Anucleate Caenorhabditis elegans sperm can crawl, fertilize oocytes and direct anterior-posterior polarization of the 1-cell embryo

Development ◽  
2000 ◽  
Vol 127 (2) ◽  
pp. 355-366 ◽  
Author(s):  
P.L. Sadler ◽  
D.C. Shakes

It has long been appreciated that spermiogenesis, the cellular transformation of sessile spermatids into motile spermatozoa, occurs in the absence of new DNA transcription. However, few studies have addressed whether the physical presence of a sperm nucleus is required either during spermiogenesis or for subsequent sperm functions during egg activation and early zygotic development. To determine the role of the sperm nucleus in these processes, we analyzed two C. elegans mutants whose spermatids lack DNA. Here we show that these anucleate sperm not only differentiate into mature functional spermatozoa, but they also crawl toward and fertilize oocytes. Furthermore, we show that these anucleate sperm induce both normal egg activation and anterior-posterior polarity in the 1-cell C. elegans embryo. The latter finding demonstrates for the first time that although the anterior-posterior embryonic axis in C. elegans is specified by sperm, the sperm pronucleus itself is not required. Also unaffected is the completion of oocyte meiosis, formation of an impermeable eggshell, migration of the oocyte pronucleus, and the separation and expansion of the sperm-contributed centrosomes. Our investigation of these mutants confirms that, in C. elegans, neither the sperm chromatin mass nor a sperm pronucleus is required for spermiogenesis, proper egg activation, or the induction of anterior-posterior polarity.

2020 ◽  
Vol 48 (3) ◽  
pp. 1243-1253 ◽  
Author(s):  
Sukriti Kapoor ◽  
Sachin Kotak

Cellular asymmetries are vital for generating cell fate diversity during development and in stem cells. In the newly fertilized Caenorhabditis elegans embryo, centrosomes are responsible for polarity establishment, i.e. anterior–posterior body axis formation. The signal for polarity originates from the centrosomes and is transmitted to the cell cortex, where it disassembles the actomyosin network. This event leads to symmetry breaking and the establishment of distinct domains of evolutionarily conserved PAR proteins. However, the identity of an essential component that localizes to the centrosomes and promotes symmetry breaking was unknown. Recent work has uncovered that the loss of Aurora A kinase (AIR-1 in C. elegans and hereafter referred to as Aurora A) in the one-cell embryo disrupts stereotypical actomyosin-based cortical flows that occur at the time of polarity establishment. This misregulation of actomyosin flow dynamics results in the occurrence of two polarity axes. Notably, the role of Aurora A in ensuring a single polarity axis is independent of its well-established function in centrosome maturation. The mechanism by which Aurora A directs symmetry breaking is likely through direct regulation of Rho-dependent contractility. In this mini-review, we will discuss the unconventional role of Aurora A kinase in polarity establishment in C. elegans embryos and propose a refined model of centrosome-dependent symmetry breaking.


Author(s):  
Dorothy Benton ◽  
Eva C Jaeger ◽  
Arielle Kilner ◽  
Ashley Kimble ◽  
Josh Lowry ◽  
...  

Abstract Puromycin-sensitive aminopeptidases are found across phyla and are known to regulate the cell-cycle and play a protective role in neurodegenerative disease. PAM-1 is a puromycin-sensitive aminopeptidase important for meiotic exit and polarity establishment in the one-cell Caenorhabditis elegans embryo. Despite conservation of this aminopeptidase, little is known about its targets during development. In order to identify novel interactors, we conducted a suppressor screen and isolated four suppressing mutations in three genes that partially rescued the maternal-effect lethality of pam-1 mutants. Suppressed strains show improved embryonic viability and polarization of the anterior-posterior axis. We identified a missense mutation in wee-1.3 in one of these suppressed strains. WEE-1.3 is an inhibitory kinase that regulates maturation promoting factor. While the missense mutation suppressed polarity phenotypes in pam-1, it does so without restoring centrosome-cortical contact or altering the cortical actomyosin cytoskeleton. To see if PAM-1 and WEE-1.3 interact in other processes, we examined oocyte maturation. While depletion of wee-1.3 causes sterility due to precocious oocyte maturation, this effect was lessened in pam-1 worms, suggesting that PAM-1 and WEE-1.3 interact in this process. Levels of WEE-1.3 were comparable between wild-type and pam-1 strains, suggesting that WEE-1.3 is not a direct target of the aminopeptidase. Thus, we have established an interaction between PAM-1 and WEE-1.3 in multiple developmental processes and have identified suppressors that are likely to further our understanding of the role of puromycin-sensitive aminopeptidases during development.


