FLORAL ONTOGENY IN CYCLAMEN PERSICUM ‘F-1 ROSEMUNDE ROSE’ (PRIMULACEAE)

Floral ontogeny was examined in Cyclamen persicum ‘F-1 Rosemunde Rose’ using a combination of light and scanning electron microscopy. The leaf plastochron index (LPI), earlier calculated for leaf elongation, was used to determine the length of each stage of floral development. LPI will provide a useful tool for selecting flowers of a given stage from large plant populations or from plants where flowers are small or inaccessible during early ontogenetic stages. Most features of floral development are similar to those previously described for other primulaceous genera. The petal-stamen relationship, however, is unusual; stamens arise through periclinal cell divisions in the adaxial surface layers of common petal-stamen primordia. Anatomical evidence suggests that the placenta is formed both by appendicular initials which give rise to the ovules and ventral carpellary bundles, and receptacular cells which form some, if not all, of the central axis.     

Cell division patterns of the protoderm and root cap in the “closed” root apical meristem ofArabidopsis thaliana

Summary The peripheral root cap and protoderm inArabidopsis thaliana are organized into modular packets of cells derived from formative T-divisions of the root cap/protoderm (RCP) initials and subsequent proliferative divisions of their daughter cells. Each module consists of protoderm and peripheral root cap packets derived from the same periclinal T-division event of an RCP initial. Anatomical analyses are used to interpret the history of extensively coordinated cell divisions producing this modular construction. Within a given layer of root cap, the columella and RCP initials divided in a centrifugal sequence from the innermost columella initials toward the RCP initials. All RCP initials in the lineages around the circumference of the root divided nearly simultaneously in waves to form one module prior to the next wave of initial divisions forming a younger module. The peripheral root cap and protoderm packets within each module completed four rounds of proliferative divisions in the axial plane to produce, on average, 16 cells per packet in the basalmost modules in axial view. Peripheral root cap and protoderm cells predominantly in the T-type (trichoblast) lineages also underwent radial divisions as they were displaced basipetally. The regularity in the cellular pattern within the modules suggests a timing mechanism controlling highly coordinated cell division in the initials and their daughter cells.Abbreviations RAM root apical meristem - RCP root cap protoderm - prc peripheral root cap     

A fossil record of developmental events: variation and evolution in epidermal cell divisions in ostracodes

The carapaces of some ostracode taxa bear reticulate skeletal ridges that outline underlying epidermal cells. This anatomy allows one to identify homologous cells across individuals, to infer the modal sequence of cell divisions that occurs over ontogeny, and to identify individuals with variant cell patterns (e.g., additional or missing cell divisions), even in fossils. Here we explore the variational properties and evolutionary history of this developmental system in the deep-sea ostracode genus Poseidonamicus. Using a sample of over 2000 specimens to capture variation in cell division sequence, we show that phenotypic variation in this system is highly structured: some variants, regions of the carapace, and lineages are much more variable than others. Much of the differences in variation among cells can be attributed to the molt stage in which cells take their final form-cell divisions occurring later in ontogeny are more variable than those earlier. Despite ample variation, only two evolutionary changes in the sequence of cell divisions occur over the 40 Myr history of this clade. The evolutionary changes that do occur parallel the two most common intraspecific variants, suggesting that developmental structuring of variation can have long-term evolutionary consequences. Analysis of the most common variant over the last two molt stages suggests that it suffers a fitness disadvantage relative to the modal form. Such normalizing selection may contribute to the evolutionary conservativeness of this developmental system in the Ostracoda.     

