The origin of the ovule

Of several theories for the origin of the ovule advanced in this century and based largely on fossil evidence, the telomic concept is widely considered the most plausible. Its principal tenet is the evolution of the integument through fusion of sterile branches or telomes around a terminal megasporangium. The only point of agreement in these theories is that the entire nucellus is a megasporangium that retains a single megaspore and the endosporic female gametophyte. Their differences center on the origin of the integument. A new concept offered here on evidence from ovules of both Paleozoic and extant seed plants significantly alters the telomic theory. It proposes that the nucellus is a sporangiophore of stem origin that bears a terminal megasporangium; that at least some of the fused integumentary telomes were fertile; and that among all features cited to characterize ovules, the unique nature of the retained megaspore alone defines the seed habit. Changes in the seed plant megaspore that extended the period of nutrient absorption over the whole course of female gametophyte development, along with complex physiological changes in the nucellus, were probably achieved along a single phylogenetic line beginning in a Late Devonian population of progymnosperms. For such a combination of events to have occurred more than once is highly unlikely, and, therefore, a monophyletic origin for seed plants is proposed. Several primitive features in ovule structure, some not evidenced since the Lower Carboniferous Period, occur in a mutant form of Arabidopsis thaliana isolated from genetically transformed plants. Their recurrence provides additional support for the proposed concept of ovule origin and also suggests that the genetic mechanisms for expression of primitive features in advanced taxa could be initiated in each case by mutation of a single homeotic gene.     

Reinvestigation of Nystroemia pectiniformis Halle, an enigmatic seed plant from the Upper Permian of China

Reinvestigation of Nystroemia pectiniformis Halle from the Upper Shihhotze Formation of Shanxi Province, China, has led to the identification of new and important features of this enigmatic Late Permian seed plant, permitting its typification and diagnosis. After reassembling several of the previously studied specimens to form a single articulated branching system comprising at least four orders of branching, previously unknown features of its branching pattern and morphology have been characterized. First–order axes are wide and branch to one side only, bearing second–order branches either singly or in pairs and of two kinds: one fertile and bearing characteristic ovulate branching systems and the other presumably vegetative. Ovulate second–order axes are narrow and branch to one side only, producing numerous, closely spaced lateral branches in two alternate to sub–opposite rows. Lateral branches are slender and produce numerous ovulate branching systems to one side of the axis only. Ovulate branching systems divide unequally to produce 3–15 ultimate axes of different lengths that are planated. Each ultimate axis bears a single terminal ovule with 180 degree rotational symmetry and two horn–like integumentary projections distally. The other kind of second–order axes are distinct from those bearing ovules; they are wider and longer and branches occur on both sides of the secondary axis, lacking divisions in close proximity to the first–order axis. These have only been observed incomplete although their distinct morphology indicates they are unlikely to be ovulate branches from which ovules/seeds have been shed. Additional organs of the Nystroemia plant are considered, including pollen organs previously assigned by Halle to the same species (displaying its characteristic branching style), and also leaves of Chiropteris reniformis Halle that were probably borne on the larger kind of second–order branches. Implications of Nystroemia on seed plant evolution and distribution are discussed, and it is concluded that this most likely represents a late stratigraphic occurrence of a plesiomorphic hydrasperman–type seed plant with affinities closely allied to members of the Lyginopteridales.     

Pollen Organ Telangiopsis sp. of Late Devonian Seed Plant and Associated Vegetative Frond

Pollen organ Telangiopsis sp., associated with but not attached to vegetative fronds, has been collected from the Upper Devonian (Famennian) Wutong Formation, Dongzhi County, Anhui Province, China. Fertile axes with terminal pollen organs are dichotomous for 2–4 times and may be proximally attached by fragmentary pinnules. Pollen organs are synangiate and borne on the top of a short stalk. Synangia are radial in symmetry and each consists of 4–8 elongate microsporangia fused at base. Microsporangia have a longitudinal dehiscence line and show a tapered apex. The associated stem is spiny and bears a vegetative frond which bifurcates once at the basalmost part. Frond rachises possess one order of pinna arranged alternately. Pinnules are borne alternately, planate, highly dissected, and equally dichotomous for 2–3 times. Comparisons among Late Devonian seed plants recognize several branching patterns in the fertile fronds/axes bearing terminal pollen organs. Telangiopsis sp. reinforces that the Late Devonian pollen organs are synangiate usually with basally fused microsporangia. It is suggested that the evolutionary divergence of radial and bilateral symmetries of pollen organs may have occurred in the Famennian, when the earliest seed plants evolved planate and sometimes laminate pinnules.     

