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Expression of Dorsal-Ventral Genes During Early Development of Rhynchosciara Americana Embryos

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Expression of Dorsal-Ventral Genes During Early Development of Rhynchosciara Americana Embryos Brazilian Journal of Medical and Biological Research (2005) 38: 27-31 Expression of dorsal ventral genes in R. americana 27 ISSN 0100-879X Short Communication Expression of dorsal-ventral genes during early development of Rhynchosciara americana embryos J.C. Carvalho, D.N. Rocha, Laboratório de Biologia Molecular Maury Miranda, R.V. Bruno, Instituto de Biofísica Carlos Chagas Filho, C.E. Vanario-Alonso Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brasil and E. Abdelhay Abstract Correspondence The establishment of dorsal-ventral polarity in Drosophila is a com- Key words E. Abdelhay plex process which involves the action of maternal and zygotically • Rhynchosciara americana Laboratório de Biologia Molecular expressed genes. Interspecific differences in the expression pattern of • Lower dipteran Maury Miranda, IBCCF, CCS some of these genes have been described in other species. Here we • Axis patterning Bloco G, Sala G-59 present the expression of dorsal-ventral genes during early embryo- • Dorsal-ventral genes 21949-900 Rio de Janeiro, RJ • Early embryogenesis Brasil genesis in the lower dipteran Rhynchosciara americana. The expres- Fax: +55-21-2280-8193 sion of four genes, the ventralizing genes snail (sna) and twist (twi) E-mail: [email protected] and the dorsalizing genes decapentaplegic (dpp) and zerknüllt (zen), was investigated by whole-mount in situ hybridization. Sense and Presented at the XI Congresso antisense mRNA were transcribed in vitro using UTP-digoxigenin and Brasileiro de Biologia Celular, hybridized at 55°C with dechorionated fixed embryos. Staining was Campinas, SP, Brazil, July 15-18, obtained with anti-digoxigenin alkaline phosphatase-conjugated anti- 2004. body revealed with NBT-BCIP solution. The results showed that, in Research supported by CNPq, CAPES general, the spatial-temporal expression of R. americana dorsal- and PRONEX. ventral genes is similar to that observed in Drosophila, where twi and sna are restricted to the ventral region, while dpp and zen are expressed in the dorsal side. The differences encountered were subtle and probably represent a particular aspect of dorsal-ventral axis determi- Received May 27, 2004 nation in R. americana. In this lower dipteran sna is expressed slightly Accepted October 19, 2004 later than twi and dpp expression is expanded over the lateral ectoderm during cellular blastoderm stage. These data suggest that the establish- ment of dorsal-ventral polarity in R. americana embryos follows a program similar to that observed in Drosophila melanogaster. The establishment of dorsal-ventral po- with the localization of dorsal protein exclu- larity in Drosophila embryos is a complex sively in the ventral nuclei of the embryo (1). process which involves the action of mater- The dorsal gene plays a particularly cru- nal and zygotically expressed genes. The cial role in the specification of dorsal-ventral first step in the establishment of the dorsal- positional identities during early develop- ventral axis is the migration of the oocyte ment. The gradient of nuclear dorsal protein nuclei to a dorsal anterior position. In this functions as a morphogen that directly acti- position the nuclei initiate a cascade of inter- vates or represses the transcription of tissue- and intracellular signaling that culminates specific genes in the pathway (2). Along the Braz J Med Biol Res 38(1) 2005 28 J.C. Carvalho et al. ventral midline, where the concentration of pattern of expression of some zygotic genes nuclear Dorsal protein is the highest, twist of the dorsal-ventral system in the lower (twi) and snail (sna) are activated in the dipteran R. americana. In this species the presumptive mesoderm. Dorsally, the activ- pattern of expression of segmentation genes ity of Dorsal is so low that it can neither (gap genes) is quite different from those activate twi and sna nor repress decapen- observed in higher dipterans (Carvalho JC, taplegic (dpp) and zerknüllt (zen), so that Rocha DN, Vanario-Alonso CE and Abdel- only dpp and zen are expressed. The hay E, unpublished results). R. americana dorsalizing genes dpp and zen are respon- shows important differences in several stages sible for the differentiation of dorsal ecto- of embryogenesis when compared to Droso- dermal derivatives, including the amniose- phila (11). R. americana has a very long rosa and dorsal epidermis (3-6). twi, sna, development. At 22ºC, embryos hatch after zen, and dpp are direct targets of Dorsal, and 12 days in comparison to the 24 h taken by their regulation represents the earliest subdi- Drosophila embryos and present an unusual vision of the dorsal-ventral axis into discrete developmental pattern, which combines some regions of zygotic gene expression. conserved characteristics similar to early and Homologues of maternal dorsal-ventral late Drosophila development with a differ- system genes have been described only in ent mid-stage (11). Rhynchosciara presents some dipterans while