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Transcript Profiling to Analyse Gene Expression During Male Meiosis in Petunia Hybrida PDF hosted at the Radboud Repository of the Radboud University Nijmegen The following full text is a publisher's version. For additional information about this publication click this link. http://hdl.handle.net/2066/19503 Please be advised that this information was generated on 2021-10-06 and may be subject to change. UITNODIGING voor het bijwonen van de openbare verdediging van mijn Transcript Profiling during male meiosis in Petunia hybrida male meiosis in Petunia during Profiling Transcript proefschrift Transcript Profiling to analyse gene expression during male meiosis in Petunia hybrida Op woensdag 6 oktober 2004 om 15.30 u precies in de Aula van de Radboud Universiteit Nijmegen, Comeniuslaan 2 Transcript profiling to analyse gene expression during male meiosis in Receptie na afloop van Petunia hybrida de promotie in de aula Filip Cnudde Filip Cnudde [email protected] Paranimfen: Janny Peters ([email protected]) Filip Cnudde Stefan Royaert ([email protected]) bw-cnudde 23-08-2004 14:49 Pagina 2 bw-cnudde 23-08-2004 14:49 Pagina 1 Transcript profiling to analyse gene expression during male meiosis in Petunia hybrida bw-cnudde 23-08-2004 14:49 Pagina 2 bw-cnudde 23-08-2004 14:49 Pagina 3 Transcript profiling to analyse gene expression during male meiosis in Petunia hybrida Een wetenschappelijke proeve op het gebied van de Natuurwetenschappen, Wiskunde en Informatica Proefschrift ter verkrijging van de graad van doctor aan de Radboud Universiteit Nijmegen op gezag van de Rector Magnificus prof. dr. C.W.P.M. Blom volgens besluit van het College van Decanen in het openbaar te verdedigen op woensdag 6 oktober 2004 des namiddags om 3.30 uur precies door Filip Cnudde geboren op 10 maart 1973 te Gent bw-cnudde 23-08-2004 14:49 Pagina 4 Promotor: Prof. Dr. T. Gerats Manuscriptcommissie: Prof. Dr. U. Grossniklaus, Universität Zürich, Switzerland Prof. Dr. H. de Jong, Wageningen Universiteit Prof. Dr. K. Goethals, Universiteit Gent, België Design: Martien Frijns ISBN 90-90184414 Printed by: PrintParners Ipskamp, Enschede bw-cnudde 23-08-2004 14:49 Pagina 5 Contents Chapter I 7 General introduction Chapter II 55 Transcript profiling on developing Petunia hybrida floral organs Chapter III 73 Expression analysis during meiosis in Petunia hybrida anthers using cDNA-AFLP-based transcript profiling Chapter IV 89 cDNA-AFLP-based transcript profiling enables the assembly of a comprehensive catalogue of genes modulated during male meiosis Chapter V 123 Clustering genes expressed during male meiosis Chapter VI 147 Cellular localisation of a selected subset of modulated Petunia hybrida transcripts by in situ hybridisation Summary and perspectives 159 Samenvatting en perspectieven 163 Dankwoord 166 Curriculum vitae 168 Appendix 169 bw-cnudde 23-08-2004 14:49 Pagina 6 Wanneer ik niet weet waar ik mee bezig ben – ben ik onderzoek aan het doen. Uit: Duizend wegen naar wijsheid, David Baird bw-cnudde 23-08-2004 14:49 Pagina 7 Chapter I General introduction submitted as a review to Plant Biology bw-cnudde 23-08-2004 14:49 Pagina 8 8 CHAPTER I History In 1883 the Belgian cytologist Edouard van Beneden made an amazing observation: fertilised eggs of the parasitic nematode Ascaris megalocephala contain four chromosomes, whereas the sperm and the egg nuclei each contain only two. Building on this observation, which was published without any comments, August Weismann (1887) speculated on the existence of a reductive cell division during the sexual life cycle to compensate for the fusion of gametes at fertilisation. Farmer and Moore (1905) introduced the term meiosis to describe this specialised form of cell division (from the Greek meioun: to diminish). Since these early observations, meiosis has been the subject of intense scientific scrutiny for more than a century. Cytogeneticists have documented numerous cytological analyses of meiosis for over 100 years. Most often these were carried out in plants and gave detailed descriptions of the behaviour of meiotic chromosomes. The molecular details underlying some of these unique structural and behavioural aspects of meiotic chromosomes are only now beginning to be unraveled. Data from different model systems suggest that the overall mechanisms of meiosis are conserved from yeast to mammals and often use homologous genes for comparable functions. However, intriguing differences exist between species, providing a challenge for geneticists and molecular biologists to comprehend the cellular processes surrounding meiosis and the rules governing genetic inheritance. Introduction The life cycle of sexually reproducing eukaryotes is characterised by an alternation of diploid and haploid generations (Fig. 1). A diploid cell contains two versions of each