Resolving the systematic and phylogenetic position of isolated ovules: a case study on a new genus from the Permian of China

Isolated ovules occur in many fossil plant assemblages, where they provide important insights into seed‐plant diversity and evolution. However, in many cases, the ovules cannot be attributed to individual groups of seed plants, restricting systematic and evolutionary assessments that can be made from otherwise well‐characterized fossil taxa. In the present paper, we describe a new kind of ovule discovered in tuffaceous sediments from the Permian‐aged Xuanwei Formation in Guizhou Province, China. This ovule has 180° rotational symmetry and an integument comprising a variably thick sarcotesta, a uniformly thick sclerotesta and a uniformly thin endotesta. The nucellus is attached to the integument at least basally and contains a collapsed seed megaspore; a nucellar apex is absent. Both the integument and nucellus are vascularized by paired bundles in the major plane of the ovule; the integumentary bundles are considerably larger than the nucellar bundles and the nucellar bundles emerge from a conical vascular pad. Generation of a three‐dimensional reconstruction based on serial peels revealed the gross morphology and organization of the ovule and highlighted the presence of features consistent with cardiocarpalean‐type ovules (ovule shape, histological features of the integument) and also features more typical of lagenostomalean‐ and trigonocarpalean‐type ovules (large integumentary bundles, presence of nucellar bundles). To assess the affinity and evolutionary significance of the ovule, it has been included in a cladistic matrix of cardiocarpalean‐, lagenostomalean‐ and trigonocarpalean‐type ovules. Results place the ovule within the cardiocarpalean group of ovules known to have been produced by several plant groups, including cordaitean coniferophytes, pteridosperms and Palaeozoic conifers. The cladistic topology supports generic level distinction of the present species, requiring the establishment of Muricosperma guizhouensis Seyfullah & J.Hilton gen. & sp. nov . Lagenostomalean ovules produced by hydrasperman pteridosperms form a basal paraphyletic grade, whereas trigonocarpalean ovules produced by medullosan pteridosperms form a monophyletic group in which Stephanospermum is paraphyletic with respect to Rhynchosperma and Pachytesta. The results also place the Mississippian ovule Mitrospermum bulbosum apart from all of the Pennsylvanian species of Mitrospermum that form a strongly supported clade. Consequently, M. bulbosum is transferred to the new genus Whitaddera Seyfullah & J.Hilton as W. bulbosa (Long) Seyfullah & J.Hilton. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164 , 84–108.     

Permineralized seed fern cupules from the Triassic of Antarctica: implications for cupule and carpel evolution

In this paper we describe the first anatomically preserved Mesozoic seed fern cupule–Petriellaea. The multiovulate cupules were produced singly at the end of a short dichotomizing axis. Cupules are bilateral with a dorsal groove and transverse narrow ventral opening. The vascular system of the cupule consists of a series of traces that extend up the dorsal surface of the cupule and down the ventral face. Ovules are orthotropus, sessile, and borne on the adaxial surface of the leaflike cupule either singly or in multiple rows. They are up to 1.5 mm long, triangular in transverse section, and characterized by a multilayered integument. Nucellus and integument are fused throughout their length, but no pollen chamber is present. In the chalaza is a small vascular disc of transfusion tracheids that represents the extent of the ovule vascular system. Ovules are interpreted as being fossilized at a prepollination stage, although a few possess some evidence of a cellularized megagametophyte. These permineralized cupules indicate that in at least one Mesozoic seed fern group, ovule enclosure resulted from the transverse folding (tip to petiole) of a megasporophyll bearing adaxial ovules. Cupule morphology and ovule enclosure in other Late Paleozoic and Mesozoic seed ferns is discussed.     

