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A Systematic Analysis of the Gap Gene System in the Moth Midge Clogmia Albipunctata

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A Systematic Analysis of the Gap Gene System in the Moth Midge Clogmia Albipunctata Developmental Biology 344 (2010) 306–318 Contents lists available at ScienceDirect Developmental Biology journal homepage: www.elsevier.com/developmentalbiology Evolution of Developmental Control Mechanisms A systematic analysis of the gap gene system in the moth midge Clogmia albipunctata Mónica García-Solache 1, Johannes Jaeger 2, Michael Akam ⁎ Laboratory for Development and Evolution, University Museum of Zoology and Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK article info abstract Article history: The segmentation gene hierarchy of Drosophila melanogaster represents one of the best understood of the Received for publication 22 November 2009 gene networks that generate pattern during embryogenesis. Some components of this network are ancient, Revised 19 April 2010 while other parts of the network have evolved within the higher Diptera. To further understand the Accepted 21 April 2010 evolution of this gene network, we are studying the role of gap genes in a representative of a basally Available online 28 April 2010 diverging dipteran lineage, the moth midge Clogmia albipunctata. We have isolated orthologues of all of the Drosophila trunk gap genes from Clogmia, and determined their domains of expression during the Keywords: Evolution blastoderm stage of development, in relation to one another, and in relation to the expression of even- Segment determination skipped (Calb-eve), a component of the pair-rule system that is directly regulated by the gap genes in Diptera Drosophila.Wefind that hunchback (Calb-hb), Krüppel (Calb-Kr), knirps (Calb-knl), giant (Calb-gt) and tailless Nematocera (Calb-tll) are all expressed in patterns consistent with a gap segmentation role during blastoderm formation, Pattern formation but huckebein (Calb-hkb) is not. In the anterior half of the embryo, the relative positions of the gap gene Gene regulation expression domains in relation to one another, and in relation to the eve stripes, are rather well conserved. In Even-skipped the posterior half of the embryo, there are significant differences. Posteriorly, Calb-gt is expressed only transiently and very weakly, in a domain that overlaps entirely with that of Calb-knl. At late blastoderm stages, none of the candidate genes we have tested is expressed in the region between the posterior Calb-knl domain and Calb-tll. It is likely that the regulation of Calb-eve expression in this posterior region depends on combinations of gap gene factors that differ from those utilised for the same stripes in Drosophila. Both the gap and the pair-rule patterns of gene expression are dynamic in Clogmia, as they are in Drosophila, shifting anteriorly as blastoderm development proceeds. © 2010 Elsevier Inc. All rights reserved. Introduction and in Lepidoptera. It has probably evolved several times, in response to pressure to speed up embryogenesis. All insects develop a segmented germ band, but the context of The situation is somewhat variable in the more basal lineages germ band development is very different in different insect lineages. among the Diptera, i.e. among the paraphyletic grouping generally In many insects, segments are generated after cellularisation, with the referred to as the Nematocera. The relationships of nematoceran more posterior segments being added sequentially, through a process lineages are not well resolved, but the mosquitoes probably represent of terminal growth. This so-called short germ mode of development is an independent derivation of extreme long germ development from seen in all of the basal, hemimetabolous orders, and in some that seen in Drosophila and other cyclorrhaphans (Goltsev et al., holometabolous insects, including some beetles. Most holometabo- 2004). Their embryogenesis is also derived in other respects — for lous insects, however, form their segments almost simultaneously, example, in the expression of the serosal marker zerknüllt (zen) with much of the patterning that underlies segment specification (Goltsev et al., 2007). In contrast, some of the midges, including those occurring while the egg is still a multinucleate syncytium. This so- likely branching near the base of the higher flies, appear to retain a called long germ mode of development is characteristic of the group of semi-long mode of germ band formation, with one or more segments higher flies called cyclorrhaphans, and is best understood in added to the germ band after gastrulation (Rohr et al., 1999), and a Drosophila. However, it is also seen in some beetles, in Hymenoptera more ancestral organisation of the extra-embryonic membranes. The moth midge that we study here, Clogmia albipunctata, is a represen- tative of one such lineage. It may therefore provide a valuable point of ⁎ Corresponding author. Fax: +44 1223 336679. comparison, both with the mosquitoes, and with the cyclorrhaphan E-mail address: [email protected] (M. Akam). flies, that have been studied in more detail. 