Distinguishing angiophytes from the earliest angiosperms: A Lower Cretaceous (Valanginian-Hauterivian) fruit-like reproductive structure

A remarkably diverse Lower Cretaceous (Valanginian-Hauterivian) flora at Apple Bay, Vancouver Island, preserves seed plants at an important time of floristic evolutionary transition, about the same time as the earliest flowering plant megafossils. The fossils are permineralized in carbonate concretions and include tetrahedral seeds within cupule- or carpel-like structures. These enclosing structures, composed of elongate sclerenchyma cells with spiral thickenings that grade externally to a few layers of parenchyma, are vascularized by one collateral vascular bundle and lack trichomes. They apparently broke open to release the tightly enclosed seeds by valves. Seeds are similar to those of the Triassic seed fern Petriellaea, but are about 100 million years younger and differ in size, vascularization, integumentary anatomy, seed attachment, and number of seeds/cupule. These new seeds are described as Doylea tetrahedrasperma gen. et sp. nov., tentatively assigned to Corystospermales. Inverted cupules are reminiscent of an outer angiosperm integument rather than a carpel. Like fruits, cupules opened to release seeds at maturity, thereby foretelling several aspects of angiospermy. They show that nearly total ovule enclosure, a level of organization approaching angiospermy, was achieved by advanced seed ferns during the Mesozoic.     

THE CRETACEOUS PTERIDOSPERMS RUFLORINIA AND KTALENIA AND IMPLICATIONS ON CUPULE AND CARPEL EVOLUTION

The vegetative (Ruflorinia sierra) and fertile (Ktalenia circularis) organs of an Early Cretaceous pteridosperm collected from Santa Cruz Province in Argentina are described. The sterile leaf is at least tripinnate and bears decurrent secondary pinnae with obliquely attached, sharply pointed pinnules. The fertile member arises from the base of the vegetative rachis and bears two types of appendages, cupules and bracts. Bracts are attached to the main axis near cupules and are present in clusters of up to six. Cupules are sessile, spherical, and arranged in opposite or subopposite pairs along the axis. A small lip is present on one surface of the cupule. The number of seeds per cupule may be one or two, with each characterized by a distal nucellar beak and circular, chalazal scar. Cuticular anatomy, including the fine structure of the stomatal complex, is described for both vegetative and reproductive organs. The cupules of Ktalenia and other Mesozoic seed plants are compared, and a discussion presented regarding the possible function of the cupule.     

Morphology of the gynoecium and systematic position of the Ochnaceae

The gynoecium is syncarpous in all Ochnaceae. In the Ochnoideae carpels are peltate with a conventional cross-zone bearing one ovule, or, in Lophira , a very broad cross-zone with an horizontal ovular row. In Ochna and Brackenridgea , the style is gynobasic, each carpel develops transmitting tissue on its morphologically dorsal surface, and this tissue lines a canal or originates a solid inner strand in each carpel at style level. The style is tubular, with an inner cuticle, and compound, each component with its own transmitting tissue. In Ouratea the style is solid with a single compound transmitting strand. In Lophira and Elvasia the transmitting tissue seems to be developed by the morphologically ventral carpellary surfaces. Ovules are unitegmic with a bivalent integument.
In the Sauvagesioideae carpels are peltate, but with ovules above the cross-zones, on margins of the symplicate zone. In Euthemis , there is one ovule on each side of, and close to, each cross-zone. The single stylar canal is bounded by the morphologically dorsal carpellary surfaces. In Sauvagesia ovules occur on both sides of the cross-zones but most of them are above on carpel margins, as are all ovules of Cespedesia. The stylar canal of Sauvagesia is bounded by the ventral carpel surfaces, three strips of the outer surface passing inside at the sutures and developing into transmitting tissue. The stylar canal of Cespedesia is bounded by the dorsal carpel surfaces. The gynoecium of Wallacea has two epeltate carpels with a laminar placentation, the carpel margins being displaced on to the topographically ventral carpel surfaces with a row of ovules along each margin. Ovules are bitegmic.
The Ochnoideae, which shows relationships with the Rutaceae, Meliaceae, Simaroubaceae and Hippocastanaceae, is more advanced than the Sauvagesioideae, which clearly belongs in the Violales. The Ochnaceae is to be placed in the Violales.     

