A developmental morphologist's perspective on plasticity

This series of essays addresses plasticity from the perspective of developmental morphology. The first essay deals with the problem of distinguishing between plasticity and other types of ontogenetic variation. In a temporally varying environment, morphological plasticity may be expressed as the production of a succession of different metamers. However, even in a constant environment, plant metamers can vary dramatically, a phenomenon known as heteroblasty. Because heteroblasty and plasticity can yield similar patterns of ontogenetic variation, the two are often confounded in analyses of developmental plasticity. The second essay discusses the integration of plant phenotypic responses and finds that the evidence for integration is equivocal. The third section shows that developmental properties can constrain the expression of morphological plasticity. Developmental lags and the epiphenotype problem are particularly important features for analyses of the evolution and expression of plasticity. Finally, in answer to the question of strategies for studying plasticity, I emphasize the need for research at multiple levels and for the inclusion of a historical or phylogenetic perspective.     

Leech segmentation: A molecular perspective

A variety of leech homeobox genes have been identified by homology with genes that are known to bring about the regionalization and segmentation of the anteroposterior body axis in other organisms. Embryonic expression patterns suggest a number of interphyletic similarities in the way that these genes are utilized. However, several interesting differences have also been observed. In particular, transplantation experiments in the leech embryo have shown that axially aligned patterns of homeobox gene expression are not specified by a global pattern of positional cues. Rather, the leech independently establishes anteroposterior patterns of gene expression in each of five discrete stem cell lineages, and these patterns are brought into their final alignment through a process of morphogenetic assembly.     

Evolutionary developmental biology and vertebrate head segmentation: A perspective from developmental constraint

Summary The question of vertebrate head segmentation has become one of the central issues in Evolutionary Developmental Biology. Beginning as a theory based in comparative anatomy, a segmental theory of the head has been adopted and further developed by comparative embryologists. With the use of molecular and cellular biology, and in particular analyses of the Hox gene complex, the question has been addressed at new levels, but it remains unresolved. In this review, vertebrate head segmentation is reevaluated, by introducing findings from experimental embryology and evolutionary biology. Developmental biology has shown that pattern is generated through hierarchically organized and causally linked series of events. The question of head segmentation can be viewed as a question of generative constraint, that is whether segmentation in the head is imposed by underlying segmental patterns, as it is in the trunk. In this respect, amphioxus appears to be segmented along the entire anteroposterior axis, with myotomes and peripheral nerves repeating with the same rhythm (somitomerism). Similarly, in the vertebrate trunk, the segmental patterns shared by myotomes, peripheral nerves and vertebrae are derived from the somites. However, in the head of vertebrates there is no such mesodermal pattern, although neuromerism and branchiomerism do indicate the presence of constraints derived from rhombomeres and pharyngeal pouches, respectively. These data fit better the concept of dual metamerism of the vertebrate body proposed by Romer (1972), than the traditional head cavity-based segmental model by Goodrich (1930).     

A life-history perspective on short- and long-term consequences of compensatory growth

Compensatory or catch-up growth (CG) is widely observed following periods of resource deprivation. Because of this commonness, it is generally assumed that compensatory growth is adaptive, but most theory to date has explicitly ignored considerations of fitness. Following a period of deprivation, when resources become plentiful again, individuals may not respond at all and continue on a "normal" trajectory from a smaller size at age, may exhibit faster-than-normal growth immediately following the end of the period, or may adopt a growth strategy that involves faster-than-normal growth at some later time. Compensating individuals may also overtake control individuals who have been growing normally throughout. We hypothesize that the key to understanding CG is that growth leads to the accumulation of damage at the cellular level that is expressed (and thus must be modeled) at the level of the organism. We show that a life-history model incorporating the mortality consequences of both size and damage provides a framework for understanding compensatory growth. We use the theory to classify physiological and life-history characteristics for which CG is predicted to be the optimal response to deprivation.     

Anterior-posterior pattern formation: an evolutionary perspective on genes specifying terminal domains

The Drosophila anterior-posterior pattern genes of the terminal class, particularly the tailless gene, affect structures derived from the acron and the tail region of the embryo. These domains correspond in position and function to asegmental domains at the termini of annelids and more primitive insect embryos. This suggests that terminal genes in Drosophila may have originated in an ancestor common to both annelids and arthropods, and thus that the specification of termini in these metameric organisms is an ancient, evolutionarily conserved process.     