Embryology of Ceratopteris richardii (Pteridaceae, tribe Ceratopterideae), with emphasis on placental development

This comprehensive study of early embryology in Ceratopteris richardii combines light microscopy with the first ultrastructural evaluation of any pteridophyte embryo. Emphasis is placed on ontogeny of the foot and placental transfer cells. The embryology of C. richardii shares many similarities with that of other polypodiacious ferns while exhibiting distinctive division patterns. Formative embryonic stages have been reconstructed into three-dimensional models for ease of interpretation. The zygote divides perpendicular to the gametophyte plane and anterioposterior axis. This division establishes a prone embryological habit that maximizes rapid independent establishment of a leaf-root axis in a cordate gametophyte. After the formation of a globular eight-celled stage, initials of the first leaf, and root and shoot apical meristems are defined early by discrete formative divisions. Concomitantly, the foot expands and differentiates to transport nutrients from the gametophyte for the developing embryonic organs. Transfer cell wall ingrowth deposition begins in the gametophyte placental cells before the adjacent sporophyte cells just after the eight-celled stage. These observations provide an anatomical framework for future comparative developmental genetic studies of embryogenesis in free-sporing plants.     

IMPERMANENT INITIALS OF THE SHOOT APEX AND DIPLONTIC SELECTION IN A JUNIPER CHIMERA

Shoot meristems of Juniperus davurica cv. Expansa Variegata possess an apical zonation pattern similar to that found in some angiosperms. Anticlinal divisions predominate in the outer layer, the tunica. The underlying core of cells, the corpus, has cell divisions oriented in all directions. Typically, this variety exists as a periclinal chimera, the outer layer genotypically albino and the inner core composed of normal, chlorophyll-producing cells. In this condition a shoot appears green. Occasionally a tunica cell divides periclinally and displaces an initial in the apical region of the corpus. This event subsequently is expressed during ontogeny as an albino sector on the stem and leaves. Frequent variation in the width of an albino sector throughout ontogeny suggests a temporary nature of cells in the position of apical initials. A correlation was documented between the position of axillary bud release and a subsequent increase or decrease in the width of an albino sector. A model based upon stochastic processes and diplontic selection is proposed to account for the dynamic nature of chimeric patterns observed in this plant.     

DNA Synthesis and Cell Division During Spore Germination in Lygodium japonicum

This paper describes the ontogenetic sequence of cell divisionsand associated DNA synthetic patterns observed in sectionedspores of Lygodium japonicum (Thunb.) Sw., collected at differentstages of germination. Following exposure to a saturating doseof red light, the spore undergoes an asymmetric division toform a basal cell, which retains nearly all of the storage inclusions,and an apical cell which expands and protrudes from the rupturedsporoderm. Division of the apical cell results in formationof a protonemal cell and an intermediate cell. Subsequently,the latter cell divides to form the primary rhizoid and a wedgecell adjacent to the protonemal cell. Secondary rhizoids mayarise from later divisions of either the basal cell or the wedgecell. In addition, the wedge cell appears to have the capacityto form a secondary prothal-lial filament. Histochemical localizationof cell constituents indicates an increasing concentration ofcytoplasmic RNA and protein in the presumptive protonemal regionof the spore cell prior to division. Autoradiography of ³H–thymidineincorporation has shown that synthesis of nuclear DNA precedeseach cell division. Although strictly nuclear DNA synthesisoccurs during early stages of germination, extra-nuclear DNAsynthesis increases greatly following division of the sporecell. The results are discussed in relation to earlier studieson cell division patterns seen in whole mount preparations ofgerminating spores of different species of Lygodium. Lygodium japonicum, spore germination, cell division, DNA synthesis     

The development of stomata and other epidermal cells on the rice leaves

In the leaves of rice (Oryza sativa), stomatal initials arose from two asymmetric cell divisions and a symmetric division. Guard mother cells (GMCs) and long cells in stomatal files (LCSs) were formed through the first asymmetric division of the precursor cell of GMCs. Subsidiary cells (SCs) were produced by the second asymmetric division of subsidiary mother cells or LCSs. Following SC formation, GMCs divided once symmetrically to generate guard cells and then differentiated terminally to form mature stomata. The developmental patterns of long cells, prickle hairs and short cells (phellem cells and silica cells) were also examined. Interestingly, we found that the different developmental stages of stomata and epidermal cells occurred in the similar location of immature leaves of the same phyllotaxis. In addition, two spacing patterns (“one stoma, one long cell” and “one short cell row”) probably exist in rice leaves.     