Latisemenia longshania,gen. et sp. nov., a new Late Devonian seed plant from China

The earliest known ovules in the Late Devonian (Famennian) are borne terminally on fertile branches and are typically enclosed in a cupule. Among these ovules are some that have terete integumentary lobes with little or no fusion. Here, we report a new taxon, Latisemenia longshania, from the Famennian of South China, which bears cupulate ovules that are terminal as well as opposite on the fertile axis. Each ovule has four broad integumentary lobes, which are extensively fused to each other and also to the nucellus. The cupule is uniovulate, and the five flattened cupule segments of each terminal ovule are elongate cuneate and shorter than the ovule. Associated but not attached pinnules are laminate and Sphenopteris-like, with an entire or lobate margin. Latisemenia is the earliest known plant with ovules borne on the side of the fertile axis and may foreshadow the diverse ovule arrangements found among younger seed plant lineages that emerge in the Carboniferous. Following the telome theory, Latisemenia demonstrates derived features in both ovules and cupules, and the shape and fusion of integumentary lobes suggest effective pollination and protection to the nucellus. Along with other recent discoveries from China, Latisemenia extends the palaeogeographic range of the earliest seed plants.     

AIRFLOW PATTERNS AROUND SOME EARLY SEED PLANT OVULES AND CUPULES: IMPLICATIONS CONCERNING EFFICIENCY IN WIND POLLINATION

Aerodynamic analyses showing characteristic airflow patterns and the potential for wind-mediated pollination are presented for models of Paleozoic (Carboniferous) ovules and ovulate cupules (i.e., Genomosperma kidstoni, G. latens, Salpingostoma dasu, Physostoma elegans, Eurystoma angulare, and Stamnostoma huttonense). Lobes on ovules and cupules are shown to produce localized regions of turbulent flow with a concomitant reduction in airflow velocity. Data based upon models that mimic the characteristics of windborne pollen (= pseudopollen) show that these regions of turbulent flow correspond to those in which suspended pseudopollen impact with ovule and/or cupule surfaces. These data have bearing on a sequence of ovule morphologies purported to show the evolution of the integument by the progressive reduction in length of “preintegumentary” lobes and their acropetal fusion. As the preintegumentary lobes of the models studied consolidate around the megasporangium, regions of turbulent flow and high pseudopollen impact become localized around the pollen chamber or salpinx. The general morphologic trend envisioned for the evolution of the ovule is seen to be associated with an aerodynamic streamlining and an increased potential for wind-mediated pollination. Data for hair-bearing ovules and for ovulate cupules are discussed within the context of possible selective pressures favouring streamlining.     

Gone and ovule ontogeny in Phyllocladus (Podocarpaceae)

TOMLINSON, P. B., TAKASO, T. & RATTENBURY, J. A., 1989. Cone and ovule ontogeny in Phyllocladus (Podocarpaceae). Cones are borne directly on phylloclades, usually in the position of basal segments or as segment appendages. Each cone consists of a series of spirally arranged bracts, of which the middle bracts each subtend a single, sessile ovule. There is no ovuliferous scale. Ovules arise as ovoid outgrowths; integument development involves periclinal divisions of hypodermal cells with the integument becoming bilobed and extended laterally. The mature ovule is flask-shaped. The integument includes an extensive middle region bounded by an inner and outer epidermis; the outer hypodermis is differentiated as two contrasted cell layers. An aril differentiates late by periclinal divisions of the outer hypodermal cells at the base of the ovule. The three outermost layers of the integument become differentiated in the mature seed as an epidermis, with thick, cutinized outer tangential walls, an outer hypodermal tanniniferous layer and a sclerotic inner layer. Each ovule is vascularized by two strands that diverge from the axial bundles delimiting the gap left by the departing bract trace.     