chromosome, one of maternal and one of paternal origin, which are called homologous chromosomes, whereas haploid cells have only one copy of each chromosome. The transition from diploid to haploid takes place at meiosis, a specialised set of two cell divisions by which four haploid gametes are produced from one diploid parental cell. In the case of pollen tetrads in plants, all four haploid nuclei give rise to four different cells, while in female meiosis only one haploid nucleus ends up in the oocyte. Chromosome numbers are reduced during meiosis because a single round of DNA replication is followed by two successive rounds of chromosome segregation. This contrasts with mitosis, during which a single round of chromosome segregation follows each round of DNA replication, and the chromosome number remains constant at the end of each cycle (Fig. 1). Fusion of two gametes during sexual reproduction restores the diploid chromosome complement in the zygote. bw-cnudde 23-08-2004 14:49 Pagina 9 Introduction 9 S Figure 1 Alternation of diploid and haploid generations in the life cycle of sexually reproducing eukaryotes (after Petronczki et al., 2003) Meiosis is a key feature of eukaryotic sexual reproduction and fulfils two primary functions. First, it serves to reduce the chromosome number of gametes twofold in anticipation of fertilisation and the reconstitution of the diploid state. Second, the high- frequency genetic exchange events not only ensure proper chromosome disjunction but also contribute to genetic diversity upon which natural selection can act. The structure and behaviour of meiotic prophase I chromosomes are very different from those observed for prophase chromosomes in mitotically dividing cells (Fig. 2). In meiosis, chromosomes replicate and compact; homologous chromosomes pair to identify partners and then these partners segregate away from each other at the first (reductional) division, while sister chromatids separate during the second (equational) division at meiosis II. The second division of meiosis resembles mitosis: sister chromatids separate and segregate. The first division, however, is unique. There are at least four crucial differences between chromosome behaviour during meiosis I and mitosis (Moore and Orr-Weaver, 1998; Zickler and Kleckner, 1998; Petronczki et al., 2003). The first is pairing and recombination between maternal and paternal chromosomes. The resulting crossovers collaborate with cohesion between sister chromatids to form temporary connections (chiasmata) between homologues that allow them to orient themselves towards opposite poles of the meiosis I spindle. Correct bw-cnudde 23-08-2004 14:49 Pagina 10 10 CHAPTER I Figure 2 Schematic representation of the mitotic (left) and meiotic (right) cell cycle (see also appendix) segregation at the meiosis I division depends on these crossover events between the DNA molecules of homologous chromosomes (Moore and Orr-Weaver, 1998). As a result of crossing-over, each offspring will carry genes from all four grandparents. If no crossing-over would occur, the offspring would only inherit genes from two grandparents. Second, sister kinetochores always attach to microtubules from the same pole, which is known as co-orientation or monopolar attachment. This ensures that sister chromatids are now pulled to the same pole at the end of the first meiotic division. Monopolar attachment is fundamentally different from the mode of attachment in mitosis and meiosis II, where sister kinetochores are attached to opposite poles (bipolar). The third major difference between meiosis I and mitosis is that cohesion between sister chromatids in the vicinity of centromeres is maintained until the onset of the second meiotic division (Moore and Orr-Weaver, 1998; Moore et al., 1998). Finally, DNA replication is inhibited in between the two meiotic divisions. Proliferating mitotic cells rely on alternating rounds of DNA replication during S-phase and segregation of the duplicated chromatids during M-phase or mitosis. This rule has to be violated between the two meiotic divisions to allow the formation of haploid nuclei. Meiotic cells, therefore, suppress S-phase after meiosis I (Petronczki et al., 2003). bw-cnudde 23-08-2004 14:49 Pagina 11 Introduction 11 Whence meiosis? Sexual reproduction among living creatures seems so common to everyone that the asexual cases (e.g. budding in yeasts, cutting and grafting of plants) are sometimes perceived as a curiosity of nature. In fact, in the evolution of living organisms, sexual reproduction has proven to be a successful strategy (Bell, 1982). This is due to its ability to recombine the genomes of individuals, resulting in increased genetic diversity that makes coping with selection more efficient (Rice and Chippindale, 2001). Although the rate of reproduction is
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