Expression of female sterility in alfalfa (<Emphasis Type="Italic">Medicago sativa</Emphasis> L.)

Female sterility associated with the presence of callose in the nucellus at anthesis was studied in an F₁ progeny of two alfalfa plants displaying 5 and 81% ovule sterility. Transgressive segregation was observed and 100% sterile plants were obtained. Two of the sterile plants were used for cytological analyses on sectioned and stain-cleared whole ovules, in comparison to a 100% fertile full sib plant. The first sign of sterility was callose deposition in the nucellus cell walls surrounding the sporogenous cells of the young ovules. At the same stage, no trace of callose was present in ovule primordia of the fertile plant. Megaspore mother cells differentiated in both fertile and sterile ovules and meiosis was initiated, as indicated by chromatin patterning typical of a zygotene stage. However, meiosis was never completed in the sterile plants. In the control, callose was deposited around the meiocyte and as sects between the cells of the dyads and tetrads during meiosis, and disappeared after the completion of meiosis; an embryo sac developed and female fertility was normal. In the sterile ovules, some nucellus cells enlarged and callose accumulation continued forming thick deposits. At anthesis, the sterile ovules lacked an embryo sac and showed massive callose accumulation in the nucellus. Male fertility was normal in female-sterile plants, thus a female-specific arrest of sporogenesis appears to be the cause of sterility. Pistil development was aberrant in some sterile genotypes, even with arrested pistil growth in early flower buds.     

Angiosperm ovules: diversity, development, evolution

Background

Ovules as developmental precursors of seeds are organs of central importance in angiosperm flowers and can be traced back in evolution to the earliest seed plants. Angiosperm ovules are diverse in their position in the ovary, nucellus thickness, number and thickness of integuments, degree and direction of curvature, and histological differentiations. There is a large body of literature on this diversity, and various views on its evolution have been proposed over the course of time. Most recently evo–devo studies have been concentrated on molecular developmental genetics in ovules of model plants.

Scope

The present review provides a synthetic treatment of several aspects of the sporophytic part of ovule diversity, development and evolution, based on extensive research on the vast original literature and on experience from my own comparative studies in a broad range of angiosperm clades.

Conclusions

In angiosperms the presence of an outer integument appears to be instrumental for ovule curvature, as indicated from studies on ovule diversity through the major clades of angiosperms, molecular developmental genetics in model species, abnormal ovules in a broad range of angiosperms, and comparison with gymnosperms with curved ovules. Lobation of integuments is not an atavism indicating evolution from telomes, but simply a morphogenetic constraint from the necessity of closure of the micropyle. Ovule shape is partly dependent on locule architecture, which is especially indicated by the occurrence of orthotropous ovules. Some ovule features are even more conservative than earlier assumed and thus of special interest in angiosperm macrosystematics.     

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.     

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.     

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.     

OVULE ABORTION IN ‘NONPAREIL’ ALMOND (PRUNUS DULCIS [MILL.] D. A. WEBB)

The earliest indication of ovule abortion in almond (Prunus dulcis [Mill.] D. A. Webb ‘Nonpareil‘) is the deposition of callose (as indicated by aniline blue fluorescence) 2 days after pollination which is 2 days before clear histological symptoms of ovule degeneration are evident and 6 days before fertilization of the viable ovule. Callose deposition begins in the chalazal region of the nucellus where the funicular trace enters the ovule and ramifies into the integuments. As ovule abortion progresses, callose deposition in the inner integument extends as a ring around the nucellus. Movement of the fluorescent dye disodium fluorescein (uranin) indicated that translocation from the vascular trace into abortive ovules becomes blocked at the chalazal position. The dye freely penetrates and diffuses into viable ovules but fails to penetrate abortive ovules. Lack of, or delayed and irregular, megagametophyte development was another characteristic of abortive ovules. Biochemical and histochemical analyses of abortive and viable ovules indicated that carbohydrate depletion parallels ovule abortion. These observations lead to the conclusion that ovule abortion is accompanied by blockage in metabolite supply although whether this blockage is the primary cause or a consequence of ovule abortion is uncertain.     