Application of the biogenetic law to behavioral ontogeny: a test using nest architecture in paper wasps

General principles derived from studies of morphological ontogeny are useful in ethology. Behavioral ontogeny may be interpreted from an holistic view in which a series of behaviors is treated as an ontogeny toward a larger, complex, behavioral product. If the component behaviors are defined broadly, many taxa may be compared to find general principles that are not evident when behaviors are dissected to their smallest recognizable units. Flow charts can illustrate such general ontogenetic sequences in a manner that shows what sorts of modifications have evolved from the general pattern. Certain changes may illustrate forms of ontogenetic evolution that are well known for morphological development, such as addition or embellishment of terminal ontogenetic steps, or compression of ontogeny by acceleration or deletion of early steps. The major modifications in nest construction behavior of 28 genera of paper wasps are presented to test the predictions of the biogenetic rule with respect to character polarity. Cladistic analyses of separate morphological and behavioral data sets show that polarity is accurately inferred with respect to the five major patterns of nest construction in paper wasps.     

The ontogeny of the vascular cambium inGinkgo biloba roots

Observation was made on early ontogeny of vascular cambium in the developing root ofGinkgo biloba L. After completion of root elongation, the vascular meristem gradually acquires cambial characteristics. Strips of the periclinal division of cells in transverse section are observed on the inner side of phloem when the primary xylem and phloem in the stele have been established. The strips are united into a continuous layer between phloem and xylem. In tangenital section, the procambium shows a homogeneous structure, which is initially composed of short cells with transverse end walls and subsequently, of long cells with tapering ends. Then, the procambium is organized into two systems of cells; axial strands of short cells with transverse end walls resulting from the sporadic transverse divisions of long cells, and long cells with tapering ends. Still later, the short cells are divided frequently in a trasverse plane exhibiting one or a few cells in width and several decades of cells in height, while the long cells are elongated. The frequency of transverse divisions of the short cells decreases in subsequent stages. Eventually, the short cells in axial strands are vertically separated from one another by the elongation of neighboring long cells and by the decrease in the frequency of transverse divisions of short cells themselves. Cambial initials occur in two forms; ray initials a few cells in height and one cell in width derived from the short cells, and fusiform initials with tapering ends derived from the long cells.     

LEAF DEVELOPMENT IN DOXANTHA UNGUIS-CATI (BIGNONIACEAE)

Leaf structure in Doxantha unguis-cati is polymorphic. The usual mature compound leaf is composed of two lanceolate leaflets and a terminal tripartite spine-tendril. Leaf primordia are initiated simultaneously in pairs on opposite flanks of the shoot apical meristem by periclinal cell divisions in the third subsurface layer of the peripheral flank meristem. Two leaflet primordia are the first lateral appendages of the compound leaf. Initiation of these leaflet primordia occurs on the adaxial side of a compound leaf primordium 63–70 μm long. Lamina formation is initiated at the base of a leaflet primordium 70–90 μm long and continues acropetally. Mesophyll differentiation occurs in later stages of development of leaflets. The second pair of lateral appendages of the leaf primordium differentiate as prongs of the tendril. Initiation of the second pair of lateral appendages occurs on the adaxial side of a primordium approximately 168 μm long. Acropetal procambialization and vacuolation of cells extend to the apex of tendrils about 112 μm long, restricting the tendril meristem to the adaxial side of the primordium and resulting in curvature of the tendril. The tendril meristem is gradually limited to a more basipetal position as elongation of apical cells continues. Initiatory divisions and early ontogenetic stages of leaflets and tendrils are similar. Their ontogeny differs when the lateral primordia are approximately 70 μm long. Marginal and submarginal initials differentiate within leaflets but not in tendrils. Apical growth of tendrils ceases very early in ontogeny as compared with leaflets.     

