Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila.

Harding, Katherine; Hoey, Timothy; Warrior, Rahul; Levine, Michael

doi:10.1002/j.1460-2075.1989.tb03493.x

Cited by 246 publications

(165 citation statements)

References 38 publications

(62 reference statements)

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“…Second, the mechanism appears to be specifically targeted to the derepression of the 1-2 interstripe in wild-type males since the MSE line, which has lost the derepression, has defective En patterning. One hypothesis for a downstream buffering mechanism is eve autoregulation (Harding et al 1989) because we observe a smaller median shift of relative repression between males and females with two eve doses ( Figure 2B, 8%) than with one eve dose (22%). Alternatively, the differential expression of gt may induce sex-specific expression in other pair-rule genes, which in turn could compensate for sex-specific eve expression in the regulation of the segment polarity genes.…”

Section: Discussionmentioning

confidence: 70%

Sex-Specific Pattern Formation During Early Drosophila Development

2013

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The deleterious effects of different X-chromosome dosage in males and females are buffered by a process called dosage compensation, which in Drosophila is achieved through a doubling of X-linked transcription in males. The male-specific lethal complex mediates this process, but is known to act only after gastrulation. Recent work has shown that the transcription of X-linked genes is also upregulated in males prior to gastrulation; whether it results in functional dosage compensation is not known. Absent or partial early dosage compensation raises the possibility of sex-biased expression of key developmental genes, such as the segmentation genes controlling anteroposterior patterning. We assess the functional output of early dosage compensation by measuring the expression of even-skipped (eve) with high spatiotemporal resolution in male and female embryos. We show that eve has a sexually dimorphic pattern, suggesting an interaction with either X-chromosome dose or the sex determination system. By manipulating the gene copy number of an X-linked transcription factor, giant (gt), we traced sex-biased eve patterning to gt dose, indicating that early dosage compensation is functionally incomplete. Despite sex-biased eve expression, the gene networks downstream of eve are able to produce sex-independent segmentation, a point that we establish by measuring the proportions of segments in elongated germ-band embryos. Finally, we use a whole-locus eve transgene with modified cis regulation to demonstrate that segment proportions have a sexdependent sensitivity to subtle changes in Eve expression. The sex independence of downstream segmentation despite this sensitivity to Eve expression implies that additional autosomal gene-or pathway-specific mechanisms are required to ameliorate the effects of partial early dosage compensation. IN Drosophila, dosage compensation occurs by an upregulation of transcription from the X chromosome in males (Mukherjee and Beermann 1965;Belote and Lucchesi 1980;Straub et al. 2005). The best-characterized mechanism of upregulation depends on the male-specific activity of the malespecific lethal (MSL) complex (Gelbart and Kuroda 2009), which binds to sites on the X chromosome and enhances the rate of transcript elongation (Larschan et al. 2011). MSL activity is inhibited in females by the translational repression of Msl2 protein, which is necessary for complex formation, by the protein product of the sex-determination gene Sex-lethal (Sxl) (Kelley et al. 1995). The canonical MSL-dependent mechanism does not appear to be active prior to gastrulation as msl2 transcript is not detected until cleavage cycle 14 (Lott et al. 2011) and the earliest expression of Msl3 protein in male embryos is detected only at stage 6 (gastrulation) (Rastelli et al. 1995;Franke et al. 1996;Cline 2005).Despite the lack of MSL-dependent dosage compensation during the blastoderm stage, the transcription of X-linked genes expressed before gastrulation is, in fact, elevated in males (Lott et al. 2011). With the exc...

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Section: Discussionmentioning

confidence: 70%

Sex-Specific Pattern Formation During Early Drosophila Development

2013

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“…The basis for such pattern formationreaction-diffusion coupling -was described by Turing more than half a century ago (Turing, 1952) and is the subject of several recent accessible presentations (Forgacs and Newman, 2005, Meinhardt and Gierer, 2000, Miura and Maini, 2004. The basic notion is that a diffusible, positively autoregulatory "activator" (e.g., the Even-skipped transcription factor in the syncytial Drosophila embryo (Harding et al, 1989), or TGF-β in limb bud mesenchyme, Miura and Shiota, 2000b) will tend, if unconstrained in its action, to create an explosive, spreading front of its own production and any downstream effects of its activity. If, however, the activator also induces in the same population of cells an inhibitor of its action that diffuses or otherwise spreads faster than the activator itself, there will be a zone around any peak of activation within which no activation can occur.…”

Section: Reaction-diffusion Couplingmentioning

confidence: 99%

Before programs: The physical origination of multicellular forms

Newman¹,

Forgács²,

Müller³

2006

Int. J. Dev. Biol.