Anatomically preserved Cycadeoidea (Cycadeoidaceae), with a reevaluation of systematic characters for the seed cones of Bennettitales

Four anatomically preserved ovulate cycadeoid cones have been recovered from three localities in Upper Cretaceous (Turonian/Coniacian-Late Campanian) sediments of Vancouver and Hornby Islands, British Columbia, Canada. All of the specimens are preserved by calcareous cellular permineralization and are quite similar to seed cones described as several species of Cycadeoidea and Bennettites. These cones, described as Cycadeoidea maccafferyi sp. nov., consist of tightly packed interseminal scales and ovulate sporophylls with terminal ovules. Two specimens also preserve remains of a small receptacle. Interseminal scales and ovulate sporophylls are oriented parallel to one another. Ovules are distinctly stellate at the base of the micropylar tube, and the sarcotesta consists of both longitudinally oriented tubular cells and large radially elongated cells attached to the sclerotesta. The vascular strand below each ovule is highly contorted in a pattern that is characteristic of contractile tissue in the roots of living plants. These specimens are the most recent anatomically preserved cycadeoid cones yet discovered, revealing details of the reproductive biology shortly before extinction of the clade. Superb preservation of the British Columbia cones confirms that Bennettitales lack a cupule, have radial seeds, and have a vascularized nucellus (but no integumentary tracheids), and that no pollen chamber is produced. Together with a new species of Williamsonia preserved at one of the same localities, these specimens reveal a clear set of contrasting systematic characters for differentiating between isolated seed cones of Williamsoniaceae and Cycadeoidaceae.     

CONE AND OVULE ONTOGENY IN TAXODIUM AND GLYPTOSTROBUS (TAXODIACEAE – CONIFERALES)

Seed cones in Taxodium distichum and Glyptostrobus pensilis occupy the position of permanent shoots and are initiated in the summer preceding spring pollination. Morphological features are similar in the two genera, reflecting their close taxonomic relationship. Ovule complexes originate as two (rarely more) ovule primordia in the axil of each fertile bract but without any indication of a preceding discrete ovuliferous scale. When the nucellus, integument, and micropyle are well developed, a series of up to ll abaxial lobes forms at the base of each ovule pair. They become fused by basal growth. After pollination the common basal meristem of lobes and bract extends by intercalary growth to form the conspicuous “ovuliferous scale” of the mature cone; the lobes enlarge and exceed the ovules. Despite the topographic similarity in the cones of both genera, there are differences in vasculature such that the vascular traces to the axillary complex originate directly from the axial cylinder in Glyptostrobus but from the bract trace in Taxodium. The complex vasculature of the mature cone develops late and primarily as an expression of intercalary growth.     

False paracarpy in Seemannaralia (Araliaceae): from bilocular ovary to unilocular fruit

Background and Aims

Seemannaralia appears to be fundamentally different from all other Araliaceae in the presence of a well-developed symplicate zone in its gynoecium, as well as in the ovule insertion in the symplicate zone (rather than in the cross-zone). The present investigation re-examined the floral structure of Seemannaralia with emphasis on the morphology and evolution of its gynoecium.

Methods

Flowers and fruits of Seemannaralia gerrardii at various developmental stages were examined using light microscopy and scanning electron microscopy.

Key Results

Ovaries in the flowers of Seemannaralia are bilocular. Each ovary locule corresponds to a carpel whose ascidiate part is distinctly longer than the plicate part. Each carpel contains one fertile ovule attached to the cross-zone, and one sterile ovule as well. The fruit is unilocular: its central cavity is occupied by a single large seed. In the course of fruit development, the growth of one ovule stops while another ovule develops into the mature seed. When this ovule outgrows the available space in the locule, the septum is ruptured, forming a united cavity of two carpels.

