Expression of the homeotic gene mab-5 during Caenorhabditis elegans embryogenesis

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.


2021 ◽  
Author(s):  
Jonathan D Rumley ◽  
Elicia A Preston ◽  
Dylan Cook ◽  
Felicia L Peng ◽  
Amanda L Zacharias ◽  
...  

Patterning of the anterior-posterior axis is fundamental to animal development. The Wnt pathway plays a major role in this process by activating the expression of posterior genes in animals from worms to humans. This observation raises the question of whether the Wnt pathway or other regulators control the expression of the many anterior-expressed genes. We found that the expression of five anterior-specific genes in Caenorhabditis elegans embryos depends on the Wnt pathway effectors pop-1/TCF and sys-1/β-catenin. We focused further on one of these anterior genes, ref-2/ZIC, a conserved transcription factor expressed in multiple anterior lineages. Live imaging of ref-2 mutant embryos identified defects in cell division timing and position in anterior lineages. Cis-regulatory dissection identified three ref-2 transcriptional enhancers, one of which is necessary and sufficient for anterior-specific expression. This enhancer is activated by the T-box transcription factors TBX-37 and TBX-38, and surprisingly, concatemerized TBX-37/38 binding sites are sufficient to drive anterior-biased expression alone, despite the broad expression of TBX-37 and TBX-38. Taken together, our results highlight the diverse mechanisms used to regulate anterior expression patterns in the embryo.



Development ◽  
1999 ◽  
Vol 126 (19) ◽  
pp. 4341-4349 ◽  
Author(s):  
T. Shandala ◽  
R.D. Kortschak ◽  
S. Gregory ◽  
R. Saint

The dead ringer (dri) gene of Drosophila melanogaster is a member of the recently discovered ARID-box family of eukaryotic genes that encode proteins with a conserved DNA binding domain. dri itself is highly conserved, with specific orthologs in the human, mouse, zebrafish and C. elegans genomes. We have generated dri mutant alleles to show that dri is essential for anterior-posterior patterning and for muscle development in the embryo. Consistent with the mutant phenotype and the sequence-specific DNA-binding properties of its product, dri was found to be essential for the normal early embryonic expression pattern of several key regulatory genes. In dri mutant embryos, expression of argos in the terminal domains was severely reduced, accounting for the dri mutant head phenotype. Conversely, buttonhead expression was found to be deregulated in the trunk region, accounting for the appearance of ectopic cephalic furrows. Curiously, dri was found also to be required for maintenance of expression of the ventrolateral region of even-skipped stripe four. This study establishes dri as an essential co-factor in the regulated expression of specific patterning genes during early embryogenesis.



Development ◽  
1991 ◽  
Vol 112 (3) ◽  
pp. 863-879 ◽  
Author(s):  
P. Schedin ◽  
C.P. Hunter ◽  
W.B. Wood

The primary sex-determining signal in Caenorhabditis elegans is the ratio of X chromosomes to sets of autosomes (X/A ratio), normally 1.0 in hermaphrodites (XX) and 0.5 in males (XO). XX triploids (X/A = 0.67) are males, but if these animals carry a partial duplication of the X chromosome such that X/A approximately equal to 0.7, they develop as intersexes that are sexually mosaic. We have analyzed these mosaics using Nomarski microscopy and in situ hybridization to obtain information on whether sex determination decisions can be made independently in different cells and tissues, and when these commitments are made. The observed patterns of male and female cells in individual animals indicate that sex determination decisions can be influenced by anterior-posterior position and that sex determination decisions can be made as late as the third larval stage of postembryonic development. Although these decisions clearly can be made independently in different lineages, they show substantial biases toward one sex or the other in individual animals. We interpret these results to suggest that sex determination in C. elegans is not entirely cell autonomous.