160

118

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By examining the formative role of physical processes in modern-day developmental systems, we infer that although such determinants are subject to constraints and rarely act in a "pure" fashion, they are identical to processes generic to all viscoelastic, chemically excitable media, non-living as well as living. The processes considered are free diffusion, immiscible liquid behavior, oscillation and multistability of chemical state, reaction-diffusion coupling and mechanochemical responsivity. We suggest that such processes had freer reign at early stages in the history of multicellular life, when less evolution had occurred of genetic mechanisms for stabilization and entrenchment of functionally successful morphologies. From this we devise a hypothetical scenario for pattern formation and morphogenesis in the earliest metazoa. We show that the expected morphologies that would arise during this relatively unconstrained "physical" stage of evolution correspond to the hollow, multilayered and segmented morphotypes seen in the gastrulation stage embryos of modern-day metazoa as well as in Ediacaran fossil deposits of 600 Ma. We suggest several ways in which organisms that were originally formed by predominantly physical mechanisms could have evolved genetic mechanisms to perpetuate their morphologies.

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“…This construct expresses lacZ in three (2, 3, and 7) of the seven normal eve stripes in the early embryo (Harding et al 1989). We used the eve 5.2-kb lacZtransformed strain in reciprocal crosses to the Lk-P(1A) P-cytotype strain.…”

Section: P Cytotype Does Not Repress Heterologous Promoters In Somatimentioning

confidence: 99%

P-element repressor autoregulation involves germ-line transcriptional repression and reduction of third intron splicing.

Roche

Schiff²,

Rio³

1995

Genes Dev.

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P cytotype is a regulatory state, characteristic of Drosophila P-strain females, in which P-element transposition is repressed. P cytotype is established maternally in the germ line but is also dependent on the presence of P elements in the zygote. One aspect of P cytotype involves transcriptional repression of the P-element promoter. Here, we show that transcriptional repression by P cytotype in the female germ line occurs by a general promoter-independent mechanism with heterologous promoters carried in P-element vectors. P-cytotype transcriptional repression results in low levels of pre-mRNA and a reduction in splicing of the P-element third intron (IVS3)-containing mRNA, thus causing an increase in the proportion of 66-kD repressor mRNA. Increased retention of IVS3 in P cytotype would result in an autoregulatory loop of 66-kD repressor production. This combination of germ-line transcriptional repression and splicing control provides a mechanism to maintain repression during the maternal inheritance of P cytotype. These findings suggest that transcriptional repression may play an additional role in the regulation of gene expression, namely allowing alteration of pre-mRNA splicing patterns.[Key Words: Tissue specificity; germ-line transcriptional control; pre-mRNA splicing regulation; germ-lineReceived January 25, 1995; revised version accepted April 13, 1995. P element transposition in Drosophila is controlled in two ways: (1) transposition is restricted to the germ line by alternative RNA splicing (tissue specificity), and (2) transposition only occurs when a P-strain male (carrying P elements} is mated to an M-strain female (lacking P elements) but does not occur in the reciprocal cross. P-strain females are said to possess "P cytotype," the regulatory state by which transposition is repressed. P cytotype is initially inherited maternally and in a manner similar to cytoplasmic inheritance but is ultimately determined zygotically by the presence of chromosomal P elements (for review, see Engels 1983Engels , 1989Rio 1991). At least part of the repressive activity of P cytotype is caused by repressor proteins encoded by the P elements, and this repressive activity can be influenced by genomic position (Robertson and Engels 1989;Misra and Rio 1990;Misra et al. 1993}. Genetic studies of cytotype suggested that repressor synthesis would be autoregulatory in the germ line (Engels 1983; O'Hare and Rubin 1983), but the underlying mechanism has remained elusive.Cytotype repression of P-element mobility has both maternal and zygotic components (Engels 1983(Engels , 1989. Genetic assays for cytotype have allowed the detection of two types of regulatory P elements. The complete 2.9-kb P elements encode the 66-kD repressor protein (Misra and Rio 1990; Gloor et al. 1993}, whereas the smaller internally deleted elements encode truncated repressor proteins, such as the KP protein (Black et al. 1987;Rasmusson et al. 1993). Complete P elements are capable of exhibiting the repressive maternal effect of P cytotype, depending o...

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Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila.

Cited by 246 publications

References 38 publications

Sex-Specific Pattern Formation During Early Drosophila Development

Sex-Specific Pattern Formation During Early Drosophila Development

Before programs: The physical origination of multicellular forms

P-element repressor autoregulation involves germ-line transcriptional repression and reduction of third intron splicing.

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