Extensive zygotic control of the anteroposterior axis in the wasp Nasonia vitripennis

Development ◽  
1999 ◽  
Vol 126 (4) ◽  
pp. 701-710 ◽  
Author(s):  
M.A. Pultz ◽  
J.N. Pitt ◽  
N.M. Alto

Insect axis formation is best understood in Drosophila melanogaster, where rapid anteroposterior patterning of zygotic determinants is directed by maternal gene products. The earliest zygotic control is by gap genes, which determine regions of several contiguous segments and are largely conserved in insects. We have asked genetically whether early zygotic patterning genes control similar anteroposterior domains in the parasitoid wasp Nasonia vitripennis as in Drosophila. Nasonia is advantageous for identifying and studying recessive zygotic lethal mutations because unfertilized eggs develop as males while fertilized eggs develop as females. Here we describe recessive zygotic mutations identifying three Nasonia genes: head only mutant embryos have posterior defects, resembling loss of both maternal and zygotic Drosophila caudal function; headless mutant embryos have anterior and posterior gap defects, resembling loss of both maternal and zygotic Drosophila hunchback function; squiggy mutant embryos develop only four full trunk segments, a phenotype more severe than those caused by lack of Drosophila maternal or zygotic terminal gene functions. These results indicate greater dependence on the zygotic genome to control early patterning in Nasonia than in the fly.

2021 ◽  
Author(s):  
Philip Abitua ◽  
Deniz Aksel ◽  
Alexander Schier

Axis formation in fish and amphibians is initiated by a prepattern of maternal gene products in the blastula. The embryogenesis of annual killifish challenges prepatterning models because blastomeres disperse and then re-aggregate to form the germ layers and body axes. This dispersion-aggregation process prompts the question how axis determinants such as Huluwa and germ layer inducers such as Nodal function in annual killifish. Here we show in Nothobranchius furzeri that huluwa, the factor thought to break symmetry by stabilizing β-catenin, is a non-functional pseudogene. Nuclear β-catenin is not selectively stabilized on one side of the blastula but accumulates in cells forming the incipient aggregate. Inhibition of Nodal signaling blocks aggregation and disrupts coordinated cell migration, establishing a novel role for this signaling pathway. These results reveal a surprising departure from classic mechanisms of axis formation: canonical Huluwa-mediated prepatterning is dispensable and Nodal coordinates morphogenesis.


Development ◽  
1989 ◽  
Vol 107 (Supplement) ◽  
pp. 21-29 ◽  
Author(s):  
Ruth Lehmann ◽  
Hans Georg Frohnhöfer

The establishment of the segmental pattern in the Drosophila embryo is directed by three sets of maternal genes: the anterior, the terminal and the posterior group of genes. Embryos derived from females mutant for one of the posterior group genes lack abdominal segmentation. This phenotype can be rescued by transplantation of posterior pole plasm into the abdominal region of mutant embryos. We transplanted posterior pole plasm into the middle of embryos mutant either for the posterior, the anterior and posterior, or all three maternal systems and monitored the segmentation pattern as well as the expression of the zygotic gap gene Krüppel in control and injected embryos. We conclude that polarity and identity of the abdominal segments do not depend on the relative concentration of posterior activity but rather on the position of gap gene expression. By changing the pattern of gap gene expression, the orientation of the abdomen can be reversed. These experiments suggest that maternal gene products act in a strictly hierarchical manner. The function of the maternal gene products becomes dispensable once the position of the zygotically expressed gap genes is determined. Subsequently the gap genes will control the pattern of the pair-rule and segment polarity genes.


Genetics ◽  
2000 ◽  
Vol 154 (3) ◽  
pp. 1213-1229
Author(s):  
Mary Anne Pultz ◽  
Kristin K Zimmerman ◽  
Neal M Alto ◽  
Matt Kaeberlein ◽  
Sarah K Lange ◽  
...  

