Development of Drosophila

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1 Development of Drosophila Hand-out CBT Chapter 2 Wolpert, 5 th edition March 2018 Introduction 6. Introduction Drosophila melanogaster, the fruit fly, is found in all warm countries. In cooler regions, the population is established by migrants during the summer or imported on fuits or by sheltering in warm places. It has been used for genetic experiments since 1909, due to its many advantages: simple and cheap breeding short life cycle high number of offspring The Drosophila research community has developed many genetic tools that are used for research in combination with molecular, cellular and biochemical techniques. 7. Drosophila life cycle 8. First day (1/2) Within just one day the fertilized egg develops from a single cell into a complete and autonomous organism consisting of many different organs. 9. First day (2/2) You will study the first 3 hours of development: the early embryonic stages in the egg. 1

2 Oogenesis 3. Q1A The germarium This is one of the two ovaries of a female fruit fly. In red is one of the ovarioles with at the top the germarium and at the bottom a ripe oocyte.oocytes and eggs are formed in the ovaries of Drosophila. Complete this sentence: The oocyte is formed from one by divisions. 4. Q1B The germarium Complete this sentence: The resulting... other cells form the Q1C The germarium Complete this sentence: The oocyte and these nurse cells are surrounded by Q2A Oocyte position In the developing egg chamber the first sign of symmetry breaking is the movement of the oocyte from a central position to the posterior end of the egg chamber. Signaling from the older to the younger egg chamber is responsible for oocyte anterior-posterior polarity. Complete this sentence: The germline cells in the older egg chamber produce and signal by binding the receptor on follicle cells. 7. Q2B Oocyte position Complete this sentence: This signal specifies the anterior follicle cells to become follicle cells. 8. Q2C Oocyte position Complete this sentence: These cells secrete Unpaired to adjacent follicle cells where the pathway is activated. 9. Q3 Anchoring of oocyte The oocyte is anchored to the posterior by adhesive interaction between the oocyte and the stalk cell posterior to it. Which protein plays an important role in this? 10. Q4 mrna movement "The posterior localization of the oocyt is accompanied by movement of maternal mrna from the anterior end of the oocyte [..] to its future posterior end." (Wolpert et al.). The oocyte is also positioned at the posterior end. Where does the movement of the mrnas depend on? 2

3 11. Q5A Gurken During oogenesis the oocyte moves to one end of the egg chamber. Gurken mrna is translated in the posterior and Gurken protein initiates the specification of terminal follicle cells as polar follicle cells. What type of gene is gurken? 12. Q5B Gurken What is the function of the Gurken protein? 13. Q5C Gurken What is the name of this receptor? 14. Q6 Bicoid and Oskar During oogenesis the gradient for (among others) bicoid and oskar mrna is formed, which will determine the anterior-posterior axis. In which cells are bicoid and oskar mrnas produced? 15. Q7ABicoid This oocyte is stained for Staufen (green) which binds bicoid mrna in the oocyte. The bicoid mrna is not dispersed evenly throughout the cell. What is causing this localization? 16. Q7B Bicoid The cytoskeleton in the oocyte will re-orient its microtubules after the nuclues has moved to the posterior. This results in the transportation of bicoid mrna to the anterior end and oskar mrna to the posterior end of the oocyte. This oocyte is stained for Staufen (green) which binds bicoid mrna at the anterior. Where does the signal to re-orient the microtubules come from? 17. Q8 Dorsal follicle cells At a certain moment the follicle cells nearest to the nucleus specialize as dorsal follicle cells. Which protein from the oocyte causes this? 3