homologues for zy- an intermediate step between blastoderm gotic genes of this system were also identi- formation and gastrulation. After cellular- fied in other species of arthropods and some ization the blastoderm starts to differentiate chordates (7). These findings suggest that into a short embryonary primordium and an dorsal-ventral patterning occurs according extraembryonary membrane (11). This dif- to a common genetic control in different ferentiation culminates in a strong spatial organisms. However, interspecific differ- cellular polarization which divides the em- ences in the pattern of dorsal-ventral gene bryo into a vegetative pole - rich in germplasm expression exist and have been well docu- with few cells - and a germinative pole that mented for insects such as Tribolium and contains the embryo primordium, which is Schistocerca gregaria (8-10). very condensed in this species (11). How- In the present study, we analyzed the ever, interestingly, the data obtained in the present study suggest that the genetic control Figure 1. Phylogenetic tree of the dorsal-ventral axis seems to be re- showing the closeness of the Drosophila markably conserved in R. americana, with species considered in the pres- (Drosophilidae) some minor differences probably due to var- ent study. Adapted from Rohr et Musca al. (14). (Muscidae) iations in gene regulation. Megaselia (Phoridae) To analyze these expression patterns, R. Rhynchosciara (Sciaridae) Diptera americana embryos were staged according Coboldia (Scatopsidae) to Carvalho et al. (11) and whole-mount in Clogmia situ hybridization was performed as described (Psychodidae) Nematocera Brachycera Psychoda by Tautz and Pfeifle (12), except that em- (Psychodidae) bryo hybridization and washing were per- Hymenoptera formed at 50ºC. Drosophila cDNA probes for the genes under study were obtained Tribolium Coleoptera from Dr. Stephen Small (New York Univer- sity) and were used to transcribe sense and Schistocerca Orthoptera antisense RNA probes. We used sense RNA under the same stringency and temperature Braz J Med Biol Res 38(1) 2005 Expression of dorsal ventral genes in R. americana 29 conditions as control and no labeling could be detected. The photographic images were digitized and then edited electronically us- ing Adobe Photoshop software. We examined the expression of twi, sna, dpp, and zen in the early embryogenesis of R. americana. For whole-mount in situ hybrid- ization we used anti-sense mRNA probes obtained from D. melanogaster cDNAs. Given the phylogenetic closeness of the two species (Figure 1), the use of heterologous probes suited our purpose and we were able to analyze the expression of all four genes. sna gene expression was detected during a short period of R. americana early embryo- genesis. This expression was confined to the syncytial blastoderm stage (8 h) and sna transcripts were localized in the ventral re- gion of the embryo (Figure 2A). Expression of twi mRNA was also detected in the ventral region of the embryo, although at a later time (12-18 h). twi gene expression was detected during blastoderm cellularization of embryo nuclei (Figure 2B). These results contrast with those obtained for Drosophila, in which both the sna and twi genes are initially ex- pressed at the 11th nuclear cleavage (4). In Drosophila, the cellular blastoderm forms during the 14th mitotic cycle and thus sna and twi are expressed early in the syncytial blastoderm. This temporal difference in twi expression could be related to the longer embryogenesis of R. americana. Probably the temporal regulation of sna and twi ex- pression in R. americana is more evident than in Drosophila due to the longer time taken by cellularization (24 h in R. americana versus 4 h in D. melanogaster). In Drosophila, Dorsal directly activates sna and twi expression and the width of the sna domain depends on twi. However, the Figure 2. Analysis of dorsal-ventral gene expression in a Rhynchosciara americana embryo initiation of twi expression is essentially nor- by whole-mount in situ hybridization. Anterior is to the left. A-B, sna and twi mRNA distribution in the syncytial blastoderm (8 h) and cellularization of nuclear blastoderm (12-18 mal in sna mutant embryos and the initiation h) stages, respectively. C-D, sna and twi expression in a Drosophila melanogaster embryo of sna expression is normal in twi mutant during the cellular blastoderm stage. E-F, dpp mRNA distribution in mid-cellular blastoderm embryos (6). Thus, the temporal difference stages of R. americana and D. melanogaster embryos, respectively. G-H, zen mRNA distribution during the early cellular blastoderm (24 h) and late cellular blastoderm stage observed in R. americana for sna and twi (48 h) of an R. americana embryo, respectively. I, zen expression in a D. melanogaster expression is a particular aspect of this spe- embryo during the late cellular blastoderm stage. Braz J Med Biol Res 38(1) 2005 30 J.C. Carvalho et al. cies that reflects a modification in the way dorsal side of the embryo (11). these genes are regulated. Nevertheless, we In Drosophila, dpp and zen are expressed can say that the expression of the sna and twi in a region of the same extension.
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