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In Drosophila Buzzatii : Gene CG13617 Silencing and Its Adaptive Significance

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In Drosophila Buzzatii : Gene CG13617 Silencing and Its Adaptive Significance Functional analysis of position effects of inversion 2j in Drosophila buzzatii : gene CG13617 silencing and its adaptive significance Análisis functional de efectos de posición de la inversión 2j en Drosophila buzzatii : el silenciamiento del gen CG13617 y su significado adaptativo Anàlisi funcional d’efectes de posició de la inversió 2j a Drosophila buzzatii : el silenciament del gen CG13617 i el seu significat adaptatiu DOCTORAL THESIS Marta Puig Font Universitat Autònoma de Barcelona Facultat de Biociències Departament de Genètica i Microbiologia Bellaterra, 2010 Memòria presentada per la Llicenciada en Biologia Marta Puig Font per a optar al grau de Doctora. Marta Puig Font Bellaterra, 10 de novembre de 2010 El Doctor Alfredo Ruiz Panadero, Catedràtic del Departament de Genètica i Microbiologia de la Facultat de Biociències de la Universitat Autònoma de Barcelona, i el Doctor Mario Cáceres Aguilar, Professor d’Investigació ICREA de l’Institut de Biotecnologia i Biomedicina de la Universitat Autònoma de Barcelona, CERTIFIQUEN que la Marta Puig Font ha dut a terme sota la seva direcció el treball de recerca realitzat al Departament de Genètica i Microbiologia de la Facultat de Biociències de la Universitat Autònoma de Barcelona que ha portat a l’elaboració d’aquesta Tesi Doctoral titulada “Functional analysis of position effects of inversion 2j in Drosophila buzzatii: gene CG13617 silencing and its adaptive significance”. I perquè consti als efectes oportuns, signen el present certificat a Bellaterra, a 10 de novembre de 2010. Dr. Alfredo Ruiz Panadero Dr. Mario Cáceres Aguilar Table of contents ABSTRACT | RESUMEN | RESUM 13 1 | INTRODUCTION 19 1.1 Chromosomal inversions 21 1.1.1 The generation of inversions 22 1.1.2 Adaptive value of inversions 23 1.1.3 Spread of inversions in populations 26 1.1.4 Traits and genes 29 1.2 Position effects of inversion breakpoints 31 1.3 Effects of transposable elements on gene expression 36 1.3.1 Regulatory changes 44 1.3.2 Epigenetic effects 48 1.4 The inversion 2j of D. buzzatii 51 1.4.1 The origin of inversion 2j 53 1.4.2 Genes flanking the inversion 2j breakpoints 56 1.5 Objetives 61 2 | MATERIALS AND METHODS 65 2.1 Drosophila lines 67 2.2 Nucleic acid isolation 68 2.3 RT-PCR and PCR 69 2.4 RACE 72 2.5 Real-time RT-PCR 72 2.6 DNA sequencing 73 2.7 Sequence analysis 75 2.7.1 Sequence annotation and comparative DNA sequence analysis 75 2.7.2 Protein analysis 76 2.8 Northern blot analysis 78 2.9 Whole-mount in situ hybridization in Drosophila embryos 78 2.10 dsRNA detection 79 2.11 RNA interference 79 2.11.1 Synthesis of a dsRNA molecule complementary to D. melanogaster gene CG13617 79 2.11.2 Microinjection 81 2.12 Microarrays 85 3 | RESULTS 91 3.1 Position effect of inversion 2j on CG13617 gene expression in D. buzzatii 93 PUIG, M., CÁCERES, M. and RUIZ, A. (2004) Silencing of a gene adjacent to the breakpoint of a widespread Drosophila inversion by a transposon-induced antisense RNA. Proc. Natl. Acad. Sci. USA 101: 9013-9018. 94 3.2 Functional consequences of CG13617 silencing 106 3.2.1 Silencing of D. melanogaster CG13617 gene expression by RNAi 107 3.2.2 Detection of gene-expression changes induced by CG13617 silencing using microarrays 110 3.2.3 Molecular consequences of CG13617 silencing in D. buzzatii 2j lines 121 3.3 Evolution and function of gene CG13617: comparative sequence analysis 127 3.3.1 CG13617 genomic structure in Drosophila species 127 3.3.2 Sequence analysis of the CG13617 protein in Drosophila species and other organisms 130 3.3.3 Identification of regulatory sequences in gene CG13617 141 4 | DISCUSSION 147 4.1 Position effect of inversion 2j on CG13617 gene expression 149 4.1.1 Possible causes of CG13617 silencing 151 4.1.2 CG13617 antisense transcript 161 4.1.3 Transposable elements can induce transcription of adjacent sequences 168 4.2 Consequences of CG13617 silencing 173 4.2.1 Expression changes associated to CG13617 silencing 173 4.2.1.1 Magnitude of the expression changes induced by CG13617 silencing 177 4.2.1.2 Specificity of CG13617 silencing effect 181 4.2.2 Gene CG13617 structure and function 183 4.2.2.1 Changes in gene structure within the Drosophila genus 184 4.2.2.2 Protein sequence analysis 185 4.2.2.3 CG13617 homologous proteins in other species 187 4.2.2.4 Is CG13617 a component of the Hedgehog signaling pathway? 