1 Present Address: Albert Einstein College of Medicine of Yeshiva University, The genetic mechanisms that directly generate segment (and Microbiology and Immunology Department, 1300 Morris Park Avenue, Bronx, NY parasegment) boundaries appear to be conserved among the insects, 10461, USA. 2 EMBL/CRG Research Unit in Systems Biology, CRG — Centre de Regulació Genòmica, and probably more broadly across the arthropods (Patel, 1994). They Universitat Pompeu Fabra (UPF), Dr. Aiguader 88, 08003 Barcelona, Spain. are mediated by segment polarity genes such as engrailed (en) and 0012-1606/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ydbio.2010.04.019 M. García-Solache et al. / Developmental Biology 344 (2010) 306–318 307 wingless (wg), and involve cell–cell communication through signalling in some other closely related cyclorrhaphans, the expression domains of networks, as is typical of patterning in a cellular environment. the gap genes are well conserved (Bonneton et al., 1997; Gregor et al., However, the network of regulators upstream of the segment polarity 2008; Lukowitz et al., 1994; McGregor et al., 2001; Sommer and Tautz, level appears to be less well conserved. Each insect group that has 1991; Treier et al., 1989; Wratten et al., 2006). been studied has evolved its own peculiarities. For example, the The only information available for lower dipterans comes from the initiation of the segmentation process depends on different maternal mosquito Anopheles gambiae (Goltsev et al., 2004), and from an earlier factors in flies, wasps and beetles (Brent et al., 2007; Driever and description of hb and Kr expression in Clogmia albipunctata (Rohr et al., Nüsslein-Volhard, 1988; Lynch et al., 2006a; Olesnicky et al., 2006; 1999). The data for Anopheles show interesting differences when Olesnicky and Desplan, 2007; Schröder, 2003). At the next levels compared with Drosophila. For example, the relative positions of the down in the hierarchy, different species utilise an overlapping but posterior domains of gt and hb appear to be reversed with respect to those distinct set of gap and pair-rule genes to pattern the embryo (Lynch, seen in Drosophila. This implies changes in gap–gap cross-regulation and 2007; Peel, 2008). These aspects of segment patterning are poorly regulation of the pair-rule gene eve in that region of the embryo (Goltsev understood in most insect groups. This present paper is concerned et al., 2004). It is not known if the deduced gap gene interactions in the with the organisation and evolution of this gene network within the mosquito are ancestral for the Diptera or if they are derived. Diptera, and focuses primarily on the level of the gap genes, and their In this paper we describe the gap genes of the nematoceran fly interaction with the pair-rule system. Clogmia albipunctata, a moth midge. We analyse the expression In Drosophila, the gap gene system is essential for establishing the pattern of the trunk gap genes hunchback (Calb-hb), Krüppel (Calb-Kr), first segmental pre-pattern along the antero-posterior (AP) axis of the knirps (Calb-knl) and giant (Calb-gt), and the terminal genes tailless embryo (Hulskamp and Tautz, 1991). The gap genes encode (Calb-tll) and huckebein (Calb-hkb) during embryonic development in transcription factors that are expressed in broad overlapping regions Clogmia, focusing on the last mitotic cycle before cellularisation and of the embryo (Pankratz and Jäckle, 1990). This non-repetitive pattern very early gastrulation. We compare the boundaries of gap gene provides a series of unique transcriptional cues at specific positions expression with the positioning of pair-rule stripes, using even-skipped along the AP axis, which are interpreted by stripe-specific elements in (Calb-eve) as the marker, to assess whether regulatory interactions in the enhancers of the pair-rule genes, to generate a repeating pattern Clogmia may be similar to those defined in Drosophila. of seven stripes of transcription, spaced at double-segment intervals (Pankratz et al., 1990; Reinitz and Sharp, 1995; Small et al., 1991). Materials and methods Combinations of these pair-rule gene products then regulate the segment polarity genes in every segment. Clogmia albipunctata culture and embryo collection Gap gene expression is initiated in broad regions of the embryo by maternally provided gene products including Bicoid (Bcd), Hunch- The flies used in this work came from the culture maintained by back (Hb), Caudal (Cad), and the terminal Torso (Tor) signalling Dr. G. Bucher at the Department of Developmental Biology, Georg cascade
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