Modulation of cell cycle control during oocyte‐to‐embryo transitions

Ex ovo omnia—all animals come from eggs—this statement made in 1651 by the English physician William Harvey marks a seminal break with the doctrine that all essential characteristics of offspring are contributed by their fathers, while mothers contribute only a material substrate. More than 360 years later, we now have a comprehensive understanding of how haploid gametes are generated during meiosis to allow the formation of diploid offspring when sperm and egg cells fuse. In most species, immature oocytes are arrested in prophase I and this arrest is maintained for few days (fruit flies) or for decades (humans). After completion of the first meiotic division, most vertebrate eggs arrest again at metaphase of meiosis II. Upon fertilization, this second meiotic arrest point is released and embryos enter highly specialized early embryonic divisions. In this review, we discuss how the standard somatic cell cycle is modulated to meet the specific requirements of different developmental stages. Specifically, we focus on cell cycle regulation in mature vertebrate eggs arrested at metaphase II (MII‐arrest), the first mitotic cell cycle, and early embryonic divisions.     

Remodeling of peripheral nerve ensheathment during the larval‐to‐adult transition in Drosophila

Over the course of a 4‐day period of metamorphosis, the Drosophila larval nervous system is remodeled to prepare for adult‐specific behaviors. One example is the reorganization of peripheral nerves in the abdomen, where five pairs of abdominal nerves (A4–A8) fuse to form the terminal nerve trunk. This reorganization is associated with selective remodeling of four layers that ensheath each peripheral nerve. The neural lamella (NL), is the first to dismantle; its breakdown is initiated by 6 hours after puparium formation, and is completely removed by the end of the first day. This layer begins to re‐appear on the third day of metamorphosis. Perineurial glial (PG) cells situated just underneath the NL, undergo significant proliferation on the first day of metamorphosis, and at that stage contribute to 95% of the glial cell population. Cells of the two inner layers, Sub‐Perineurial Glia (SPG) and Wrapping Glia (WG) increase in number on the second half of metamorphosis. Induction of cell death in perineurial glia via the cell death gene reaper and the Diptheria toxin (DT‐1) gene, results in abnormal bundling of the peripheral nerves, suggesting that perineurial glial cells play a role in the process. A significant number of animals fail to eclose in both reaper and DT‐1 targeted animals, suggesting that disruption of PG also impacts eclosion behavior. The studies will help to establish the groundwork for further work on cellular and molecular processes that underlie the co‐ordinated remodeling of glia and the peripheral nerves they ensheath. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 1144–1160, 2017     

Morphological and histological changes of dermal scales during the fish‐to‐tetrapod transition

Witzmann F. (2011). Morphological and histological changes of dermal scales during the fish‐to‐tetrapod transition. —Acta Zoologica (Stockholm) 92 : 281–302. The gastral scales of limbed tetrapodomorphs evolved from the ‘elpistostegid’‐type of scale by an enlargement and differentiation of the articulation facets and a shortening and broadening of the keel. These changes caused a tighter connection between gastral scales within a scale row and a greater overlap between the rows. Dorsal round scales of limbed tetrapodomorphs developed from a gastral scale‐type by an alteration of the ontogenetic pathway. The posterolateral direction of scale rows in ‘elpistostegids’ was retained in the gastral scalation of most limbed tetrapodomorphs, whereas the arrangement of round dorsal scales is modified to a transverse orientation. Both gastral and dorsal scales of limbed tetrapodomorphs consist solely of parallel‐fibred bone with circumferential growth marks. The proportionally larger overlap surfaces of gastral scales and their mode of articulation in the ventral midline indicate that the body of limbed tetrapodomorphs might have been more flexible than that of their finned relatives. The alteration of dermal scales was one of the most rapid morphological changes during the fish‐to‐tetrapod transition. Once established, gastral and dorsal scales were retained as a conservative character in different lineages of basal tetrapods, in both the amphibian and the amniote lineages.     