Patterns of intraspecific variation through ontogeny: a case study of the Cretaceous nautilid Eutrephoceras dekayi and modern Nautilus pompilius

The magnitude and ontogenetic patterns of intraspecific variation can provide important insights into the evolution and development of organisms. Understanding the intraspecific variation of organisms is also a key to correctly pursuing studies in major fields of palaeontology. However, intraspecific variation has been largely overlooked in ectocochleate cephalopods, particularly nautilids. Furthermore, little is known regarding the evolutionary pattern. Here, we present morphological data for the Cretaceous nautilid Eutrephoceras dekayi (Morton) and the modern nautilid Nautilus pompilius Linnaeus through ontogeny. The data are used to describe conch morphology and to elucidate the evolutionary patterns of intraspecific variation. We discovered a similar overall pattern of growth trajectories and the presence of morphological changes at hatching and maturity in both taxa. We also found that intraspecific variation is higher in earlier ontogeny than in later ontogeny in both taxa. The high variation in earlier ontogeny may imply increased flexibility in changing the timing of developmental events, which probably played an important role in nautilid evolution. We assume that the decrease in variation in later ontogeny reflects developmental constraints. Lastly, we compared the similarity/dissimilarity of ontogenetic patterns of variation between taxa. Results reveal that the similarity/dissimilarity of the ontogenetic pattern differs between E. dekayi and N. pompilius. We conclude that this shift in the ontogenetic pattern of variation may be rooted in changes in the developmental programme of nautilids through time. We propose that studying ontogenetic patterns of intraspecific variation can provide new insights into the evolution and development of organisms.     

Clonal analysis of the Arabidopsis root confirms that position, not lineage, determines cell fate

 The cellular organization of the Arabidopsis thaliana (L.) Heynh. root meristem suggests that a regular pattern of cell divisions occurs in the root tip. Deviations from this pattern of division might be expected to disrupt the organization of cells and tissues in the root. A clonal analysis of the 3-d-old primary root meristem was carried out to determine if there is variability in division patterns, and if so to discover their effect on cellular organization in the root. Clones induced in the seedling meristem largely confirmed the predicted pattern of cell divisions. However, the cellular initials that normally give rise to the different cell files in the root were shown to exhibit some instability. For example, it was calculated that a lateral root cap/epidermal initial is displaced every 13 d. Furthermore, the existence of large marked clones that included more than two adjacent cell layers suggests that intrusive growth followed by cell division may occur at low frequency, perhaps in response to local cell deaths in the meristem. These findings support the view that even in plant organs with stereotypical cell division patterns, positional information is still the key determinant of cell fate. Received: 27 August 1999 / Accepted: 4 December 1999     

Phylogenetic interpretation of ontogenetic change: sorting out the actual and artefactual in an empirical case study of centrarchid fishes

