Evolutionary divergence of anaphase spindle mechanics in nematode embryos constrained by antagonistic pulling and viscous forces.

Cellular functions such as cell division are remarkably conserved across phyla. However, the evolutionary principles of cellular organization that drive them are less well explored. Thus, an essential question remains: to what extent do cellular parameters evolve without altering the basic functions they sustain? Here we have observed six different nematode species for which the mitotic spindle is positioned asymmetrically during the first embryonic division. Whereas the C. elegans spindle undergoes oscillations during its displacement, the spindle elongates without oscillations in other species. We asked which evolutionary changes in biophysical parameters could explain differences in spindle motion while maintaining a constant output. Using laser microsurgery of the spindle, we revealed that all species are subjected to cortical pulling forces of varying magnitudes. Using a viscoelastic model to fit the recoil trajectories and with an independent measurement of cytoplasmic viscosity, we extracted the values of cytoplasmic drag, cortical pulling forces, and spindle elasticity for all species. We found large variations in cytoplasmic viscosity, whereas cortical pulling forces and elasticity were often more constrained. In agreement with previous simulations, we found that increased viscosity correlates with decreased oscillation speeds across species. However, the absence of oscillations in some species despite low viscosity can only be explained by smaller pulling forces. Consequently, we find that spindle mobility across the species analyzed here is characterized by a tradeoff between cytoplasmic viscosity and pulling forces normalized by the size of the embryo. Our work provides a framework for understanding mechanical constraints on evolutionary diversification of spindle mobility.

Force Transmission between Three Tissues Controls Bipolar Planar Polarity Establishment and Morphogenesis.

How tissues from different developmental origins interact to achieve coordinated morphogenesis at the level of a whole organism is a fundamental question in developmental biology. While biochemical signaling pathways controlling morphogenesis have been extensively studied [1-3], morphogenesis of epithelial tissues can also be directed by mechanotransduction pathways physically linking two tissues [4-8]. C. elegans embryonic elongation requires the coordination of three tissues: muscles, the dorsal and ventral epidermis, and the lateral epidermis. Elongation starts by cell-shape changes driven by actomyosin contractions in the lateral epidermis [9, 10]. At mid-elongation, muscles become connected to the apical surface of the dorsal and ventral epidermis by molecular tendons formed by muscle integrins, extracellular matrix, and C. elegans hemidesmosomes (CeHDs). The mechanical signal generated by the onset of muscle contractions in the antero-posterior axis from mid-elongation is translated into a biochemical pathway controlling the maturation of CeHDs in the dorsal and ventral epidermis [11]. Consistently, mutations affecting muscle contractions or molecular tendons lead to a mid-elongation arrest [12]. Here, we found that the mechanical force generated by muscle contractions and relayed by molecular tendons is transmitted by adherens junctions to lateral epidermal cells, where it establishes a newly identified bipolar planar polarity of the apical PAR module. The planar polarized PAR module is then required for actin planar organization, thus contributing to the determination of the orientation of cell-shape changes and the elongation axis of the whole embryo. This mechanotransduction pathway is therefore essential to coordinate the morphogenesis of three embryonic tissues.

Males as somatic investment in a parthenogenetic nematode.

We report the reproductive strategy of the nematode Mesorhabditis belari This species produces only 9% males, whose sperm is necessary to fertilize and activate the eggs. However, most of the fertilized eggs develop without using the sperm DNA and produce female individuals. Only in 9% of eggs is the male DNA utilized, producing sons. We found that mixing of parental genomes only gives rise to males because the Y-bearing sperm of males are much more competent than the X-bearing sperm for penetrating the eggs. In this previously unrecognized strategy, asexual females produce few sexual males whose genes never reenter the female pool. Here, production of males is of interest only if sons are more likely to mate with their sisters. Using game theory, we show that in this context, the production of 9% males by M. belari females is an evolutionary stable strategy.

Callose-associated silica deposition in Arabidopsis.

The mechanism of biological silicification in plants remains to be elucidated. There are strong arguments supporting a role for the plant extracellular matrix and the ß-1-3-glucan, callose, has been identified as a possible template for silica deposition in the common horsetail, Equisetum arvense. The model plant Arabidopsis thaliana, which is not known as a silica accumulator, can be engineered to produce mutants in which, following a pathogen-associated molecular pattern challenge, callose production in leaves is either induced (35S:PMR4-GFP) or not (pmr4). We have grown these mutants hydroponically in the presence of added silicon to test if the induction of callose results in greater silica deposition in the leaves. Callose induction was identified throughout leaf tissue of wild type Arabidopsis and the mutant 35S:PMR4-GFP but not in the mutant pmr4. Similarly both wild type Arabidopsis and the mutant 35S:PMR4-GFP showed extensive silicification of leaf tissue while the pmr4 mutant deposited very little silica in its leaf tissues. Wild type Arabidopsis and the mutant 35S:PMR4-GFP responded to a pathogen-like challenge by producing both callose and biogenic silica coincidently in their leaf tissues. Trichomes in particular showed both callose deposition and extensive silicification. The lack of both induced callose deposition and subsequent silicification in the pmr4 mutant strongly suggested that the biochemistry of callose formation and deposition were allied to biological silicification in Arabidopsis.