MITROSPERMUM VINCULUM SP. NOV., A CARDIOCARPALEAN OVULE FROM THE UPPER PENNSYLVANIAN OF OHIO

Numerous anatomically preserved ovules assignable to the genus Mitrospermum have been discovered in Upper Pennsylvanian sediments of Eastern Ohio. Although basically similar to Mitrospermum compressum, the newly discovered specimens exhibit several consistent differences. Ovules are strongly platyspermic, up to 4.2 mm long, 4.0 mm wide, and 0.6 mm thick. In the minor plane, ovules are broadest at the base and taper toward the micropyle. The integument exhibits three topographic regions: endotesta, sclerotesta, and sarcotesta. The sarcotesta is extremely broad in the major plane, where it forms two membranous wings. A single terete vascular bundle enters the base of the ovule, traverses the integument, and divides to form two integumentary bundles and a conspicuous nucellar platform. Integumentary bundles extend toward the tip of the ovule at the margin of the sarcotesta and sclerotesta. A pollen chamber with a prominent nucellar beak is delimited at the tip of the nucellus. Consistent differences in vascularization, size, nature of the seed base, features of the pollen chamber, and the Late Pennsylvanian age demonstrate that the specimens represent a distinct species. The discovery of these ovules extends the stratigraphic range of Mitrospermum to the Upper Pennsylvanian of Ohio.     

A comparative study of the ontogenetic development of the cupules inCastanea andLithocarpus (Fagaceae)

Two contradicting theories have been proposed for the morphological nature of fagaceous cupules; the intercalary growth theory and the higher order dichasial branch theory. All the previous ontogenetic studies insist on the latter one, but the genera investigated have been rather restricted and have not covered all the cupule types. A comparative study of the ontogenetic development of cupules inCastanea crenata andLithocarpus edulis, which are representatives of fundamentally different cupule types, revealed that both the theories are incomplete. InL. edulis, the higher order dichasial branches contribute to cupule formation along the anterior portions of the lateral flowers. However, along the adaxial portion of the central flower, the cupule develops as an intercalary growth, represented by rapid increase of tangentially oblong epidermal cells. InCastanea, intercalary growth is not clearly observable, for presumably, the flowers are surrounded by a well-developed partial inflorescence mound from the beginning of development.Contributions from the Osaka Museum of Natural History No. 305.     

Female flower and cupule structure in Balanopaceae,an enigmatic rosid family

The Balanopaceae, whose flowers were poorly known, have, in the past, been variously allocated to the Fagales, Euphorbiaceae, Salicales or other hamamelids and rosids (these groups being in Fagales, Malpighiales and Saxifragales, according to the Angiosperm Phylogeny Group). This paper attempts a clarification based on flower morphology. Female flowers and cupules were studied in Balanops vieillardii, young fruits in B. australiana. The cupules are simple involucres of bracts which are spirally arranged (according to a Fibonacci pattern) on the floral axis preceding the flower. They contrast with the complicated cupules of Fagaceae which consist of a condensed cymose ramification system of axes of several orders around the flower. Flowers appear later than most of the cupular bracts, in contrast to Fagaceae. In addition to a terminal flower there may be several smaller lateral flowers in the axil of cupular bracts, each surrounded by its own small cupule. The female flowers do not have a perianth. They consist of two to three large carpels. At anthesis, the ovary is completely septate; the syncarpous part (ovary and lower style) is completely symplicate. The carpels are free for most of their length, with the free parts once, twice or three times bifurcate, in contrast to simple in Fagales. The stigmatic surface covers the ventral side of each stigmatic branch and at the margins also spreads to the dorsal side. The stigma is wet and secretion appears holocrine. The two ovules per carpel are collateral and axile in early development. However, at anthesis they appear one above the other, because in one ovule the funicle greatly elongates. As the ovary elongates only above the placenta, the ovules appear basal at anthesis. The ovules are (weakly) crassinucellar, bitegmic (not unitegmic), anatropous, and intermediate between apotropous and epitropous (not apotropous). The ovules are mature at anthesis, in contrast to Fagales. In mature ovules the upper part of the nucellus disintegrates, and a weakly differentiated endothelium is present in the inner integument. The morphological results of this study support a position of Balanopaceae in Malpighiales, and not Fagales or other orders, and are thus in accordance with recent molecular results based on chloroplast rbcL sequences data. However, within Malpighiales, as opposed to molecular results, Balanopaceae agree more with Euphorbiaceae s.l. than with Dichapetalaceae/Trigoniaceae and Chrysobalanaceae/Euphroniaceae.     