The rubber‐to‐glass transition in high sugar agarose systems

The small and large deformation properties of agarose in the presence of high levels of sugar were investigated. Mixtures can be described as lightly cross‐linked rubbers, which undergo vitrification upon cooling. The combined Williams–Landel–Ferry (WLF)/free volume framework was used to derive the glass transition temperature, the fractional free volume, and the thermal expansion coefficient of the glass. Sucrose‐rich cosolute crystallizes, but addition of the polymer encourages intermolecular interactions, which transform the mixture into a high viscosity glass. The mechanical properties of glucose syrup, a noncrystalline sugar, follow WLF behavior in the glass transition region and revert to an Arrhenius‐type prediction in the glassy state. Measurements on sugar samples and agarose–sugar mixtures were resolved into a basic function of temperature alone and a basic function of frequency (time) alone. The former traces the energetic cost of vitrification, which increases sharply with decreasing temperature. The latter, at long time scales, is governed by the infinite molecular weight of the agarose network. In the region of short times, the effect of free volume is active regardless of the sample composition. © 1999 John Wiley & Sons, Inc. Biopoly 49: 267–275, 1999     

The maternal‐to‐zygotic transition: An asynchronous split

The early cell cycles of preimplantation embryo development are unique in the scheme of mitotic cell proliferation as cell division is not coupled to cell growth, leading to a halving of blastomere volume with each cleavage event. Among the early mouse embryonic divisions, the fi rst two are particularly different, lasting almost twice as long as subsequent divisions. The third cell cycle is marked by the transition of a four‐cell embryo into an eight‐cell embryo, and represents the fi rst complete cell cycle occurring after activation of the zygotic genome. The G2/M phase of the third cell cycle is highly variable, lasting between 2–5 hours, and heterogeneity between blastomeres within the same embryo may occur as a part of normal development. The embryo in this image is actively undergoing cleavage from the four‐ to the eight‐cell stage, and blastomeres are captured in multiple phases of the cell cycle, as visualized by chromatin structure (DNA, blue) and microtubule staining (α‐tubulin, green). Two blastomeres sit in interphase with decondensed chromatin masses and a mesh‐like microtubule network, while the remaining blastomeres are actively undergoing mitosis. Of the latter, one is in metaphase, one in early anaphase, and the last in late anaphase. All together, the diversity in cell cycle stages reveals the inherit asynchrony existent within individual blastomeres of a cleavage stage embryo. Mol. Reprod. Dev. 80: 1–1, 2012. © 2012 Wiley Periodicals, Inc.     

Emigration behavior and molting during the sea‐to‐land transition of terrestrial hermit crabs under laboratory conditions

Terrestrial hermit crabs in the family Coenobitidae (genera Coenobita and Birgus) must migrate onto land after completing a pelagic larval stage in the ocean. Better knowledge of emigration behavior would assist in the conservation and management of coenobitid populations by helping identify and protect the habitats they need to complete their life cycles. We cultured laboratory‐born individuals of five coenobitid species (Coenobita cavipes, C. purpureus, C. rugosus, C. violascens, and Birgus latro) from megalopae to early juveniles (first, second, and/or third crabs) in vessels containing seawater and a hard substrate, and analyzed their behavior and molting in conjunction with our published data for C. brevimanus. Our results confirm that the coenobitids migrated from sea to land at the megalopal stage. Megalopae and early juveniles tended to select shells based on their body size. Inland‐dwelling coenobitids, such as C. brevimanus, C. cavipes, and B. latro, had a longer duration from landing to first molt and had a prolonged first crab intermolt period compared with those of the beach‐dwelling coenobitids C. purpureus, C. rugosus, and C. violascens, probably because of the adaptive traits for migrating to inland habitats. Little burrowing behavior was observed by megalopae of B. latro, but they had a strong tendency to be cryptic under shelters. Additionally, megalopae and early juveniles of Coenobita spp. created and utilized burrows somewhat differently. Our results suggest that coenobitids require specific microhabitats for completing their early life stages in the wild. In particular, megalopae of B. latro may need structurally complex refuges to migrate from the sea.     