189 4.2.3 CG13617 and inversion 2j evolutionary history 197 5 | CONCLUSIONS 205 APPENDIX I 209 CÁCERES, M., PUIG, M. and RUIZ, A. (2001) Molecular characterization of two natural hotspots in the Drosophila buzzatii genome induced by transposon insertions. Genome Res 11: 1353-1364. APPENDIX II 223 CLARK, A.G., EISEN, M.B., SMITH, D.R., BERGMAN, C.M., OLIVER, B., MARKOW, T.A., KAUFMAN, T.C., KELLIS, M., GELBART, W., IYER, V.N., et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218. APPENDIX III 241 MARZO, M., PUIG, M. and RUIZ, A. (2008) The Foldback-like element Galileo belongs to the P superfamily of DNA transposons and is widespread within the Drosophila genus. Proc Natl Acad Sci U S A 105: 2957-2962. APPENDIX IV 249 DELPRAT, A., NEGRE, B., PUIG, M. and RUIZ, A. (2009) The transposon Galileo generates natural chromosomal inversions in Drosophila by ectopic recombination. PLoS One 4: e7883. BIBLIOGRAPHY 265 WEB REFERENCES 281 ABBREVIATIONS 285 INDEX OF FIGURES 290 INDEX OF TABLES 293 INDEX OF BOXES 295 AKNOWLEDGEMENTS | AGRADECIMIENTOS | AGRAÏMENTS 296 A la Sara i el Joan Abstract Chromosomal inversions have been known for a long time to be maintained by natural selection in Drosophila populations. However, the molecular mechanisms underlying their adaptive value remain uncertain. In D. buzzatii natural populations, inversion 2j forms a balanced polymorphism with the 2st arrangement, in which 2j individuals have a larger size and a longer developmental time compared to 2st carriers. In this work we tested the hypothesis that a position effect of one of the inversion breakpoints could be the cause of these phenotypic changes by analyzing the expression of a gene adjacent to the proximal breakpoint, CG13617, in D. buzzatii lines with and without inversion 2j. We have found that in 2j embryos an antisense RNA originated in a copy of a Galileo family transposon inserted at the breakpoint causes a 5-fold decrease of the expression level of CG13617. In order to investigate the functional consequences of the reduction in CG13617 expression, we have used RNA interference to reproduce this silencing in D. melanogaster. Microarray and real-time RT-PCR experiments comparing first instar larvae with and without CG13617 expression revealed that 41 genes show reduced expression levels when CG13617 is silenced, while none is up-regulated. Interestingly, genes involved in DNA replication and cell cycle are significantly enriched among those affected by CG13617 silencing. Nine out of ten of these genes analyzed in D. buzzatii also show a reduced expression level in 2j embryos, but not in first instar larvae, a stage where the CG13617 expression difference between chromosomal arrangements is lower and the antisense RNA is no longer transcribed. To gain insight into the potential function of this gene we have carried out a comprehensive nucleotide and protein sequence analysis in the 12 available Drosophila genomes and also in other organisms. CG13617 protein contains a conserved C2H2 zinc finger, three coiled coil regions, two PEST sequences, and putative nuclear localization and export signals, and shows similarity to human DZIP1 and zebrafish Iguana (a component of the Hedgehog signaling pathway) proteins, which indicates that its cellular role could be related to the transport of transcription factors in and out of the nucleus. These results suggest that gene CG13617 could be involved in the regulation of DNA replication and that the position effect in 2j carriers might contribute to explain the Abstract 13 phenotypic differences observed between 2st and 2j individuals as well as the adaptive value of the inversion. 14 Abstract Resumen Es sabido desde hace mucho tiempo que las inversiones cromosómicas son mantenidas por selección natural en muchas poblaciones de Drosophila. Sin embargo, los mecanismos que causan este valor adaptativo aún no se conocen. En las poblaciones naturales de D. buzzatii, la inversión 2j forma un polimorfismo equilibrado con la ordenación 2st, en que los individuos 2j tienen un mayor tamaño y un tiempo de desarrollo más largo en comparación con los 2st. En este trabajo hemos puesto a prueba la hipótesis de que un efecto de posición de uno de los puntos de rotura de la inversión podría ser la causa de estos cambios fenotípicos. Para ello, hemos analizado la expresión de un gen adyacente al punto de rotura proximal, CG13617, en líneas de D. buzzatii con y sin la inversión 2j. Hemos encontrado que los embriones 2j presentan un nivel de expresión de CG13617 cinco veces menor causado por un RNA antisense originado en una copia de un transposón de la familia Galileo insertado en el punto de rotura. Las consecuencias funcionales de esta reducción en la expresión de CG13617 se han investigado utilizado la técnica de RNA interferencia para reproducir este silenciamiento en D. melanogaster. Los experimentos con microarrays y RT-PCR en tiempo real comparando larvas de primer estadio con y sin expresión de CG13617 han revelado que 41 genes muestran niveles de expresión reducidos cuando CG13617 es silenciado, mientras que ningún gen presenta un incremento. Además, hay un exceso significativo de genes implicados en la replicación del DNA y en el ciclo celular entre los afectados por el silenciamiento de CG13617.
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