Embryogenesis and seed development in Sinomanglietia glauca (Magnoliaceae)

The development of the floral bud, especially the ovule and seed coat, of Sinomanglietia glauca was observed. Floral buds were covered by eight to nine hypsophyll pieces. The hypsophyll nearest the tepal was closed completely and characterized by two arrays of densely stained cells with dense cytoplasm, which split longitudinally at flowering. The perianth consisted of 16 tepals arranged in three whorls. The gynoecium was composed of numerous apocarpous carpels; the ovule was anatropous with two integuments. Embryogenesis was of the Polygonum type, and the endosperm was nuclear. The inner integument degenerated during seed development. The seed of S. glauca had an endotestal seed coat comprised of a sclerotic layer derived from the inner adaxial epidermis of the outer integument and a sarcotesta derived mainly from the middle cells between the inner and outer epidermis of the outer integument. The embryo developed normally, so embryogenesis is not the cause of difficult regeneration.     

Studies on the cupulate seed genus Hydrasperma Long from Berwickshire and East Lothian in Scotland and County Kerry in Ireland

Twelve petrified cupules containing seeds of Hydrasperma tenuis Long from the Upper-Devonian/ Lower Carboniferous Transition Series from Ballyheigue, Kerry Head, Ireland have been studied. The cupules containing 2–6 seeds are borne in pairs. Each cupule is campanulate and composed of up to 24 oval to terete units. The axis of the cupule is forked, each resultant branch dividing in an alternate monopodial fashion producing six major axes. These divide repeatedly, each terminating in a narrow rounded tip. A reconstruction of a four-seeded cupule is presented. Hydrasperma longii sp. nov. is proposed for the first 'named' Scottish cupulate seeds named by Long as Hydrasperma cf. tenuis. Hydrasperma longii differs from H. tenuis: comparison of H. tenuis with other cupulate Lower Carboniferous seeds indicates that two major branching patterns of the cupule occur in early seed plants. Following an initial dichotomy, branching may either be entirely dichotomous, or alternately monopodial. The Aneurophytales appears to have the branching patterns consistent with its position as the ancestral group.     

Axial nature of the cupule‐bearing organ in Caytoniales

Abstract Caytoniales are an important group of seed plants, and the nature of their female reproductive organ may influence interpretations of the seed plant phylogeny and the origin of angiosperms. Although not convincingly demonstrated by clear evidence, cupules on previously described specimens were interpreted as being distichously arranged, implying that the cupule‐bearing organ in Caytoniales was a pinnate megasporophyll. Here a female reproductive organ of Paracaytonia hongtaoi gen. et sp. nov. (Caytoniales) is reported from Liaoning, China. The well preserved specimen clearly shows a spiral arrangement of cupules along the reproductive axis, suggesting that the cupule‐bearing organ in Caytoniales is not a megasporophyll but a branch. This new information on the axial nature of the cupule‐bearing organ in Caytoniales has significant implications on the placement of Caytoniales in the seed plant phylogeny and interpretation of the relationship between Caytoniales and angiosperms.     

ONTOGENY OF THE PALEOZOIC OVULE,CALLOSPERMARION PUSILLUM

The ontogeny of the upper Pennsylvanian age gymnospermous ovule, Callospermarion pusillum, is described from petrifaction specimens collected at the Berryville locality in Illinois. Ovules exhibit a wide range of dimensional and structural features that indicate an extensive developmental sequence. Specimens range from ovules with indistinct zonation of the thin-walled integument to those with thick-walled cells of the sclerotesta. The apex of the fleshy nucellus in some specimens is preserved as a cellular mound, while in others a well-formed cellular pollen chamber is present; still other ovules are characterized by a papery-thin nucellus and pollen chamber wall. The megagametophyte of most specimens is represented by a hollow megaspore membrane that may be restricted to the base of the nucellus, or occupy the entire seed cavity. In a few specimens cellular gametophytes are preserved, and in one ovule archegonia with supposed eggs are also present. Variability in each of the features is compared with ontogenetic changes in comparable structures of living gymnospermous ovules and is correlated with ovule size. A developmental sequence for the fossil ovules is proposed.     