Abstract We have screened for zygotic embryonic lethal mutations affecting cuticular morphology in Nasonia vitripennis (Hymenoptera; Chalcidoidea). Our broad goal was to investigate the use of Nasonia for genetically surveying conservation and change in regulatory gene systems, as a means to understand the diversity of developmental strategies that have arisen during the course of evolution. Specifically, we aim to compare anteroposterior patterning gene functions in two long germ band insects, Nasonia and Drosophila. In Nasonia, unfertilized eggs develop as haploid males while fertilized eggs develop as diploid females, so the entire genome can be screened for recessive zygotic mutations by examining the progeny of F1 females. We describe 74 of >100 lines with embryonic cuticular mutant phenotypes, including representatives of coordinate, gap, pair-rule, segment polarity, homeotic, and Polycomb group functions, as well as mutants with novel phenotypes not directly comparable to those of known Drosophila genes. We conclude that Nasonia is a tractable experimental organism for comparative developmental genetic study. The mutants isolated here have begun to outline the extent of conservation and change in the genetic programs controlling embryonic patterning in Nasonia and Drosophila.


2007 ◽  
Vol 139 (5) ◽  
pp. 678-684 ◽  
Author(s):  
B.H. King

AbstractWhen habitat quality is variable, there should be strong selection for the ability to detect and respond to the variation. Adult females of the parasitoid wasp Nasonia vitripennis (Walker) are known to increase their restlessness (the proportion of time in locomotion) both during and after exposure to a poor quality host. Doing so provides a mechanism for leaving a poor host and potentially finding a better host. This study examined whether restlessness also changes in response to competition as indicated by the presence of adult conspecifics. Both restlessness and the probability of dispersing across an inhospitable environment were greater when a female was with another female than when she was alone. However, restlessness did not remain elevated after the other female was removed. In contrast with females, restlessness of males did not increase either during or after exposure to other males, and the probability of dispersing across an inhospitable environment was unaffected by the presence of another male. The difference between females and males may be related to differences in dispersal ability and in the abundance and distribution of hosts versus mates.


Genetics ◽  
1983 ◽  
Vol 105 (4) ◽  
pp. 881-896
Author(s):  
John M Belote

ABSTRACT The male-specific lethal mutations (msl's) identify loci whose wild-type gene products are essential for male, but not female, viability. Earlier studies in which X-linked gene activities were monitored in msl/msl male larvae demonstrated that these genes are responsible for setting and/or maintaining the level of X chromosome transcription in males (i.e., they are necessary for proper dosage compensation). The present study examines several important questions concerning their mode of action during development—The results of an examination of the effects of an msl-1 deficiency on male-lethal phase and female viability suggest that this mutation is an amorph, or a severe hypomorph. The effects of rendering a fly mutant for more than one male-lethal mutation were also examined. Multiply mutant flies were no more severely affected than singly mutant ones. A gynandromorph analysis revealed that the male-limited lethality associated with msl-2 has no single lethal focus. Somatic clones of homozygous msl-2 cells were initiated at various times during development by X-ray-induced mitotic recombination. An examination of the viability, growth patterns and morphology of marked clones demonstrated that: (1) msl-2  + acts in a cell autonomous manner, (2) msl-2  + function is required not only in larval (polytene) cells as was shown in previous work but is also needed in the diploid cells that give rise to adult structures, (3) the msl-2  + gene is needed fairly late in development and perhaps continuously, (4) the msl-2 mutation does not affect sexual differentiation.


