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Arthropod Embryogenesis FlyFISH h7ps://www.mpi-cbg.de/research-groups/current-groups/pavel-tomancak/open-access/ Lecture Outline • Two (main) modes of arthropod embryogenesis • Drosophila embryogenesis • Drosophila axis formaon and segmentaon • What geneIc aspects of arthropod development are conserved? Short vs. Long embryo • The mechanisms of embryo arthropod embryogenesis occur via one of two embryo mechanisms, the “long- embryo germ” mode, or the embryo “short germ” mode. embryo embryo – Short germ: only a small porIon of the egg embryo embryo embryo becomes the embryo (more ancestral). – Long germ: the majority embryo embryo embryo of the egg becomes the Long Germ-Drosophila (Parkhurst Lab) embryo (derived and has evolved in mulIple lineages secondarily). embryo Short Germ-Tribolium (Tautz et al. 1999) Short vs. Long Nakamura et al. 2010 Tomer et al. 2012 Insect Embryogenesis in Drosophila melanogaster • Why Drosophila? – The geneIc tools available for Drosophila have allowed for the discovery of geneIc mechanisms controlling animal development. – Early work by Ed Lewis, ChrisIane Nusslein-Volhard and Eric Weischaus led to them being awarded the Nobel Prize in Physiology or Medicine in 1995. Insect Ovaries • Insect ovaries are composed of many smaller units known as “ovarioles.” Wikimedia Commons Hyalophora cecropia, Telfer 2009 Three Types of Insect Ovarioles • Three insect ovariole types • Polytrophic merois/c (A), in which each oocyte is associated with nurse cells. • Telotrophic meroisc (B) in which the oocytes are aached to the terminal nurse cells. • Panois/c (C) in which there are no nurse cells. Jeremy A. Lynch, and Siegfried Roth Genes Dev. 2011;25:107-118 The Drosophila Ovariole The Drosophila Life Cycle Early Embryonic Events: Pre-ferIlizaon Nurse Cells Load Axial Determinants and Germline Components into the Oocyte St. Johnston 2005 Dorso/Ventral Axes Formaon •Gurken/Egfr signaling is used to establish the dorso-ventral axis before ferIlizaon in Drosophila. •gurken mRNA is localized around the asymmetrical oocyte nucleus. •A`er translaon, Gurken protein signals to the overlying follicle cells via the Egfr receptor to demark the future dorsal side of the embryo. Gilbert et al. 2014 A/P Axis Formaon in the FerIlized Egg Sanson 2002 bicoid and Nanos mRNA translate Into Protein Gradients Porcher et al. 2010 nanos mRNA Nanos Protein Dahunakar and Wharton 1996 Bicoid Phenotype •Depleon of bicoid mRNA causes a mirror image of the posterior in the anterior. •Arrowheads point to the “filzkorper,” which are structures on the 8th abdominal segment. Staller et al. 2015 Bicoid and Nanos Protein Gradients and the Establishment of Gap Gene boundaries Sanson 2002 hunchback (hb) and cuadal (cad) Are Maternally Ubiquitous •Bicoid protein inhibits caudal translaon •Nanos protein inhibits the translaon of hunchback mRNA •Bicoid protein also acIvates zygoIc hunchback translaon in the anterior. •The hunchback gene contains mulIple occupancy sites for Bicoid protein which are needed for its anterior translaon. Carroll et al. 2004 Drosophila Gap Genes • These genes are named for the “gap” in segments caused by their mutaon. • The coordinates of gap gene expression are controlled by the read-out of maternal gene expression boundaries • Controlled by the differenIal use of enhancers in the gap genes. Nuslein-Volhard and Wieschaus, 1980 Pair-rule Genes Sanson 2002 The Pair-rule Genes • The expression of these genes occur in stripes that correspond to future segments. • There are 7 stripes, Carroll et al. 2004 each alternang for every other segment boundary even-skipped (eve) Mutaons even-skipped mutaons cause a loss in every other segment Manoukian and Krause 1992 How Do We Go From an Aperiodic Gap Gene to Periodic Gene Expression? • Aperiodic gap and maternal genes establish the periodic expression of the 7 stripes of the primary pair-rule genes. • This is accomplished, again, by the “read- out” of the maternal and gap gene coordinate system on the pair-rule gene enhancers. • Each stripe of expression is formed by the binding of maternal and gap gene protein products. Carroll et al. 2004 Gilbert et al. 2014 Segment Polarity Genes Sanson 2002 Segment Polarity Genes • These are expressed in 14 stripes (7x2). • These demark the anterior and posterior boundaries of the final segments. • These are iniIally controlled by pair-rule gene acIvity, but later interact with one another to refine their boundaries. Carroll et al. 2004 Segment Polarity Genes Kornberg 1980 In Summary… Carroll et al. 2004 How Much of This is Conserved in Other Arthropod Groups? Peel et al. 2005 Maternal Effect Genes • bicoid is a derived Hox3 gene, as seen in other arthropods, like the mite, where it is expressed as a Hox gene. • Many other insects rely on the funcon of orthoden>cle orthologs to paern their head regions; bicoid may have been co-opted for this in the fly lineage leading to Archegozetes longisetosus; Telford and Thomas 1998 Drosophila. • The role of nanos in other arthropods is less clear, but it is localized to the posterior of Schistocerca oocytes. Schistocerca belongs to a basally branching Schistocerca americana; Lall et al. 2003 group of insects. Gap Genes- “Gap” funcIon is Likely Restricted to Insects engrailed abdominal-A hb RNAi in the beetle Tribolium castaneum; bucher et al. 2004 Pair-rule Gene Conservaon? • Orthologues of Drosophila pair- rule genes are expressed in segmental paerns in every paired arthropod group, however the do not always display double-segment periodicity. • The cenpede Strigamia mari>ma uses paired and sloppy-paired orthologues in a pair-rule manner. sloppy-paired Green and Akam 2013 Segment Polarity Genes? • The expression of the segment polarity genes has the highest level of conservaon across arthropods engrailed expression; Carroll et al., 2004 Conclusions • Drosophila provides a useful model to understand the maternal contribuIon to axial paerning • Drosophila dorso-ventral paerning is iniIated in the oocyte via Gurken and Egfr signaling. • Drosophila antero-posterior paerning progresses from maternally-derived factors to the acIvaon of gap genes, to pair-rule genes and lastly to the segment-polarity genes. • The acIvaon of these gene classes stems from their “read-out” of the posiIonal informaon that was provided previously. • In terms of evoluIonary conservaon, the gap genes likely evolved in the insect lineage, however the engrailed/ wingless segment-polarity pathway is widely conserved in all arthropod groups. .
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