2015 ◽  
Vol 112 (12) ◽  
pp. 3606-3611 ◽  
Author(s):  
Jinzhou Yuan ◽  
David M. Raizen ◽  
Haim H. Bau

The ability to orient oneself in response to environmental cues is crucial to the survival and function of diverse organisms. One such orientation behavior is the alignment of aquatic organisms with (negative rheotaxis) or against (positive rheotaxis) fluid current. The questions of whether low-Reynolds-number, undulatory swimmers, such as worms, rheotax and whether rheotaxis is a deliberate or an involuntary response to mechanical forces have been the subject of conflicting reports. To address these questions, we use Caenorhabditis elegans as a model undulatory swimmer and examine, in experiment and theory, the orientation of C. elegans in the presence of flow. We find that when close to a stationary surface the animal aligns itself against the direction of the flow. We elucidate for the first time to our knowledge the mechanisms of rheotaxis in worms and show that rheotaxis can be explained solely by mechanical forces and does not require sensory input or deliberate action. The interaction between the flow field induced by the swimmer and a nearby surface causes the swimmer to tilt toward the surface and the velocity gradient associated with the flow rotates the animal to face upstream. Fluid mechanical computer simulations faithfully mimic the behavior observed in experiments, supporting the notion that rheotaxis behavior can be fully explained by hydrodynamics. Our study highlights the important role of hydrodynamics in the behavior of small undulating swimmers and may assist in developing control strategies to affect the animals’ life cycles.


Genes ◽  
2021 ◽  
Vol 12 (11) ◽  
pp. 1651
Author(s):  
Juan A. Subirana ◽  
Xavier Messeguer

It has been shown in recent years that many repeated sequences in the genome are expressed as RNA transcripts, although the role of such RNAs is poorly understood. Some isolated and tandem repeats (satellites) have been found to be transcribed, such as mammalian Alu sequences and telomeric/centromeric satellites in different species. However, there is no detailed study on the eventual transcription of the interspersed satellites found in many species. Therefore, we decided to study for the first time the transcription of the abundant DNA satellites in the bacterium Bacillus coagulans and in the nematode Caenorhabditis elegans. We have updated the data for C. elegans satellites using the latest version of the genome. We analyzed the transcription of satellites in both species in available RNA-seq results and found that they are widely transcribed. Our demonstration that satellite RNAs are transcribed adds a new family of non-coding RNAs. This is a field that requires further investigation and will provide a deeper understanding of gene expression and control.


1994 ◽  
Vol 126 (3) ◽  
pp. 591-601 ◽  
Author(s):  
S Dimitrov ◽  
M C Dasso ◽  
A P Wolffe

We find that the remodeling of the condensed Xenopus laevis sperm nucleus into the paternal pronucleus in egg extracts is associated with phosphorylation of the core histones H2A, H2A.X and H4, and uptake of a linker histone B4 and a HMG 2 protein. Histone B4 is required for the assembly of chromatosome structures in the pronucleus. However neither B4 nor core histone phosphorylation are required for the assembly of spaced nucleosomal arrays. We suggest that the spacing of nucleosomal arrays is determined by interaction between adjacent histone octamers under physiological assembly conditions.


2017 ◽  
Author(s):  
Malgorzata J. Liro ◽  
Diane G. Morton ◽  
Lesilee S. Rose

AbstractThe PAR-1 kinase of C. elegans is localized to the posterior of the one-cell embryo and its mutations affect asymmetric spindle placement and partitioning of cytoplasmic components in the first cell cycle. However, unlike mutations in the posteriorly localized PAR-2 protein, par-1 mutations do not cause failure to restrict the anterior PAR polarity complex. Further, it has been difficult to examine the role of PAR-1 in subsequent divisions due to the early defects in par-1 mutant embryos. Here we show that the PIG-1 kinase acts redundantly with PAR-1 to restrict the anterior PAR-3 protein for polarity maintenance in the one-cell embryo. By using a weak allele of par-1 that exhibits enhanced lethality when combined with a pig-1 mutation we have further explored roles for these genes in subsequent divisions. We find that both PIG-1 and PAR-1 regulate spindle orientation in the EMS blastomere of the four-cell stage embryo to ensure that it undergoes an asymmetric division. In this cell, PIG-1 and PAR-1 act in parallel pathways for spindle positioning, PIG-1 in the MES-1/SRC-1 pathway and PAR-1 in the Wnt pathway.


Development ◽  
1996 ◽  
Vol 122 (10) ◽  
pp. 3133-3140 ◽  
Author(s):  
J.L. Watts ◽  
B. Etemad-Moghadam ◽  
S. Guo ◽  
L. Boyd ◽  
B.W. Draper ◽  
...  

