Developmental mechanisms in heterospory. II. Evidence for pinocytosis in the microspores of Selaginella

At a stage in ontogeny while they are still held together in tetrads, but before the formation of the exine, the microspores of Selaginella brooksii Hieron. show features of the cell surface which suggest that material is being taken up by pinocytosis. These features, which are confined to the proximal face of the spore, are: (1) cytoplasmic fringes which arise near, arch over and enclose membrane-bound particles on the cell surface, (2) invaginations of the plasma membrane which form smooth-surfaced vesicles, and (3) invaginations of the plasma membrane to form coated vesicles. The membranes which limit all three kinds of vesicle are asymmetrical. Sections that cut the surface of the microspore tangentially at or in the vicinity of this surface activity show a hexagonal lattice which is a surface specialization possibly connected with pinocytosis. There are indications that the pinocytosed material is digested by lysosomal enzymes; myelin-like residual bodies are formed which migrate to the periphery of the cell. These observations are discussed in relation to the nutritional explanation of heterospory in the pteridophytes.     

Developmental mechanisms in heterospory. III. The plastid cycle during megasporogenesis in Isoetes.

The megasporocyte of Isoetes englemanni at the leptotene-zygotene interval of meiosis contains 4 disk-shaped proplastids about 12 mum in diameter. The disposition of these organelles in the cell is such that each of the four megaspores delimited during cytokinesis contains a single proplastid. During prophase and following their incorporation into the spores, the proplastids are undergoing fission by budding. The buds are first discernible as low surface evaginations which contain a complement of granular somal material, some wefts of tubular membrane and osmiophilic globuli, in addition to a number of vesicles derived by invagination from the inner membrane of the proplastid envelope. As the evaginations emerge they enlarge and the link with the parent body is reduced to a narrow channel. At this stage one or more of the vesicles derived from the proplastid envelope comes into register with the lumen of the channel. One vesicle is transported into the lumen, elongating as it passes through. The passage of the vesicle into the channel destroys the connexion between the matrix of the evagination and the stroma of the proplastid. The occurrence in the cytoplasm around the proplastid of bodies not connected to the proplastid, but identical in structure to the evaginations and carrying a membranous tail suggests that the evaginations are released by abscission of the channel close to the surface of the parent body. After release the bodies undergo division by constriction. Regression of the tail follows division in those bodies which are regular in outline and in which the matrix is ultrastructurally similar to the stroma of the parent organelle. The process does not seem to occur in co-existing forms which have assumed an irregular outline and have a less-opque matrix. The more mature megaspore of Isoetes contains proplastids up to 4 mum in greatest dimension. The stroma in these is dense and granular and contains membrane-bound vesicles, osmiophilic globuli, starch granules and wefts of tubular membrane. There is no evidence that the large budding organelle persists to this later stage in development. The resemblance of the plastids in the more mature megaspore to the bodies produced by evagination earlier in development suggests a common identity. The observations and interpretations lead to the proposition that the plastids in Isoetes englemanni are autonomous. This situation contrasts with the one described for another heterosporous haploid dioecious pteridophyte, Marsilea vestita, where nucleocytoplasmic interaction has been interpreted as the de novo creation of plastids and mitochondria following the elimination by autophagy of the organelles inherited at meiosis. It is suggested that an explanation to account for the 2 different mechanisms might be sought in regard to the degree of developmental success enjoyed by the individual megaspores in the 2 plants. In Isoetes all 4 megaspores of every tetrad survive and develop, while in Marsilea the mature megasporangium contains a single functional megaspore.     

Cellular differentiation of heterospory inSelaginella

Summary Selaginella pilijera consistently displays two rows of microsporangia and two rows of megasporangia. It is therefore possible to detect in longitudinal sections of strobili at least three significant differences in development between both types of sporangia prior to meiosis: size of young sporangia, abortion or development of sporocytes based an RNA staining, and presence or absence of callose walls around sporocytes. The functional significance of these differences is discussed in relation to the heterosporous habit and higher plant sporogenesis.     

