in the vicinity of the fructification, but one has broken off and is turned completely around, so that the micropyle is now directed toward the megasporo- phyll (Fig. 1, arrow). In addition, the remains ofa small stalk are present between two of the attached ovules, indicating the position of a fifth ovule. Since the entire length of the seed-bearing leaf is unknown, it is not possible to determine whether it bore more than five ovules. Each ovule is sessile FIG. 3. Cross section of vascular bundle. Arrow, xylem; space and slightly sunken into the adaxial surface of the mega- below it was probable site of phloem tissue (arrowheads). o, ovule sporophyll. Surrounding the micropyle is a region ofthicker- attached to upper surface. (x65.) walled tissue that is usually well-preserved. Other ovular tissues, such as layers of the integument, are too poorly settle this morphological controversy, it is possible that a preserved to identify. The ovules measure 1.8 mm long, 0.7 morphological "bauplan" existed in these Permian plants mm in the secondary plane, and 2.3 mm in the primary plane. that is no longer represented among the limited groups ofseed They contain simple pollen chambers and a narrow wing =0.5 plants still extant today. mm wide (Fig. 4). Basic information on the reproductive biology of the glos- A number ofovules that appear identical to those attached sopterids is also poorly known, in part because of the to the megasporophyll are present dispersed in the peat problems caused by various interpretations of the seed- matrix (Figs. 4 and 5). These show the characteristic ring of bearing organs. Only a handful of fructifications have ever resistant tissue around the micropyle (Fig. 5, arrow) but also been found attached to axes and, because of this, the rela- contain bisaccate, striate pollen grains in the pollen chamber tionship ofthe reproductive unit to its subtending leafand the (Fig. 4, arrow). These are most comparable to dispersed orientation of the megasporophyll (i.e., whether the ovules pollen ofProtohaploxypinus, which has been recovered from are borne on the adaxial or abaxial surface) has been open to rocks of similar age of the Buckley Formation in the Beard- conjecture. Pant and Singh (21) described a fructification that more Glacier area (18). Some of the dispersed ovules are in was attached to a stalk bearing Glossopteris taenioides a later stage of development than those that are attached to leaves. This fructification was borne in the axil ofthe leafand the megasporophyll. A few contain mature female gameto- bore ovules on the apparent adaxial surface. With the dis- phytes and, in one case, a possible embryo. covery of the first anatomically preserved (i.e., permineral- Although >30 genera of ovulate fructifications have been ized) Glossopteris fructification in the Bowen Basin of assigned to the Glossopteridales, there is widespread con- Queensland (1), it was hoped that the affinities of the glos- troversy over the morphology of these reproductive organs. sopterids and their reproductive biology could be better Originally described by Plumstead (19) as bisexual, this understood. Unfortunately, however, these specimens were interpretation has now been generally discounted. Contro- too poorly preserved to discern the position ofthe xylem and versy still exists, however, over whether some fructifications phloem in the vascular bundles and, therefore, the correct are fundamentally dorsiventral or three-dimensional and orientation ofthe megasporophyll. Thus, the present material cone-like (8). Plumstead described the dorsiventral struc- from Antarctica represents definitive proof for the attach- tures, such as Scutum, as two-valved, with the ovules ment of the ovules in this group to the adaxial surface of the attached to one valve and the second valve overlying this megasporophyll. (and presumably providing a protective function). Rigby (20) Although it has been suggested previously that glosso- suggests that these reproductive organs more likely consist of pterid ovules were borne on the adaxial surface of the a single fleshy bract bearing ovules, which is split into two megasporophyll (e.g., see refs.