4 Maternal genes 3. Q1A Definition What is the correct definition of maternal factors in Drosophila? 4. Q1B Maternal gene expression Which cells can express maternal genes? 5. Q2A Influence Maternal genes are the genes that are expressed in the cells of the mother and the products of maternal genes have a role in the development of the oocyte or embryo. Mutations in these genes have no effect on the embryonic development of the mother, but only on her progeny. Examples of maternal genes are bicoid and nanos. Which gene products influence the development of the Drosophila embryo? 6. Q2B Localization Maternal genes are the genes that are expressed in the cells of the mother and the products of maternal genes affect the development of the oocyte or embryo. These genes have no effect on the embryonic development of the mother, but only on her progeny. Examples of maternal genes are bicoid and nanos. In the unfertilized egg, the mrnas of these maternal genes are present. Where are the mrna of bicoid and nanos localized in the egg? 7. Q2C Distribution In the unfertilized egg, the mrnas of these maternal genes are present. How are the mrnas of bicoid or nanos kept in these locations, instead of distributed evenly throughout the egg? 8. Q3 Number Drosophila has maternal genes which determine the posterior-anterior axis and genes which determine the dorsal-ventral polarity. How many maternal genes for the posterior-anterior axis have (so far) been discovered? 9. Q4 Anterior-posterior axis There are maternal genes which determine the anterior-posterior axis and genes which determine the dorsal-ventral polarity in the larva. The genes for the anterior-posterior axis are divided in three groups: Group mutations effect example anterior anterior region bicoid posterior posterior region nanos terminal both terminal regions torso 4

5 Each larva is the result of a mutation in one of these genes. Which gene is most probably mutated in each one? 10. Mutants in genes of anterior-posterior axis In mutant 1, the normal structures at the side where the head will be formed are absent; instead a telson has been formed, a structure from the end where the tail will be formed. The side where the tail will be formed looks normal. This is probably a mutant of a maternal gene from the anterior group: bicoid. In mutant 2, the normal structures at both ends are absent. This is a mutant of a maternal gene from the group that affects both terminal sides: torso. In mutant 3, the side where the head will be formed looks normal. The end of the side where the tail will be formed also looks normal, but lacks a number of posterior segments. This is a mutant of a maternal gene from the posterior group: nanos (nanous = dwarf). 11. bicoid mutant In the bicoid mutant embryo the anterior regions are absent. The mutant embryos can be injected at the anterior end with several materials. Injection with which ones of the following materials has the best chance of the embryo developing normally? o anterior cytoplasm from a wild type embryo o bicoid mrna o transcription factors that activate the bicoid gene Q6 nanos and hunchback In this unfertilized egg nanos mrna is present at the posterior end. Nanos helps to establish an anteriorposterior gradient of the Hunchback protein. What are the levels of the hunchback mrna in this Drosophila egg? 5

6 12. Interaction nanos and hunchback Animated graphical representation of Nanos and Hunchback protein levels 13. Q6B Nanos and Hunchback Which of the following mechanisms could Nanos use to influence the Hunchback protein gradient? o preventing translation of the hunchback mrna o degradation of the Hunchback protein o degradation of the hunchback mrna o preventing transcription of hunchback gene 14. Q6C nanos What are the levels of the maternal nanos mrna after fertilization? (You can draw this in the graph ) 15. Q7A Torso Torso is also a maternal gene and mutations in torso affects both anterior and posterior end of the embryo. What is the function of the Torso protein? 16. Q7B Torso The Torso protein is a tyrosine-kinase receptor, present in the plasma membrane. What are the levels of this receptor in a fertilized Drosophila egg plasma membrane? 17. Q7C Torso Why do these receptors only affect the terminal regions of the embryo? 6

7 18. Q7D Torso Receptors in the membrane and ligand in the vitelline envelope are both present before fertilization. Why are these receptors not activated before fertilization? 19. Torso animation The egg of Drosophila is enveloped by a vitelline envelope, consisting of glycoproteins. At the terminal end there is a space between the envelope and the plasma membrane of the egg: the perivitelline space. The receptor protein Torso is distributed evenly through the plasma membrane. Before fertilization the ligand for Torso is also present, but immobilized in the vitelline envelope. After fertilization small amounts of the ligand are transported into the perivitelline space and are able to bind to the receptor. When the Torso receptors form dimers, they will activate a signaling pathway in the cell. This occurs only at the terminal ends. 7

8 Dorso-ventral axis 3. Q1 Gene groups There are four groups of genes or gene products that lead to the subdivision of the fly embryo into segmental entities. Put the gene groups in the order in which they effect the forming of segmentation in Drosophila. 4. Q2 Genes in groups To which group of genes do these genes belong? bicoid wingless even-skipped giant Krüppel 5. Genes Explanation of page Experiment The genes have effect in a certain order, and influence the expression of each other. This gives rise to a certain hierarchy between the genes. Determine the hierarchy of the genes A, B and C by mutant analysis. Determine also whether the interactions are predominantly activating or repressing. Embryo View expression of A View expression of B View expression of C Wildtype Mutant A Mutant B Mutant C 7. Q3A Gene hierarchy What is the hierarchy of genes A, B and C? Q3B Are the interactions predominantly activating or repressing? 8