Interactions among Genes Regulating Ovule Development in Arabidopsis Thaliana

The INNER NO OUTER (INO) and AINTEGUMENTA (ANT) genes are essential for ovule integument development in Arabidopsis thaliana. Ovules of ino mutants initiate two integument primordia, but the outer integument primordium forms on the opposite side of the ovule from the normal location and undergoes no further development. The inner integument appears to develop normally, resulting in erect, unitegmic ovules that resemble those of gymnosperms. ino plants are partially fertile and produce seeds with altered surface topography, demonstrating a lineage dependence in development of the testa. ant mutations affect initiation of both integuments. The strongest of five new ant alleles we have isolated produces ovules that lack integuments and fail to complete megasporogenesis. ant mutations also affect flower development, resulting in narrow petals and the absence of one or both lateral stamens. Characterization of double mutants between ant, ino and other mutations affecting ovule development has enabled the construction of a model for genetic control of ovule development. This model proposes parallel independent regulatory pathways for a number of aspects of this process, a dependence on the presence of an inner integument for development of the embryo sac, and the existence of additional genes regulating ovule development.     

Morphological and ontogenetic studies on southern African podocarps. Initiation of the seed scale complex and early development of integument, nucellus and epimatium

STOFFBERG, E., 1991. Morphological and ontogenetic studies on southern African podocarps. Initiation of the seed scale complex and early development of integument, nucellus and epimatium. The primordium of the seed scale complex (ssc) (ovule with epimatium) is initiated in the axil of the first or second cone bracts (prophylls) as a dome shaped structure consisting of a group of uniform, meristematic cells. A distinct protodermal layer develops. The nucellus is a dome on the ventral side of the ssc primordium. In the species of section Podocarpus the integument is initiated as a circular ridge around the nucellus, while in P.falcatus two protrusions on the anterior and posterior sides of the nucellus are the first indications of integumentary differentiation. The integument of all species studied is of subdermal origin. The epimatium (sensu stricto) is initiated after the integument, is of subdermal origin and forms a hood around the developing ovule. Considering research results, together with related literature, it is concluded that the integument of gymnosperms may be homologous with the outer integument of a bitegmic angiospermous ovule, that the position of integumentary initiation may be specific for certain taxa and that there seems to be no constant sequence of emergence of ovular envelopes in gymnosperms.     

Homeotic Transformation of Ovules into Carpel-like Structures in Arabidopsis

Ovules are specialized reproductive organs that develop within the carpels of higher plants. In Arabidopsis, mutations in two genes, BELL1 (BEL1) and APETALA2 (AP2), disrupt ovule development. In Bel1 ovules, the inner integument fails to form, the outer integument develops abnormally, and the embryo sac arrests at a late stage of megagametogenesis. During later stages of ovule development, cells of the outer integument of a Bel1 ovule sometimes develop into a carpel-like structure with stigmatic papillae and second-order ovules. The frequency of carpel-like structures was highest when plants were grown under conditions that normally induced flowering and was correlated with ectopic expression in the ovule of AGAMOUS (AG), an organ-identity gene required for carpel formation. Together, these results suggested that BEL1 negatively regulates AG late in ovule development. Likewise, mutants homozygous for the strong AP2 allele ap2-6 sometimes displayed structures with carpel-like features in place of ovules. However, such abnormal Ap2 ovules are much less ovulelike in morphology and form earlier than the Bel1 carpel-like structures. Because one role of the AP2 gene is to negatively regulate AG expression early in flower development, it is possible that AP2 works in a similar manner in the ovule. A novel ovule phenotype observed in Bel1/Ap2-6 double mutants suggested that BEL1 and AP2 genes function independently during ovule development.