Hypothesized relationships between ontogenetic and phylogenetic change in morphological characters were empirically tested in centrarchid fishes by comparing observed patterns of character development with patterns of character evolution as inferred from a representative phylogenetic hypothesis. This phylogeny was based on 56–61 morphological characters that were polarized by outgroup comparison. Through these comparisons, evolutionary changes in character ontogeny were categorized in one of eight classes (terminal addition, terminal deletion, terminal substitution, non-terminal addition, non-terminal deletion, non-terminal substitution, ontogenetic reversal and substitution). The relative frequencies of each of these classes provided an empirical basis from which assumptions underlying hypothesized relationships between ontogeny and phylogeny were tested. In order to test hypothesized relationships between ontogeny and phylogeny that involve assumptions about the relative frequencies of terminal change (e.g. the use of ontogeny as a homology criterion), two additional phylogenies were generated in which terminal addition and terminal deletion were maximized and minimized for all characters. Character state change interpreted from these phylogenies thus represents the maxima and minima of the frequency range of terminal addition and terminal deletion for the 8.7 × 10³⁶ trees possible for centrarchids. It was found for these data that terminal change accounts for c. 75% of the character state change. This suggests either that early ontogeny is conserved in evolution or that interpretation and classification of evolutionary changes in ontogeny is biased in part by the way that characters are recognized, delimited and coded. It was found that ontogenetic interpretation is influenced by two levels of homology decision: an initial decision involving delimitation of the character (the ontogenetic sequence), and the subsequent recognition of homologous components of developmental sequences. Recognition of phylogenetic homology among individual components of developmental sequences is necessary for interpretation of evolutionary changes in ontogeny as either terminal or non-terminal. If development is the primary criterion applied in recognizing individual homologies among parts of ontogenetic sequences, the only possible interpretation of phylogenetic differences is that of terminal change. If homologies of the components cannot be ascertained, recognition of the homology of the developmental sequence as a whole will result in the interpretation of evolutionary differences as substitutions. Particularly when the objective of a study is to discover how ontogeny has evolved, criteria in addition to ontogeny must be used to recognize homology. Interpretation is also dependent upon delimitation within an ontogenetic sequence. This is in part a function of the way that an investigator ‘sees’ and codes characters. Binary and multistate characters influence interpretation differently and predictably. The use of ontogeny for determining phylogenetic polarity as previously proposed rests on the assumptions that ancestral ontogenies are conserved and that character evolution occurs predominantly through terminal addition. It was found for these data that terminal addition may comprise a maximum of 51.9% of the total character state change. It is concluded that the ontogenetic criterion is not a reliable indicator of phylogenetic polarity. Process and pattern data are collected simultaneously by those engaged in comparative morphological studies of development. The set of alternative explanatory processes is limited in the process of observing development. These form necessary starting points for the research of developmental biologists. Separating ‘empirical’ results from interpretational influences requires awareness of potential biases in the course of character selection, coding and interpretation. Consideration of the interpretational problems involved in identifying and classifying phylogenetic changes in ontogeny leads to a re-evaluation of the purpose, usefulness and information conveyed by the current classification system. It is recommended that alternative classification schemes be pursued.     

Genetic Analysis of Size-Scaling Patterns in the Mouse Mandible

The relationship between multidimensional form of the adult mouse mandible and body size is examined from an ontogenetic perspective. The origin and ontogeny of phenotypic correlations are described in terms of genetic and environmental covariance patterns between adult skeletal morphology and growth in body weight. Different ontogenetic patterns are observed in the genetic correlations, and these can be related to the developmental as well as the functional aspects of mandibular form. The quantitative genetic aspects of craniomandibular growth and morphogenesis are explored, together with an examination of the impact of ontogenetic changes in the genetic variance-covariance structure on morphogenetic integration and evolution by selection.     

Differentiation of germinal and somatic cells in Volvox carteri

Volvox carteri is a spherical alga with a complete division of labor between around 2000 biflagellate somatic cells and 16 asexual reproductive cells (gonidia). It provides an attractive system for studying how a molecular genetic program for cell-autonomous differentiation is encoded within the genome. Three types of genes have been identified as key players in germ-soma differentiation: a set of gls genes that act in the embryo to shift cell-division planes, resulting in asymmetric divisions that set apart the large-small sister-cell pairs; a set of lag genes that act in the large gonidial initials to prevent somatic differentiation; and the regA gene, which acts in the small somatic initials to prevent reproductive development. Somatic-cell-specific expression of regA is controlled by intronic enhancer and silencer elements.     

DEVELOPMENTAL CHANGES IN THE VASCULAR CAMBIUM IN LEITNERIA FLORIDANA

Developmental changes in the vascular cambium of Leitneria floridana, a shrub, were determined primarily by an analysis of the secondary xylem. During the production of the first growth ring of secondary xylem, 37% of the anticlinal divisions in the fusiform initials were lateral, the remaining were oblique. The oblique partition averaged ½ of the length of the dividing initials during this period of growth. Following their origin in anticlinal division, daughter cells elongated at a rapid rate until they were about as long as the mean for all cells, and then most cells elongated at a slow rate. Almost all initials survived during the formation of the inner secondary xylem (growth rings 1–10), and few new rays were formed from fusiform initials. During the production of the outer secondary xylem (growth rings 22–26), lateral divisions accounted for less than 5% of all anticlinal divisions. The oblique partition averaged only ¼ of the length of the dividing cells during this period, although the mean length of dividing initials was relatively constant throughout secondary growth. About 20% of the initials studied during the deposition of the outer secondary xylem disappeared from the cambium, and many others were transformed into ray initials. The findings are discussed in relation to the developmental changes in the vascular cambium in plants of different habits.     