Conclusions

Despite literature data, the synascidiate zone is well developed in the gynoecium of Seemannaralia, and the ovules are attached to the cross-zone. Its preanthetic and anthetic gynoecium has nearly the same structure as gynoecia of most other Araliaceae. The Seemannaralia fruit resembles the paracarpous gynoecium but its ground plan is very different because the central cavity is formed by mechanical rupture of the septum. The term ‘pseudoparacarpy’ (‘false paracarpy’) is proposed to describe this condition, which has not been reported to date for indehiscent fruits in any taxa other than Seemannaralia. In this genus, the pseudoparacarpy has probably resulted from a decrease in seed number in the course of the transition from zoochory to anemochory.     

Influence of intraovular reserves on ovule fate in apricot (Prunus armeniaca L.)

 In many plant species with multiovulate ovaries, a considerable reduction in the number of ovules takes place. However, the underlying physiological causes are not clear. In Prunus spp., although flowers present two ovules, usually only one seed is produced. We have followed the development and degeneration of the two ovules in apricot (Prunus armeniaca L.) and examined the extent to which carbohydrates within the ovule might be involved in determining the fate of the ovule. While the primary ovule grows in the days following anthesis, growth of the secondary ovule is arrested. Starch distribution along the different ovular tissues exhibits several changes that are different in the two ovules. Primary ovule growth is inversely related to starch content and this growth takes place independently of pollination since it occurs in the same way in pollinated and unpollinated flowers. In the secondary ovule, starch disappears simultaneously from all ovular structures and callose is layered at the chalazal end of the nucellus. The size of the secondary ovule does not change significantly from anthesis to degeneration, and callose starts to accumulate 5 days after anthesis. Likewise, this process occurs independently of pollination. These results are discussed in terms of the implications of the starch content of ovules in fertilization success and ovule fate. Received: 26 August 1997 / Revision accepted: 17 December 1997     

Leaf evolution in early-diverging ferns: insights from a new fern-like plant from the Late Devonian of China

Background and Aims With the exception of angiosperms, the main euphyllophyte lineages (i.e. ferns sensu lato, progymnosperms and gymnosperms) had evolved laminate leaves by the Late Devonian. The evolution of laminate leaves, however, remains unclear for early-diverging ferns, largely represented by fern-like plants. This study presents a novel fern-like taxon with pinnules, which provides new insights into the early evolution of laminate leaves in early-diverging ferns.Methods Macrofossil specimens were collected from the Upper Devonian (Famennian) Wutong Formation of Anhui and Jiangsu Provinces, South China. A standard degagement technique was employed to uncover compressed plant portions within the rock matrix.Key Results A new fern-like taxon, Shougangia bella gen. et sp. nov., is described and represents an early-diverging fern with highly derived features. It has a partially creeping stem with adventitious roots only on one side, upright primary and secondary branches arranged in helices, tertiary branches borne alternately or (sub)oppositely, laminate and usually lobed leaves with divergent veins, and complex fertile organs terminating tertiary branches and possessing multiple divisions and numerous terminal sporangia.Conclusions Shougangia bella provides unequivocal fossil evidence for laminate leaves in early-diverging ferns. It suggests that fern-like plants, along with other euphyllophyte lineages, had independently evolved megaphylls by the Late Devonian, possibly in response to a significant decline in atmospheric CO₂ concentration. Among fern-like plants, planate ultimate appendages are homologous with laminate pinnules, and in the evolution of megaphylls, fertile organs tend to become complex.     

Studies of carboniferous pteridosperm seeds: The relationship of the integument and nucellus in Pachytesta gigantea

Specimens of the medullosan ovule Pachytesta gigantea possess internal ribs which extend from the chalaza up to the level of the pollen chamber. These internal ribs are present adjacent to the primary ribs on the inner surface of the integument and appear histologically similar to the sclerotesta. The cuticle of the endotesta and the nucellus closely conform to the internal ribs in shape and the shrinkage pattern exhibited by the cuticular membranes suggests that the cuticle of the nucellus and cuticle of the endotesta may have been fused to one another along the internal ribs at some stage of development. The implications of this possible nucellar—integumentary fusion are discussed relative to the classification and phylogeny of Paleozoic seeds.     

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.