Development ◽  
2000 ◽  
Vol 127 (16) ◽  
pp. 3429-3440 ◽  
Author(s):  
G.J. Hermann ◽  
B. Leung ◽  
J.R. Priess

The C. elegans intestine is a simple tube consisting of a monolayer of epithelial cells. During embryogenesis, cells in the anterior of the intestinal primordium undergo reproducible movements that lead to an invariant, asymmetrical ‘twist’ in the intestine. We have analyzed the development of twist to determine how left-right and anterior-posterior asymmetries are generated within the intestinal primordium. The twist requires the LIN-12/Notch-like signaling pathway of C. elegans. All cells within the intestinal primordium initially express LIN-12, a receptor related to Notch; however, only cells in the left half of the primordium contact external, nonintestinal cells that express LAG-2, a ligand related to delta. LIN-12 and LAG-2 mediated interactions result in the left primordial cells expressing lower levels of LIN-12 than the right primordial cells. We propose that this asymmetrical pattern of LIN-12 expression is the basis for asymmetry in later cell-cell interactions within the primordium that lead directly to intestinal twist. Like the interactions that initially establish LIN-12 asymmetry, the later interactions are mediated by LIN-12. The later interactions, however, involve a different ligand related to delta, called APX-1. We show that the anterior-posterior asymmetry in intestinal twist involves the kinase LIT-1, which is part of a signaling pathway in early embryogenesis that generates anterior-posterior differences between sister cells.



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.



Development ◽  
1998 ◽  
Vol 125 (24) ◽  
pp. 4877-4887 ◽  
Author(s):  
D.F. Schroeder ◽  
J.D. McGhee

The endoderm of higher organisms is extensively patterned along the anterior/posterior axis. Although the endoderm (gut or E lineage) of the nematode Caenorhabditis elegans appears to be a simple uniform tube, cells in the anterior gut show several molecular and anatomical differences from cells in the posterior gut. In particular, the gut esterase ges-1 gene, which is normally expressed in all cells of the endoderm, is expressed only in the anterior-most gut cells when certain sequences in the ges-1 promoter are deleted. Using such a deleted ges-1 transgene as a biochemical marker of differentiation, we have investigated the basis of anterior-posterior gut patterning in C. elegans. Although homeotic genes are involved in endoderm patterning in other organisms, we show that anterior gut markers are expressed normally in C. elegans embryos lacking genes of the homeotic cluster. Although signalling from the mesoderm is involved in endoderm patterning in other organisms, we show that ablation of all non-gut blastomeres from the C. elegans embryo does not affect anterior gut marker expression; furthermore, ectopic guts produced by genetic transformation express anterior gut markers generally in the expected location and in the expected number of cells. We conclude that anterior gut fate requires no specific cell-cell contact but rather is produced autonomously within the E lineage. Cytochalasin D blocking experiments fully support this conclusion. Finally, the HMG protein POP-1, a downstream component of the Wnt signalling pathway, has recently been shown to be important in many anterior/posterior fate decisions during C. elegans embryogenesis (Lin, R., Hill, R. J. and Priess, J. R. (1998) Cell 92, 229–239). When RNA-mediated interference is used to eliminate pop-1 function from the embryo, gut is still produced but anterior gut marker expression is abolished. We suggest that the C. elegans endoderm is patterned by elements of the Wnt/pop-1 signalling pathway acting autonomously within the E lineage.



Development ◽  
1999 ◽  
Vol 126 (7) ◽  
pp. 1537-1546 ◽  
Author(s):  
K. Brunschwig ◽  
C. Wittmann ◽  
R. Schnabel ◽  
T.R. Burglin ◽  
H. Tobler ◽  
...  

The Caenorhabditis elegans lin-39, mab-5 and egl-5 Hox genes specify cell fates along the anterior-posterior body axis of the nematode during postembryonic development, but little is known about Hox gene functions during embryogenesis. Here, we show that the C. elegans labial-like gene ceh-13 is expressed in cells of many different tissues and lineages and that the rostral boundary of its expression domain is anterior to those of the other Hox genes. By transposon-mediated mutagenesis, we isolated a zygotic recessive ceh-13 loss-of-function allele, sw1, that exhibits an embryonic sublethal phenotype. Lineage analyses and immunostainings revealed defects in the organization of the anterior lateral epidermis and anterior body wall muscle cells. The epidermal and mesodermal identity of these cells, however, is correctly specified. ceh-13(sw1) mutant embryos also show fusion and adhesion defects in ectodermal cells. This suggests that ceh-13 plays a role in the anterior organization of the C. elegans embryo and is involved in the regulation of cell affinities.



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 ◽  
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.



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.



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