A major role for zygotic hunchback in patterning the Nasonia embryo

Department of Biology, Western Washington University, Bellingham, WA 98225, USA.
Development (Impact Factor: 6.46). 09/2005; 132(16):3705-15. DOI: 10.1242/dev.01939
Source: PubMed


Developmental genetic analysis has shown that embryos of the parasitoid wasp Nasonia vitripennis depend more on zygotic gene products to direct axial patterning than do Drosophila embryos. In Drosophila, anterior axial patterning is largely established by bicoid, a rapidly evolving maternal-effect gene, working with hunchback, which is expressed both maternally and zygotically. Here, we focus on a comparative analysis of Nasonia hunchback function and expression. We find that a lesion in Nasonia hunchback is responsible for the severe zygotic headless mutant phenotype, in which most head structures and the thorax are deleted, as are the three most posterior abdominal segments. This defines a major role for zygotic Nasonia hunchback in anterior patterning, more extensive than the functions described for hunchback in Drosophila or Tribolium. Despite the major zygotic role of Nasonia hunchback, we find that it is strongly expressed maternally, as well as zygotically. Nasonia Hunchback embryonic expression appears to be generally conserved; however, the mRNA expression differs from that of Drosophila hunchback in the early blastoderm. We also find that the maternal hunchback message decays at an earlier developmental stage in Nasonia than in Drosophila, which could reduce the relative influence of maternal products in Nasonia embryos. Finally, we extend the comparisons of Nasonia and Drosophila hunchback mutant phenotypes, and propose that the more severe Nasonia hunchback mutant phenotype may be a consequence of differences in functionally overlapping regulatory circuitry.