Developmental mechanisms of gyrification

Folding of the cerebral cortex is a fundamental milestone of mammalian brain evolution associated with dramatic increases in size and complexity. Cortex folding takes place during embryonic and perinatal development and is important to optimize the functional organization and wiring of the brain, while allowing fitting a large cortex in a limited cranial volume. Cortex growth and folding are the result of complex cellular and mechanical processes that involve neural stem progenitor cells and their lineages, the migration and differentiation of neurons, and the genetic programs that regulate and fine-tune these processes. Here, we provide an updated overview of the most significant and recent advances in our understanding of developmental mechanisms regulating cortical gyrification.     

The adaptive value of heterospory: Evidence from Selaginella

Heterospory was a pivotal evolutionary innovation for land plants, but it has never been clear why it evolved. We used the geographic distributions of 114 species of the heterosporous lycophyte Selaginella to explore the functional ecology of microspore and megaspore size, traits that would be correlated with many aspects of a species’ regeneration niche. We characterized habitats at a global scale using leaf area index (LAI), a measure of foliage density and thus shading, and net primary productivity (NPP), a measure of growth potential. Microspore size tends to decrease as habitat LAI and NPP increase, a trend that could be related to desiccation resistance or to filtration of wind‐borne particles by leaf surfaces. Megaspore size tends to increase among species that inhabit regions of high LAI, but there is an important interaction with NPP. This geographical pattern suggests that larger megaspores provide an establishment advantage in shaded habitats, although in open habitats, where light is less limiting, higher productivity of the environment seems to give an advantage to species with smaller megaspores. These results support previous theoretical arguments that heterospory was originally an adaptation to the increasing height and density of Devonian vegetative canopies that accompanied the diversification of vascular plants with leaves.     

Heterochrony: Developmental mechanisms and evolutionary results

The concept of heterochrony, that the relative timing of ontogenetic events can shift during evolution, has been a major paradigm for understanding the role of developmental processes in evolution. In this paper we consider heterochrony from the perspective of developmental biology. Our objective is to redefine heterochrony more broadly so that the concept becomes readily applicable to the evolution of the full range of ontogenetic processes, from embryogenesis through the adult. Throughout, we stress the importance of considering heterochrony from a hierarchical perspective. Thus, we recognize that a heterochronic change at one level of organization may be the result of non-heterochronic events at an underlying level. As such, heterochrony must be studied using a combination of genetic, molecular, cellular, and morphological approaches.     

Developmental mechanisms of threshold evolution in a polyphenic beetle

Polyphenic development is thought to play a pivotal role in the origin of morphological novelties. However, little is known about how polyphenisms evolve in natural populations, the developmental mechanisms that may mediate such evolution, and the consequences of such modification for patterns of morphological variation. Here we examine the developmental mechanisms of polyphenism evolution in highly divergent natural populations of the dung beetle, Onthophagus taurus. Males of this species express two alternative morphologies in response to larval feeding conditions. Favorable conditions cause males to grow larger than a threshold body size and to develop a pair of horns on their heads. Males that encounter relatively poor conditions during larval life do not reach this threshold size and remain hornless. Exotic populations of O. taurus have diverged dramatically in body size thresholds in less than 40 years since introduction to new habitats, resulting in the expression of highly divergent and novel horn length-body size scaling relationships in these populations. Here we show that larvae of populations that have evolved a larger threshold body size (1) have to accumulate greater mass to become competent to express the horned morph, (2) require more time to complete the final instar, (3) are less sensitive to the juvenile hormone (JH) analogue methoprene, and (4) exhibit a delay in the sensitive period for methoprene relative to other developmental events. JH has been shown previously to control horn expression in this species. Our results show that threshold evolution may be mediated via changes in the degree and timing of sensitivity to JH and may result in correlated changes in the dynamics and duration of larval development. Strain-specific differences in JH sensitivity have previously been demonstrated in other insects. However, to the best of our knowledge this is the first demonstration that changes in the timing of the sensitive period for JH may play an equally important role in the evolution of novel thresholds. We discuss our findings in the context of the developmental regulatory mechanisms that underlie polyphenic development and use our results to explore the consequences of, and constraints on, polyphenism evolution in nature.     

