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Hedgehog Shows The HIGHLIGHTS GENE REGULATION Although it is known that fertilization protein synthesis, indicating that pre- triggers events that ultimately lead to exisiting factors in one or both the transcriptional activation of the gametes regulate the expression of Probing zygotic gene control zygotic genome, we know surprisingly these genes. As zygote maturation little about these events — a factor continues, zygotes clump together to that probably contributes to the low form large aggregates and mt−-derived success rates of current mammalian- choloroplasts are selectively degraded cloning efforts. So, to investigate the — zygotes germinate on return to a mechanisms that control zygotic gene nutrient-rich medium. transcription, Zhao et al. turned to The previous finding that GSP1 Chlamydomonas reinhardtii — a uni- is present only in mt+ gametes led cellular alga — in which early zygotic the authors to consider it as a candi- development is easier to study. Here date regulator of zygotic gene tran- they report that the gamete-specific, scription in Chlamydomonas. To test homeodomain protein GSP1 can acti- this, they expressed gsp1 in mt− cells, vate the transcription of some zygotic and found that although the vegeta- genes in the absence of gamete fusion. tive mt− transformants appeared Their findings show that both gametes normal, they formed zygote-like contribute proteins that are required aggregates on undergoing gameto- for zygote development. genesis — a behaviour not seen in Chlamydomonas’s quirky life cycle transformed mt+ cells. The trans- makes it amenable to studies of fertil- formed mt− gametes expressed six ization. Upon nutrient starvation, its out of seven zygote-specific genes — haploid vegetative cells of two mating the unexpressed gene, ezy1,is types — mt− and mt+ — undergo thought to be required for mt− gametogenesis. When gametes of chloroplast destruction. Its lack of opposite mating type meet, they fuse expression in mt− transformants together (see picture), triggering rapid indicates that it is under separate zygote-specific gene expression. This regulatory control or perhaps is Courtesy of William Snell, University of Texas Southwestern, USA. expression occurs independently of imprinted in mt− gametes. DEVELOPMENTAL BIOLOGY that germ cells were drawn to ectopic SGP cells newly induced by Hh — is unlikely, as the Hh-expressing cells were negative for a SGP-cell-specific marker. Hedgehog shows the way If germ cells respond directly to Hh, rather than to a secondary signal, then it follows that the germ line should require cell- Cells that originate in one place in the attractive signals derived from the SGP autonomous components of the Hh pathway embryo often have to migrate some cells, and that the identity of such for proper migration. Indeed, when mutant distance to reach their ultimate place of molecules could best be found by looking for positively acting members of the pathway residence. A good example of this is the at genes involved in specifying SGP cell (such as smoothened or fused), germ cells Drosophila germ cells. These cells are fate. Of several such genes, Hh seemed a scattered randomly specified by maternal factors and lie particularly promising candidate — it and failed to outside the posterior of the embryo, is expressed in the SGPs (as shown segregated from the soma until by the distribution of gastrulation. At this stage, they undergo a Hh–lacZ) and is known to complex pattern of migration that brings be a short- and long-range them inside the embryo and into contact signalling molecule. A with two lateral clusters of somatic gonadal crucial experiment precursor (SGP) cells — an association that reinforced this creates a functional gonad. But how do prediction: when germ cells know where to go? In their study Hh was ectopically of this process, Girish Deshpande and expressed in the colleagues have found that, by secreting embryo, using four Hedgehog (Hh), SGP cells could provide different Gal4 drivers, it the attractive cue that guides germ cells to redirected the migration of their destination. a subset of germ cells towards The study, published in Cell, was based on the new source of Hh. An the premise that germ cells would follow alternative explanation for these results — 830 | NOVEMBER 2001 | VOLUME 2 www.nature.com/reviews/genetics © 2001 Macmillan Magazines Ltd But if GSP1 regulates zygote- specific genes in mt− cells, why does it not affect zygotic gene expression in mt+ gametes? Perhaps this is because, as the authors suggest, zygote-specific gene promoters are inaccessible to GSP1 in mt+ gametes or because GSP1 associates with a pre-existing mt–-specific partner molecule to form a transcription-regulatory complex that activates zygote-specific gene expression. The parallels between these events and those in budding yeast indicate that atypical, gamete- specific, homeodomain proteins, such as GSP1 and budding yeast’s MATα2, might have evolved to