Confocal Microscopy Study of <Emphasis Type="Italic">Arabidopsis</Emphasis> Embryogenesis Using GFP:mTn

Embryogenesis in transgenic Arabidopsis plants with GFP:mTn, a chimeric fusion of soluble shifted green fluorescent protein and a mouse actin binding domain, was studied. Confocal laser scanning microscopy was used to determine patterns of formation and cellular responses during asymmetric cell division. Before such cells divide, the nucleus moves to the position where new cell walls are to be formed. The apical–basal axis of the embryo develops mainly at the zygote to octant stage, and these events are associated with asymmetric divisions of the zygote and hypophyseal cells. Formation of the radial axis is established from the dermatogen to the globular-stage embryo via tangential cell division within the upper tiers. Bilateral symmetry of the embryo primarily happens at the triangular stage through zig-zag cell divisions of initials of the cotyledonary primordia. All stages of embryogenesis are described in detail here.     

Timing of morphological and histological development in premeiotic anthers of Nicotiana tabacum cv. Xanthi (Solanaceae)

The tobacco stamen has been the object of many developmental studies, and the organ has more recently become a model for molecular genetic studies of anther differentiation. However, the spatial and temporal details of cellular differentiation of early anther development have never been thoroughly characterized. In the present study, the age of 15 tobacco flowers from plants grown under constant light and temperature was estimated using growth analysis. Prior to tissue fixation for light microscopy, moulds of stamen and anther primordia were made with a dental impression polymer so morphological and histological observations could be made on each tissue sample. Flower ages spanned an 8-d interval during which petal and stamen initiation occurred, and sporogenous cells reached the leptonema stage of meiosis. The initial development of the tetrasporangiate anther shape largely preceded periclinal division of archesporial initials. Anatomically, periclinal divisions in the hypodermal ∗∗∗(l₂) layer were observed before archesporial initials began to divide. These data indicate differences in the cellular basis of tobacco anther development compared to earlier clonal analyses of Datura. The pattern of mitotic cell division associated with microsporangial development suggested modal peaks in division over time. The ability to estimate developmental time in the tobacco anther has implications for future studies directed at understanding mechanisms of anther evolution via heterochrony.     

Autoreproductive cells and plant meristem construction: The case of the tomato cap meristem

Summary Root apical meristems are composed of two zones in which either formative or proliferative cell divisions occur. Within the formative zone, autoreproductive initial cells (a-cells) occupy distinctive locations. By means of graph-L-systems, the behavior of one such type of a-cells has been investigated, with particular reference to root caps within the developing primordia of lateral roots ofLycopersicon esculentum cultivated in vitro. Here, the a-cells constitute the protoderm initials, cells which are found also in the root cap of many angiosperm species. A set of cuboidal (i.e., six-sided) acells develops early in the ontogeny of a lateral-root primordium. Then, according to both anatomical observations and theoretical simulations obtained by the application of graph-L-systems, sequential production of descendents from each a-cell leads to the formation of a new autoreproductive cell (a), a cap columella initial (c), and two mother cells (e and f) whose respective descendents differentiate as root epidermis and cap flank cells. In this graph-L-system, there is specification of the location of sister cells with respect to the three orthogonal directions of a cuboidal. In the early stage of root cap formation, only a few rounds of these formative cell divisions by each a-cell and its four types of descendents are required to provide the basic set of cells necessary for full cap development. After the lateral root emerges from the parent root, there may be a temporary cessation of the formative divisions of the a-cells which give rise to columella initials. Columella production is then supported entirely by its own independent set of autoreproductive c-initials. At the same time, division of the autoreproductive protoderm initial cell is directed towards maintaining the cap flank and the epidermal cell files. The regulation of the types of formative division by the a-cell may be represented by means of a division counter which may be specific for a given species.Dedicated to Professor Brian E. S. Gunning on the occasion of his 65th birthday