Biology ◽  
2022 ◽  
Vol 11 (1) ◽  
pp. 102
Author(s):  
De-Li Shi

Maternal gene products accumulated during oogenesis are essential for supporting early developmental processes in both invertebrates and vertebrates. Therefore, understanding their regulatory functions should provide insights into the maternal control of embryogenesis. The CRISPR/Cas9 genome editing technology has provided a powerful tool for creating genetic mutations to study gene functions and developing disease models to identify new therapeutics. However, many maternal genes are also essential after zygotic genome activation; as a result, loss of their zygotic functions often leads to lethality or sterility, thus preventing the generation of maternal mutants by classical crossing between zygotic homozygous mutant adult animals. Although several approaches, such as the rescue of mutant phenotypes through an injection of the wild-type mRNA, germ-line replacement, and the generation of genetically mosaic females, have been developed to overcome this difficulty, they are often technically challenging and time-consuming or inappropriate for many genes that are essential for late developmental events or for germ-line formation. Recently, a method based on the oocyte transgenic expression of CRISPR/Cas9 and guide RNAs has been designed to eliminate maternal gene products in zebrafish. This approach introduces several tandem guide RNA expression cassettes and a GFP reporter into transgenic embryos expressing Cas9 to create biallelic mutations and inactivate genes of interest specifically in the developing oocytes. It is particularly accessible and allows for the elimination of maternal gene products in one fish generation. By further improving its efficiency, this method can be used for the systematic characterization of maternal-effect genes.


2015 ◽  
Vol 5 (12) ◽  
pp. 2885-2892 ◽  
Author(s):  
Nicola Cook ◽  
Urmi Trivedi ◽  
Bart A. Pannebakker ◽  
Mark Blaxter ◽  
Michael G. Ritchie ◽  
...  

Development ◽  
1998 ◽  
Vol 125 (22) ◽  
pp. 4349-4358 ◽  
Author(s):  
J. Charite ◽  
W. de Graaff ◽  
D. Consten ◽  
M.J. Reijnen ◽  
J. Korving ◽  
...  

Studies of pattern formation in the vertebrate central nervous system indicate that anteroposterior positional information is generated in the embryo by signalling gradients of an as yet unknown nature. We searched for transcription factors that transduce this information to the Hox genes. Based on the assumption that the activity levels of such factors might vary with position along the anteroposterior axis, we devised an in vivo assay to detect responsiveness of cis-acting sequences to such differentially active factors. We used this assay to analyze a Hoxb8 regulatory element, and detected the most pronounced response in a short stretch of DNA containing a cluster of potential CDX binding sites. We show that differentially expressed DNA binding proteins are present in gastrulating embryos that bind to these sites in vitro, that cdx gene products are among these, and that binding site mutations that abolish binding of these proteins completely destroy the ability of the regulatory element to drive regionally restricted expression in the embryo. Finally, we show that ectopic expression of cdx gene products anteriorizes expression of reporter transgenes driven by this regulatory element, as well as that of the endogenous Hoxb8 gene, in a manner that is consistent with them being essential transducers of positional information. These data suggest that, in contrast to Drosophila Caudal, vertebrate cdx gene products transduce positional information directly to the Hox genes, acting through CDX binding sites in their enhancers. This may represent the ancestral mode of action of caudal homologues, which are involved in anteroposterior patterning in organisms with widely divergent body plans and modes of development.


Development ◽  
1993 ◽  
Vol 118 (2) ◽  
pp. 499-507 ◽  
Author(s):  
H. Steinbeisser ◽  
E.M. De Robertis ◽  
M. Ku ◽  
D.S. Kessler ◽  
D.A. Melton

In this study, we compare the effects of three mRNAs-goosecoid, activin and Xwnt-8- that are able to induce partial or complete secondary axes when injected into Xenopus embryos. Xwnt-8 injection produces complete secondary axes including head structures whereas activin and goosecoid injection produce partial secondary axes at high frequency that lack head structures anterior to the auditory vesicle and often lack notochord. Xwnt-8 can activate goosecoid only in the deep marginal zone, i.e., in the region in which this organizer-specific homeobox gene is normally expressed on the dorsal side. Activin B mRNA, however, can turn on goosecoid in all regions of the embryo. We also tested the capacity of these gene products to restore axis formation in embryos in which the cortical rotation was blocked by UV irradiation. Whereas Xwnt-8 gives complete rescue of anterior structures, both goosecoid and activin give partial rescue. Rescued axes including hindbrain structures up to level of the auditory vesicle can be obtained at high frequency even in the absence of notochord structures. The possible functions of Wnt-like and activin-like signals and of the goosecoid homeobox gene, and their order of action in the formation of Spemann's organizer are discussed.


Science ◽  
1982 ◽  
Vol 215 (4536) ◽  
pp. 1133-1134 ◽  
Author(s):  
S. W. SKINNER

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