9 9. Q4A. Transcription factors Which group(s) of genes encode mostly transcription factors? o maternal genes o gap genes o pair-rule genes o segment polarity genes 10. Q4B. Transcription factors What is the reason segment polarity genes do not always encode for transcription factors? 11. Pathway for Dorsal to proceed to nucleus The dorso-ventral axis is determined at the same time as the anterior-posterior axis. There are a lot of proteins involved in this process. Only one of these proteins is not distributed evenly the egg and therefore responsible for setting up the dorso-ventral axis. The Dorsal protein is a transcription factor, which has to go into the nucleus to activate and repress transcription of certain genes involved in dorsoventral polarity. Dorsal is initially bound to Cactus, which prevents it from entering the nucleus. To break down Cactus a signalling pathway has to be activated. The receptors are formed by the Toll proteins. The ligand for this receptor is the Spätzle fragment. This, however, is part of the Spätzle protein, and has to be cleaved from the full length protein before it can act as a ligand. The Spätzle protein is processed by a chain of interactions, including a protease. The pipe gene product is required to localize the protease that cleaves Spätzle.The ventral follicle cells express pipe. Pipe is a sulfotransferase and the enzymatic activity of Pipe leads to a ventrally localized protease activity in the perivitelline space. This protease cleaves Spätzle at the ventral side. A fragment of Spätzle then functions as a ligand for Toll. When the Toll receptor is activated, it binds to the Tube protein. Tube in its turn activates Pelle. Tube and Pelle together are able to break down the Cactus protein, this allows Dorsal to enter the nucleus. 12. Q5A Responsible protein Which of these proteins is known to be expressed by the ventral follicle cells? 13. Q5B Spätzle activation Where is spätzle active? 14. Q5C Maternal Which of these genes are maternal genes? 9

10 15. Q6A Dorsal influence Dorsal enters the nuclei at the ventral side of the embryo. There it activates or suppresses several genes. What is the direct influence of Dorsal on the expression of these genes? Dorsal activates: Dorsal suppresses: 16. Q6B Influence mechanism How does Dorsal influence these genes? 17. Q6C Rhomboid Dorsal is present in a gradient from the ventral side. Dorsal above a certain level activates the expression of snail. Rhomboid is already activated at very low levels of Dorsal, but is suppressed by Snail. What will the levels of Rhomboid be in this Drosophila embryo? 10

11 Parasegmentation and segmentation 3. Q1A Bicoid mrna This is a Drosophila egg with in red the concentration of the mrna of the maternal gene of bicoid. Above is the graphical representation of the left end of the egg, and the bicoid mrna concentration. Before fertilization there is a distinct area in the egg where bicoid mrna is found. At which side will the head be formed? 4. Q1B Bicoid protein After fertilization bicoid mrna is translated into Bicoid protein, which diffuses to the posterior end. Why is it not distributed evenly at the end of this stage? 5. Q1C Bicoid mrna concentration Why does the bicoid mrna itself not diffuse to the posterior end? 6. Parasegmentation The Bicoid concentration activates gap genes in the zygote cells, which start to regulate each other s expression and the expression of the pair-rule genes. Among those are giant, hunchback and Krüppel, which can activate or inhibit the pair-rule genes. Pair-rule genes are expressed in 7 bands across the zygote, thus dividing it into 14 parasegments. It is not possible to find a common rule for activation of all the 7 bands of the pair-rule genes. 7. Q2A Regulating pair-rule genes How are these pair-rule genes regulated? 8. Q2B Third parasegment Think of the regulation of the third parasegment, determined by the second stripe of Even-skipped. What would be the regulatory pattern needed for this band? Bicoid: Krüppel: Hunchback: Giant: 9. even-skipped and fushi tarazu Expression of even-skipped (stained black) and fushi tarazu (stained brown) at the end of stage 4. These activate the segment polarity genes in stage 5. 11