The generation of asymmetry in the one-cell embryo of Caenorhabditis elegans is necessary to establish the anterior-posterior axis and to ensure the proper identity of early blastomeres. Maternal-effect lethal mutations with a partitioning defective phenotype (par) have identified several genes involved in this process. We have identified a new gene, par-6, which acts in conjunction with other par genes to properly localize cytoplasmic components in the early embryo. The early phenotypes of par-6 embryos include the generation of equal-sized blastomeres, improper localization of P granules and SKN-1 protein, and abnormal second division cleavage patterns. Overall, this phenotype is very similar to that caused by mutations in a previously described gene, par-3. The probable basis for this similarity is revealed by our genetic and immunolocalization results; par-6 acts through par-3 by localizing or maintaining the PAR-3 protein at the cell periphery. In addition, we find that loss-of-function par-6 mutations act as dominant bypass suppressors of loss-of-function mutations in par-2.


Development ◽  
1992 ◽  
Vol 116 (2) ◽  
pp. 481-490 ◽  
Author(s):  
D.W. Cowing ◽  
C. Kenyon

mab-5 is a member of a complex of homeobox-containing genes evolutionarily related to the Antennapedia and bithorax complexes of Drosophila melanogaster. Like the homeotic genes in Drosophila, mab-5 is required in a particular region along the anterior-posterior body axis, and acts during postembryonic development to give cells in this region their characteristic identities. We have used a mab-5-lacZ fusion integrated into the C. elegans genome to study the posterior-specific expression of mab-5 during embryogenesis. The mab-5-lacZ fusion was expressed in the posterior of the embryo by 180 minutes after the first cleavage, indicating that the mechanisms responsible for the position-specific expression of mab-5-lacZ act at a relatively early stage of embryogenesis. In embryos homozygous for mutations in the par genes, which disrupt segregation of factors during early cleavages, expression of mab-5-lacZ was no longer localized to the posterior. This suggests that posterior-specific expression of mab-5 depends on the appropriate segregation of developmental factors during early embryogenesis. After extrusion of any blastomere of the four-cell embryo, descendants of the remaining three cells could still express the mab-5-lacZ fusion. In these partial embryos, however, the fusion was often expressed in cells scattered throughout the embryo, suggesting that cell-cell interactions and/or proper positioning of early blastomeres are required for mab-5 expression to be localized to the posterior.


Development ◽  
1994 ◽  
Vol 120 (7) ◽  
pp. 2051-2064 ◽  
Author(s):  
H. Hutter ◽  
R. Schnabel

Two successive inductions specify blastomere identities, that is complex cell lineages and not specific tissues, in a major part of the early C. elegans embryo. The first induction acts along the anterior-posterior axis of the embryo and the second along the left-right axis. During the first induction a specific lineage program is induced in the posterior of the two AB blastomeres present in the four cell embryo. During the second induction, almost all of the left-right differences of the embryo are specified by interactions between a single signalling blastomere, MS, and the AB blastomeres that surround it. In both cases the inductions break the equivalence of pairs of blastomeres. The inductions correlate with the cell-cell contacts to the inducing blastomeres. The stereotype cleavage patterns of the early embryo results in invariant cell-cell contacts that guarantee the specificity of the inductions. Both inductions are affected in embryos mutant for glp-1 suggesting that in both cases glp-1 is involved in the reception of the signal.


Development ◽  
1997 ◽  
Vol 124 (19) ◽  
pp. 3805-3814 ◽  
Author(s):  
M. Epstein ◽  
G. Pillemer ◽  
R. Yelin ◽  
J.K. Yisraeli ◽  
A. Fainsod

Patterning along the anterior-posterior axis takes place during gastrulation and early neurulation. Homeobox genes like Otx-2 and members of the Hox family have been implicated in this process. The caudal genes in Drosophila and C. elegans have been shown to determine posterior fates. In vertebrates, the caudal genes begin their expression during gastrulation and they take up a posterior position. By injecting sense and antisense RNA of the Xenopus caudal gene Xcad-2, we have studied a number of regulatory interactions among homeobox genes along the anterior-posterior axis. Initially, the Xcad-2 and Otx-2 genes are mutually repressed and, by late gastrulation, they mark the posterior- or anterior-most domains of the embryo, respectively. During late gastrulation and neurulation, Xcad-2 plays an additional regulatory function in relation to the Hox genes. Hox genes normally expressed anteriorly are repressed by Xcad-2 overexpression while those normally expressed posteriorly exhibit more anterior expression. The results show that the caudal genes are part of a posterior determining network which during early gastrulation functions in the subdivision of the embryo into anterior head and trunk domains. Later in gastrulation and neurulation these genes play a role in the patterning of the trunk region.


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