Microbial growth on hydrocarbons: terminal branching inhibits biodegradation

A variety of octane-utilizing bacteria and fungi were screened for growth on some terminally branched dimethyloctane derivatives to explore the effects of iso- and anteiso-termini on the biodegradability of such hydrocarbons. Of 27 microbial strains tested, only 9 were found to use any of the branched hydrocarbons tested as a sole carbon source, and then only those hydrocarbons containing at least one iso-terminus were susceptible to degradation. Anteiso-or isopropenyl termini prevented biodegradation. None of the hydrocarbonoclastic yeasts tested was able to utilize branched-hydrocarbon growth sustrates. In the case of pseudomonads containing the OCT plasmid, whole-cell oxidation of n-octane was poorly induced by terminally branched dimethyloctanes. In the presence of a gratuitous inducer of the octane-oxidizing enzymes, the iso-branched 2,7-dimethyloctane was slowly oxidized by whole cells, whereas the anteiso-branched 3,6-dimethyloctane was not oxidized at all. This microbial sampling dramatically illustrated the deleterious effect of alkyl branching, especially anteiso-terminal branching, on the biodegradation of hydrocarbons.     

The evolutionary history of crustacean segmentation: a fossil-based perspective

The evolution of segmentation in Crustacea, that is, the formation of sclerotized and jointed body somites and arrangement of somites into tagmata, is viewed in light of historical traits and functional constraints. The set of Early to Late Cambrian 'Orsten' arthropods have informed our current views of crustacean evolution considerably. These three-dimensionally preserved fossils document ancient morphologies, as opposed to purely hypothetical models and, because of the unusual preservation of larval stages, provide us with unparalleled insight into the morphogenesis of body somites and their structural equipment. The variety of evolutionary levels represented in the 'Orsten' including lobopodians, tardigrades, and pentastomids also allows phylogenetic interpretations far beyond the Crustacea. The 'Orsten' evidence and data from representatives of the Lower Cambrian Chengjiang biota in southwestern China, including phylogenetically earlier forms, form the major source of our morphology-based review of structural and functional developments that led toward the Crustacea. The principal strategy of arthropods is the simultaneous development of head somites, as expressed in a basal "head larva," and a successive addition of postcephalic somites from a preterminal budding zone with progressive maturation of metameric structures. This can be recognized in the developmental patterns of extant and fossil representatives of several euarthropod taxa, particularly crustaceans, trilobites, and chelicerates (at least basally). The development of these taxa points to an early somite-poor and free-living hatching stage. Embryonic development to a late stage within an egg, as occurring in recent onychophorans and certain in-group euarthropods, is regarded as achieved several times convergently.     

Orienting axon growth: spinal nerve segmentation and surround-repulsion

The study of spinal nerve trajectories in higher vertebrate embryos has revealed an inherent polarity within somites along the antero-posterior axis, and provides a simple system in which to study the factors that influence axon pathfinding. We argue that the orientation of spinal axons is determined by the simultaneous operation of two distinct guidance mechanisms, contact repulsion and chemorepulsion. Motor and sensory axons traverse the anterior half of each somite because they are excluded by contact repulsion from the posterior half-somite, and the molecular nature of several candidate contact repellents is reviewed. In contrast, we find that the dorsoventral trajectory of primary sensory axons is oriented by diffusible repellents originating from the notochord medially and dermamyotome laterally. In this system, therefore, repulsion by surrounding tissues ('surround-repulsion') is the main force directing axon growth in three dimensions.     

Microbial growth on hydrocarbons: terminal branching inhibits biodegradation.

A variety of octane-utilizing bacteria and fungi were screened for growth on some terminally branched dimethyloctane derivatives to explore the effects of iso- and anteiso-termini on the biodegradability of such hydrocarbons. Of 27 microbial strains tested, only 9 were found to use any of the branched hydrocarbons tested as a sole carbon source, and then only those hydrocarbons containing at least one iso-terminus were susceptible to degradation. Anteiso-or isopropenyl termini prevented biodegradation. None of the hydrocarbonoclastic yeasts tested was able to utilize branched-hydrocarbon growth sustrates. In the case of pseudomonads containing the OCT plasmid, whole-cell oxidation of n-octane was poorly induced by terminally branched dimethyloctanes. In the presence of a gratuitous inducer of the octane-oxidizing enzymes, the iso-branched 2,7-dimethyloctane was slowly oxidized by whole cells, whereas the anteiso-branched 3,6-dimethyloctane was not oxidized at all. This microbial sampling dramatically illustrated the deleterious effect of alkyl branching, especially anteiso-terminal branching, on the biodegradation of hydrocarbons.     