Light‐induced stabilization of ACS contributes to hypocotyl elongation during the dark‐to‐light transition in Arabidopsis seedlings

Hypocotyl growth during seedling emergence is a crucial developmental transition influenced by light and phytohormones such as ethylene. Ethylene and light antagonistically control hypocotyl growth in either continuous light or darkness. However, how ethylene and light regulate hypocotyl growth, including seedling emergence, during the dark‐to‐light transition remains elusive. Here, we show that ethylene and light cooperatively stimulate a transient increase in hypocotyl growth during the dark‐to‐light transition via the light‐mediated stabilization of 1‐aminocyclopropane‐1‐carboxylic acid (ACC) synthases (ACSs), the rate‐limiting enzymes in ethylene biosynthesis. We found that, in contrast to the known inhibitory role of light in hypocotyl growth, light treatment transiently increases hypocotyl growth in wild‐type etiolated seedlings. Moreover, ACC, the direct precursor of ethylene, accentuates the effects of light on hypocotyl elongation during the dark‐to‐light transition. We determined that light leads to the transient elongation of hypocotyls by stabilizing the ACS5 protein during the dark‐to‐light transition. Furthermore, biochemical analysis of an ACS5 mutant protein bearing an alteration in the C‐terminus indicated that light stabilizes ACS5 by inhibiting the degradation mechanism that acts through the C‐terminus of ACS5. Our study reveals that plants regulate hypocotyl elongation during seedling establishment by coordinating light‐induced ethylene biosynthesis at the post‐translational level. Moreover, the stimulatory role of light on hypocotyl growth during the dark‐to‐light transition provides additional insights into the known inhibitory role of light in hypocotyl development.     

Epithelial‐to‐mesenchymal transition in epicardium is independent of snail1

The epicardium is the outer epithelial covering the heart. This tissue undergoes an epithelial‐to‐mesenchymal transition (EMT) to generate mesenchymal epicardial‐derived cells (EPDCs) that populate the extracellular matrix of the subepicardium and contribute to the development of the coronary vessels and cardiac interstitial cells. Although epicardial EMT plays a crucial role in heart development, the molecular regulation of this process is incompletely understood. Here we examined the possible role of the EMT regulator Snail1 in this process. Snail1 is expressed in the epicardium and EPDCs during mouse cardiac development. To determine the function of Snail1 in epicardial EMT, we deleted Snail1 in the epicardium using Wt1‐ and Tbx18‐Cre drivers. Unexpectedly, epicardial‐specific Snail1 mutants are viable and fertile and do not display any obvious morphological or functional cardiac abnormalities. Molecular analysis of these mice reveals that epicardial EMT occurs normally, and epicardial derivatives are established in these mutants. We conclude that Snail1 is not required for the initiation and progression of embryonic epicardial EMT. genesis 51:32–40, 2013. © 2012 Wiley Periodicals, Inc.     

Multiple natural enemies cause distance‐dependent mortality at the seed‐to‐seedling transition

Specialised natural enemies maintain forest diversity by reducing tree survival in a density‐ or distance‐dependent manner. Fungal pathogens, insects and mammals are the enemy types most commonly hypothesised to cause this phenomenon. Still, their relative importance remains largely unknown, as robust manipulative experiments have generally targeted a single enemy type and life history stage. Here, we use fungicide, insecticide and physical exclosure treatments to isolate the impacts of each enemy type on two life history stages (germination and early seedling survival) in three tropical tree species. Distance dependence was evident for five of six species‐stage combinations, with each enemy type causing distance dependence for at least one species stage and their importance varying widely between species and stages. Rather than implicating one enemy type as the primary agent of this phenomenon, our field experiments suggest that multiple agents acting at different life stages collectively contribute to this diversity‐promoting mechanism.     

Anatomical network analysis of the musculoskeletal system reveals integration loss and parcellation boost during the fins‐to‐limbs transition

Tetrapods evolved from within the lobe‐finned fishes around 370 Ma. The evolution of limbs from lobe‐fins entailed a major reorganization of the skeletal and muscular anatomy of appendages in early tetrapods. Concurrently, a degree of similarity between pectoral and pelvic appendages also evolved. Here, we compared the anatomy of appendages in extant lobe‐finned fishes (Latimeria and Neoceratodus) and anatomically plesiomorphic amphibians (Ambystoma, Salamandra) and amniotes (Sphenodon) to trace and reconstruct the musculoskeletal changes that took place during the fins‐to‐limbs transition. We quantified the anatomy of appendages using network analysis. First, we built network models—in which nodes represent bones and muscles, and links represent their anatomical connections—and then we measured network parameters related to their anatomical integration, heterogeneity, and modularity. Our results reveal an evolutionary transition toward less integrated, more modular appendages. We interpret this transition as a diversification of muscle functions in tetrapods compared to lobe‐finned fishes. Limbs and lobe‐fins show also a greater similarity between their pectoral and pelvic appendages than ray‐fins do. These findings on extant species provide a basis for future quantitative and comprehensive reconstructions of the anatomy of limbs in early tetrapod fossils, and a way to better understand the fins‐to‐limbs transition.     