Developmental mechanisms for the generation of telencephalic interneurons

Interneurons, which release the neurotransmitter γ-aminobutyric acid (GABA), are the major inhibitory cells of the central nervous system (CNS). Despite comprising only 20-30% of the cerebral cortical neuronal population, these cells play an essential and powerful role in modulating the electrical activity of the excitatory pyramidal cells onto which they synapse. Although interneurons are present in all regions of the mature telencephalon, during embryogenesis these cells are generated in specific compartments of the ventral (subpallial) telencephalon known as ganglionic eminences. To reach their final destinations in the mature brain, immature interneurons migrate from the ganglionic eminences to developing telencephalic structures that are both near and far from their site of origin. The specification and migration of these cells is a complex but precisely orchestrated process that is regulated by a combination of intrinsic and extrinsic signals. The final outcome of which is the wiring together of excitatory and inhibitory neurons that were born in separate regions of the developing telencephalon. Disruption of any aspect of this sequence of events during development, either from an environmental insult or due to genetic mutations, can have devastating consequences on normal brain function.     

Developmental mechanisms underlying tooth patterning in continuously replacing osteichthyan dentitions

The dentition of osteichthyans presents an astonishing diversity with regard to the distribution of teeth in the oral cavity, tooth numbers, arrangements, shapes, and sizes. Taking examples from three unrelated teleosts--the most speciose group of osteichthyans--and from the literature, this study explores how the initial tooth pattern is set up, and how this relates to the establishment and maintenance (or modification) of the tooth replacement pattern. In teleosts, first-generation teeth (the very first teeth in ontogeny to develop at a particular locus) are commonly initiated in adjacent or in alternate (odd and even) positions. The mechanisms responsible for these divergent developmental patterns remain to be elucidated, in particular, whether they reflect a field or local type of control. However, patterns of adjacent or alternate tooth initiation, set up by the first-generation teeth, can easily turn into replacement patterns where new teeth are initiated simultaneously every second, or even every third position, by synchronizing the formation of new first-generation teeth to the formation of replacement teeth at older loci. Our observations suggest that, once established, the replacement pattern appears to be maintained, as a kind of "default" state. Variations and modifications in this pattern are nevertheless common and suggest that tooth replacement is under local control, exerted at the level of the initiation of replacement teeth. Further studies are needed to test the hypothesis that regular replacement patterns are more frequent in association with the plesiomorphic condition of extramedullary replacement (replacement on the surface of the dentigerous bone) and more rare in the derived condition of intramedullary replacement (replacement within the medullary cavity of the dentigerous bone).     

Developmental mechanisms that regulate retinal ganglion cell dendritic morphology

One of the fundamental features of retinal ganglion cells (RGCs) is that dendrites of individual RGCs are confined to one or a few narrow strata within the inner plexiform layer (IPL), and each RGC synapses only with a small group of presynaptic bipolar and amacrine cells with axons/dendrites ramified in the same strata to process distinct visual features. The underlying mechanisms which control the development of this laminar-restricted distribution pattern of RGC dendrites have been extensively studied, and it is still an open question whether the dendritic pattern of RGCs is determined by molecular cues or by activity-dependent refinement. Accumulating evidence suggests that both molecular cues and activity-dependent refinement might regulate RGC dendrites in a cell subtype-specific manner. However, identification of morphological subtypes of RGCs before they have achieved their mature dendritic pattern is a major challenge in the study of RGC dendritic development. This problem is now being circumvented through the use of molecular markers in genetically engineered mouse lines to identify RGC subsets early during development. Another unanswered fundamental question in the study of activity-dependent refinement of RGC dendrites is how changes in synaptic activity lead to the changes in dendritic morphology. Recent studies have started to shed light on the molecular basis of activity-dependent dendritic refinement of RGCs by showing that some molecular cascades control the cytoskeleton reorganization of RGCs.