act as regula- tors of zygotic gene expression before animals and plants diverged. If so, HUMAN GENETICS The starting point for the second study, by then such studies could inform our Mehmet Sözen et al., was their earlier finding of a understanding of how zygote gene gene responsible for the inherited CL/P-ectodermal expression is controlled in mammals. Closing in on dysplasia syndrome (CLPED1), an autosomal- Jane Alfred recessive disorder attributable to mutations in the References and links palatal disorders poliovirus receptor-related 1 gene, PVRL1. In the ORIGINAL RESEARCH PAPER Zhao, H. et al. Venezuelan community on Margarita Island that Ectopic expression of a Chlamydomonas mt+- − they studied, CLPED1 is very frequent and is specific homeodomain protein in mt gametes The formation of the lip and palate is a complex and initiates zygote development without gamete fusion. delicate process in craniofacial development, requir- caused by homozygosity for the PVRL1 nonsense Genes Dev. 15, 2767–2777 (2001) ing the careful joining of tissues from two opposite mutation, W185X. Because the level of sporadic WEB SITE The Chlamydomonas genome database: sides of the mouth. Cleft lip/palate (CL/P) — in CL/P is also high on this island, the authors were http://www.biology.duke.edu/chlamy_genome/ which the lip and palate have failed to close — affects curious to find out whether the same W185X vari- up to 0.2% of live births, with most instances occur- ant was involved in both familial and sporadic ring in families with no history of the disease. forms of CL/P.Although there was no significant However, ~30% of cases occur as part of single-gene difference between the heterozygosity for W185X associate with SGP cells, as if they had lost all sense of direction — syndromes. Understanding the genetics behind this in sporadic CL/P patients and normal, unrelated consistent with loss of Hh. class of common birth disorder has not been easy, islanders, a difference was observed in a population Conversely, patched or protein but the recent identification of two loci, one for CL/P on the adjacent Venezuelan mainland. It seems kinase A mutant germ cells, in and the other for isolated cleft palate (CP), has pro- likely that heterozygosity for W185X is a moderate which Hh signalling is vided clues to the developmental defects that under- genetic risk factor for sporadic CL/P,at least in this constitutively active, clumped lie these malformations. The importance of these population, but is only one of many genetic and together in the middle of the studies is underscored by the finding that mutations environmental contributors. embryo and failed to migrate at all. at the same locus could be responsible for both the The story will not end here, as more susceptibili- Interest in germ-cell migration inherited and sporadic forms of CL/P,indicating a ty loci for CL/P defects will no doubt emerge. For is not new and so several genes model that could lead to the identification of genes all of them, the identification of the molecular that affect this process, such as for other common, complex birth defects. lesion must be followed by a characterization of the wunen and Columbus,have In the first of two studies, Claire Braybrook and resulting developmental pathology. In the case of already been identified. How does co-workers went in search of the causative locus for a PVRL1, which encodes nectin 1 — a cell–cell adhe- Hh fit in with previous models of specific subclass of CP — cleft palate with ankyloglos- sion molecule important for cell fusion — this germ-cell migration? As there are sia (CPX) — which is inherited as a semi-dominant process has already begun. A key message to emerge countless sources of Hh in the X-linked disorder. The locus was delimited to a region from these two papers is that rare developmental embryo, how is specificity of of Xq21; of the three plausible transcripts within the syndromes can indicate candidate loci for more migration achieved? This is candidate interval, only one, the conserved TBX22 common disorders — a strategy that is especially probably only one leg of a longer (T-box 22) gene, was mutated in affected males from welcome when standard mapping approaches are journey to find out how germ an Icelandic family. Mutations in TBX22 — missense, not an option. cells reach their targets. nonsense, splice site and frameshift — were also Tanita Casci Tanita Casci observed in individuals with CPX from five other References and links families of different ethnic backgrounds, and are pre- References and links ORIGINAL RESEARCH PAPER Deshpande, G. ORIGINAL RESEARCH PAPERS Braybrook, C. et al. The T-box et al. Hedgehog signaling in germ cell dicted to cause a complete loss of function of TBX22. transcription factor gene TBX22 is mutated in X-linked cleft palate and migration. Cell 106, 759–769 (2001) This mutation distribution, the expression of TBX22 ankyloglossia. Nature Genet. 29, 179–183 (2001) | Sözen, M.
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