12 10. Parasegments: schematic This is the schematic representation of a small section of the egg. Even-skipped and Fushi tarazu are dividing the egg in 14 parasegments. As you see the parasegments are only about three to four cells wide. 11. Q3A Segment polarity genes Expression of even-skipped (stained black) and fushi tarazu (stained brown) at the end of stage 4. These pair-rule genes activate three major segment polarity genes in stage 5 which have key roles in segmentation. Which genes are this? 12. Q3B Engrailed In which cells do you expect engrailed to be expressed? 13. Q4 Border These cells were stained for Engrailed. Where will the segment boundaries be formed? 14. Q5 Clones In a series of blastoderm stage embryos, you injected one single cell in each embryo with a blue stain. Shortly after, you fixed the embryos and counterstained with an antibody against Engrailed (brown). Which of the images below show(s) possible outcomes of the experiment? 15. Lineage animations from FlyMove See SElin_media/SEli_lineage4.html 16. Q6 Boundary enforcement Engrailed is expressed in the most anterior cells of the parasegment; wingless in the most posterior. Together they determine the parasegment boundary, and establish and maintain this via intercellular signaling. 12

13 Complete this statement: stimulates/suppresses expression of in the adjacent/same parasegment on its turn activates hedgehog expression, which stimulates/suppresses expression of Wolpert figure Q7 Domains of lineage The parasegment boundary is a boundary of cell lineage restriction. Cells and their descendants from one parasegment never move into adjacent ones. These domains of lineage run through the segments. What is the name for these domains? 13

14 Segment identity 3. Q1A Genes So far the embryo has: - a posterior, anterior, dorsal and ventral side (maternal genes) - parasegmentation (gap and pair-rule genes) - segmentation (segment polarity genes) All segments are different. Which class of genes defines the segment identity? 4. Q1B Defenition selector What is a selector gene? 5. Q1C Defenition homeotic What is a homeotic gene? 6. Q2 Control By the products of which genes is the homeotic selector gene expression controlled? 7. Q3 Activation During the development of the fruit fly not all genes are constantly active. Indicate the period in which the groups of genes are active: gene group oogenesis first day 2-10 days adult fly 8. Activation of gene groups The maternal-effect genes are activated during oogenesis, when the oocyte is inside the mother's body. There is no zygote yet, so activity of all other (zygotic) genes is impossible. The genes are also activated the first day after fertilization. Gap genes are active soon after fertilization, but the activity disappears after four hours. This means that in larvae these genes are not active anymore. Pair-rule genes are activated by the gap-genes (and maternal genes), but their activity also disappears after four hours. This means that in larvae these genes are also not active anymore. Segment polarity genes are activated by pair-rule genes shortly after these are activated. Expression of these genes lasts into the adult fly. 14

15 Homeotic selector genes are also activated by gap and pair-rule genes shortly after these are activated. These genes are active during the whole life of the fruit fly. 9. Q4 Expression Segment polarity genes and homeotic selector genes are activated by gap and/or pair-rule genes. These proteins, however, are no longer active after about four hours. Segment polarity genes also stimulate each other's expression and their expression is no longer stimulated by pair-rule genes after these have ceased their activity. The correct expression of selector homeotic genes is continued with the aid of the proteins of the Polycomb and Trithorax gene groups. How do these continue the correct expression of homeotic selector genes? 10. Q5A Parasegments 1-5 There are two homeotic gene complexes in Drosophila. One complex of five homeobox genes controls the behaviour of the parasegments 1-5. How is this HOM complex called? 11. Q5B Parasegments 5-14 The other complex consists of three homeobox genes, and controls the behaviour of the parasegments How is this HOM complex called? 12. Q6 Homeotic gene complexes Is the identity of all segments determined by these homeotic selector genes? 13. Q7A Bithorax complex missing The three genes of the bithorax complex act in a combinational manner. In a normal fruit fly the parasegments and segments develop as is shown right (T=thorax, A=abdomen). What will be the parasegment identity if the whole complex is missing? 14. Q7B Ultrabithorax missing Ultrabithorax is one of the genes of the bithorax complex. It controls the identity of parasegments 5 and 6. What will be the parasegment identity if only this gene is missing? 15. Q7C Ultrabithorax only present What will be the parasegment identity when this is the only gene present of the bithorax group? 15

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