Starch metabolism and antiflorigenic signals modulate the juvenile‐to‐adult phase transition in Arabidopsis

The physiology and genetics underlying juvenility is poorly understood. Here, we exploit Arabidopsis as a system to understand the mechanisms that regulate floral incompetence during juvenility. Using an experimental assay that allows the length of juvenility to be estimated and mutants impaired in different pathways, we show that multiple inputs influence juvenility. Juvenile phase lengths of wild type (WT) accessions Col‐0, Ler‐0 and Ws‐4 are shown to differ, with Col‐0 having the shortest and Ws‐4 the longest length. Plants defective in sugar signalling [gin1‐1, gin2‐1, gin6 (abi4)] and floral repressor mutants [hst1, tfl1, tfl2 (lhp1)] showed shortened juvenile phase lengths compared to their respective WTs. Mutants defective in starch anabolism (adg1‐1, pgm1) and catabolism (sex1, sex4, bam3) showed prolonged juvenile phase lengths compared to Col‐0. Examination of diurnal metabolite changes in adg1‐1 and sex1 mutants indicates that their altered juvenile phase length may be due to lack of starch turnover, which influences carbohydrate availability. In this article, we propose a model in which a variety of signals including floral activators and repressors modulate the juvenile‐to‐adult phase transition. The role of carbohydrates may be in their capacity as nutrients, osmotic regulators, signalling molecules and/ or through their interaction with phytohormonal networks.     

Spatio‐temporal control of neural epithelial cell migration and epithelium‐to‐mesenchyme transition during avian neural tube development

As opposed to the neural crest, the neural epithelium is generally viewed as a static and cohesive structure. Here, using an ex vivo system free of the environmental influences and physical constraints encountered in the embryo, we show that neural epithelial cells are on the contrary intrinsically motile, although they do not undergo spontaneous epithelium‐to‐mesenchyme transition and display molecular and cellular characteristics distinct from those of neural crest cells. However, they can be instructed to undergo epithelium‐to‐mesenchyme conversion independently of the acquisition of neural crest traits. Migration potentialities of neural epithelial cells are transient and are progressively restricted during neural tube development. Restriction of cell migration is irreversible and can be in part accounted for by increase in N‐cadherin in cellular junctions and in cell polarity. In conclusion, our study reveals that the neural epithelium is a highly flexible tissue in which cells are maintained cohesive under the control of a combination of extrinsic factors and physical constraints.     

Steric hindrance of SNARE transmembrane domain organization impairs the hemifusion‐to‐fusion transition

SNAREs fuse membranes in several steps. Trans‐SNARE complexes juxtapose membranes, induce hemifused stalk structures, and open the fusion pore. A recent penetration model of fusion proposed that SNAREs force the hydrophilic C‐termini of their transmembrane domains through the hydrophobic core of the membrane(s). In contrast, the indentation model suggests that the C‐termini open the pore by locally compressing and deforming the stalk. Here we test these models in the context of yeast vacuole fusion. Addition of small hydrophilic tags renders bilayer penetration by the C‐termini energetically unlikely. It preserves fusion activity, however, arguing against the penetration model. Addition of large protein tags to the C‐termini permits SNARE activation, trans‐SNARE pairing, and hemifusion but abolishes pore opening. Fusion proceeds if the tags are detached from the membrane by a hydrophilic spacer or if only one side of the trans‐SNARE complex carries a protein tag. Thus, both sides of a trans‐SNARE complex can drive pore opening. Our results are consistent with an indentation model in which multiple SNARE C‐termini cooperate in opening the fusion pore by locally deforming the inner leaflets.