NGF and the local control of nerve terminal growth

It is generally believed that the mechanism of action of neurotrophic factors involves uptake of neurotrophic factor by nerve terminals and retrograde transport through the axon and back to the cell body where the factor exerts its neurotrophic effect. This view originated with the observation almost 20 years ago that nerve growth factor (NGF) is retrogradely transported by sympathetic axons, arriving intact at the neuronal cell bodies in sympathetic ganglia. However, experiments using compartmented cultures of rat sympathetic neurons have shown that neurite growth is a local response of neurites to NGF locally applied to them which does not directly involve mechanisms in the cell body. Recently, several NGF-related neurotrophins have been identified, and several unrelated molecules have been shown to act as neurotrophic or differentiation factors for a variety of types of neurons in the peripheral and central nervous systems. It has become clear that knowledge of the mechanisms of action of these factors will be crucial to understanding neurodegenerative diseases and the development of treatments as well as the means to repair or minimize neuronal damage after spinal injury. The concepts derived from work with NGF suggest that the site of exposure of a neuron to a neurotrophic factor is important in determining its response. 1994 John Wiley & Sons, Inc.     

A perspective on Q-cycles

An examination is made of both the Q-cycle andb-cycle formulations of electron transfer and energy conservation in the cytochromebc ₁ complex. A working hypothesis for the complex is presented, based upon the Q-cycle notion of vectorial reaction sites, but incorporating theb-cycle feature of semiquinone movement between these sites.     

A perspective on inversin

Over the past 5 years, there has been increasing evidence for the role of primary (9+0) cilia in renal physiology and in establishing the left-right axis. The cilia in the renal tract are immotile and thought to have a sensory function. Cilia at the murine embryonic node have a vortical movement that sets up a leftward flow. Inversin, the protein defective in the inv mouse and in patients with type-2 nephronophthisis, localizes to both renal and node primary cilia. However, we present evidence that it is also expressed before the node forms and that its subcellular localization in renal tubular cells is not confined to the cilia. Its role in both the pathway determining left-right axis and renal function remains to be elucidated.     

Notch-mediated segmentation and growth control of the Drosophila leg.

The possession of segmented appendages is a defining characteristic of the arthropods. By analyzing both loss-of-function and ectopic expression experiments, we show that the Notch signaling pathway plays a fundamental role in the segmentation and growth of the Drosophila leg. Local activation of Notch is necessary and sufficient to promote the formation of joints between segments. This segmentation process requires the participation of the Notch ligands, Serrate and Delta, as well as Fringe. These three proteins are each expressed in the developing leg and antennal imaginal discs in a segmentally repeated pattern that is regulated downstream of the action of Wingless and Decapentaplegic. Our studies further show that Notch activation is both necessary and sufficient to promote leg growth. We also identify target genes regulated both positively and negatively downstream of Notch signaling that are required for normal leg development. Together, these observations outline a regulatory hierarchy for the segmentation and growth of the leg. The Notch pathway is also deployed for segmentation during vertebrate somitogenesis, which raises the possibility of a common origin for the segmentation of these distinct tissues.     

Growth factors and gangliosides: A possible new perspective in neuronal growth control

For many permanent cell lines the transition from a growing (P) to a resting (R) state is reversibly controlled by growth factors present in serum. This P-to-R transition was studied in a neuronal cell line (B 104) with respect to the action of serum, dibutyryl cyclic AMP (DBcAMP), gangliosides, and a glioma cell-produced growth factor GGF. In this cell system gangliosides seem to act as differentiation and survival factors. The kinetics of uptake of radioactively labeled gangliosides and survival experiments both support the idea of the stable incorporation of exogenously added gangliosides into the cells. Based on the experimental evidence a new model of cell development is proposed. Thus in addition to the R or G₀ state, which in this cell system is rather unstable and probably regulated by cyclic nucleotides, we postulate a differentiated D state, which is controlled by gangliosides and which is characterized by its stability (survival time). This D compartment seems to be closer to the in vivo differentiated neuron than does the R or P state. The possible mechanisms for the action of gangliosides are discussed.     

The relationship between epidermal growth factor receptors and the terminal differentiation of A431 carcinoma cells

Escherichia coli harboring the gene coding for human interleukin-2 (IL-2) produced methionyl IL-2 (Met-IL-2) having an additional methionine residue at the amino terminus as well as IL-2 starting with the amino terminal alanine. IL-2 and Met-IL-2 were copurified from a cell-free extract. It was difficult to separate these two molecular species from each other because of the similarities of their physico-chemical characteristics. We found that the isoelectric points of IL-2 and Met-IL-2 were slightly but significantly different and succeeded in separating these two molecular species by utilizing the difference of their isoelectric points. The isoelectric points of IL-2 and Met-IL-2 thus obtained were determined to be 7.7 and 7.5, respectively. The in vitro specific activities of these two species were the same and similar to that of natural human IL-2 derived from peripheral blood lymphocytes.