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    • "c body region , has also been detected in several insect species , includ - ing the beetle Tribolium castaneum and the cricket Gryllus bimaculatus , and the millipede Glomeris marginata , in which the hunchback domains encompass the presumptive gnathal and / or first thoracic segments ( Tautz et al . 1987 ; Wolff et al . 1995 ; Mito et al . 2005 ; Pultz et al . 2005 ; Janssen et al . 2011 ) ."
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    ABSTRACT: Zinc finger transcription factors encoded by hunchback homologs play different roles in arthropods, including maternally mediated control, segmentation, and mesoderm and neural development. Knockdown experiments in spider and insect embryos have also revealed homeotic effects and gap phenotypes, the latter indicating a function of hunchback as a "gap gene". Although the expression pattern of hunchback has been analysed in representatives of all four major arthropod groups (chelicerates, myriapods, crustaceans and insects), nothing is known about its expression in one of the closest arthropod relatives, the Onychophora (velvet worms). We therefore examined the expression pattern of hunchback in embryos of the onychophoran Euperipatoides rowelli. Our transcriptomic and phylogenetic analyses revealed only one hunchback ortholog in this species. The putative Hunchback protein contains all nine zinc finger domains known from other protostomes. We found no indication of maternally contributed transcripts of hunchback in early embryos of E. rowelli. Its initial expression occurs in the ectodermal tissue of the antennal segment, followed by the jaw, slime papilla and trunk segments in an anterior-to-posterior progression. Later, hunchback expression is seen in the mesoderm of the developing limbs. A second "wave" of expression commences later in development in the antennal segment and continues posteriorly along each developing nerve cord. This expression is restricted to the neural tissues and does not show any segmental pattern. These findings are in line with the ancestral roles of hunchback in mesoderm and neural development, whereas we find no evidence for a putative function of hunchback as a "gap gene" in Onychophora.
    Development Genes and Evolution 06/2015; 225(4). DOI:10.1007/s00427-015-0505-4 · 2.44 Impact Factor
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    • "Nv otd acts in combination with Nv hunchback (hb) and localized maternal Nv giant (gt) at the anterior, and with localized maternal Nv caudal (cad) at the posterior, to specify positional identity. The domains of zygotic expression of Nv hb, Nv gt, Nv cad, Nv Krüppel (Kr), Nv tailless (tll), and Nv knirps (kni) closely resemble their Drosophila counterparts, consistent with a similar mode of blastoderm allocation (Pultz et al., 2005; Lynch et al., 2006; Olesnicky et al., 2006; Brent et al., 2007). Although these data support Drosophila-like early regulatory interactions and a long germ mode of embryogenesis, little was known about later stages of Nasonia embryonic patterning. "
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    ABSTRACT: Embryonic anterior-posterior patterning is well understood in Drosophila, which uses 'long germ' embryogenesis, in which all segments are patterned before cellularization. In contrast, most insects use 'short germ' embryogenesis, wherein only head and thorax are patterned in a syncytial environment while the remainder of the embryo is generated after cellularization. We use the wasp Nasonia (Nv) to address how the transition from short to long germ embryogenesis occurred. Maternal and gap gene expression in Nasonia suggest long germ embryogenesis. However, the Nasonia pair-rule genes even-skipped, odd-skipped, runt and hairy are all expressed as early blastoderm pair-rule stripes and late-forming posterior stripes. Knockdown of Nv eve, odd or h causes loss of alternate segments at the anterior and complete loss of abdominal segments. We propose that Nasonia uses a mixed mode of segmentation wherein pair-rule genes pattern the embryo in a manner resembling Drosophila at the anterior and ancestral Tribolium at the posterior.
    eLife Sciences 03/2014; 3(3):e01440. DOI:10.7554/eLife.01440 · 9.32 Impact Factor
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    • "Such ubiquitous expression is unusual (Liu and Kaufman, 2004a; Nakamura et al., 2010), and may indicate that Ap-hb has a role in establishing or in maintaining the growth zone or that Ap-hb RNA is under translational control at this stage of embryogenesis. Translation of hb RNA is regulated by nos in Drosophila (Irish et al., 1989; Sonoda and Wharton, 1999) and nos response elements (NREs) are found in the 3 0 UTR of hunchback in many insect species (Huang et al., 2010; Pultz et al., 2005) including the Ap-hb 3 0 UTR (Huang et al., 2010). The different 3 0 UTRs we have identified in viviparous and oviparous oogenesis do not contain either of these NREs. "
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    ABSTRACT: The pea aphid (Acyrthosiphon pisum) can reproduce either sexually or asexually (parthenogenetically), giving rise, in each case, to almost identical adults. These two modes of reproduction are accompanied by differences in morphology of the ovaries and the developmental environment, with sexual forms producing eggs that are laid, whereas asexual development occurs within the mother. Here we examine the effect each mode of reproduction has on the expression of key maternal and axis patterning genes; orthodenticle (otd), hunchback (hb), caudal (cad) and nanos (nos). We show that three of these genes (Ap-hb, Ap-otd and Ap-cad) are expressed differently between the sexually and asexually produced oocytes and embryos of the pea aphid. We also show, using immunohistochemistry and cytoskeletal inhibitors, that Ap-hb RNA is localized differently between sexually and asexually produced oocytes, and that this is likely due to differences in the 3' untranslated regions of the RNA. Furthermore, Ap-hb and Ap-otd have extensive expression domains in early sexually produced embryos, but are not expressed at equivalent stages in asexually produced embryos. These differences in expression likely correspond with substantial changes in the gene regulatory networks controlling early development in the pea aphid. These data imply that in the evolution of parthenogenesis a new program has evolved to control the development of asexually produced embryos, whilst retaining the existing, sexual, developmental program. The patterns of modification of these developmental processes mirror the changes that we see in developmental processes between species, in that early acting pathways in development are less constrained, and evolve faster, than later ones. We suggest that the evolution of the novel asexual development pathway in aphids is not a simple modification of an ancestral system, but the evolution of two very different developmental mechanisms occurring within a single species.
    Developmental Biology 02/2013; 377(1). DOI:10.1016/j.ydbio.2013.01.036 · 3.55 Impact Factor
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