Evolution and Diversity of Meiosis / Evolution et diversité de la méiose

Séminaire FSER organisé par Jean-René Huynh (Collège de France, CNRS, Paris) et Scott Hawley (Stowers Institute, Kansas City, USA) du 4 au 9 Avril 2022.

 

Participants 

Kirsten Bomblies (ETH Zurich, CH), Cori Cahoon (University of Oregon, US), Monica Colaiacovo (Harvard University, US), Gregory Copenhaver (University of North Carolina, US), Scott Hawley (Stowers Institute, Kansas City, USA), Jean-René Huynh (Collège de France, CNRS, FR), Simone Immler (East Anglia University, UK), Raphael Mercier (Max Planck Institute, Koln, Germany), Catriona Munro (Collège de France, Villefranche-sur-mer Marine Station), Jesus Page (Universidad Autonoma de Madrid, Spain), Thomas Robert (CBS, Montpellier, FR), Ofer Rog (University of Utah, US), Leah Rosin (NIH, Bethesda, USA), Denis Roze (Roscoff Marine station, SU, CRNS), Akera Takeshi (NIH, Bethesda, USA, visioconference), Allan Spradling (Carnegie, Baltimore, US), Denise Zickler (Université Paris-Saclay, FR).

 

Résumé 

Synaptonemal complex (Drosophila melanogaster) C(3)G in green and Corona in red (super-resolution microscopy, OMX, Thomas Rubin, Tristan Piolot, Jean-René Huynh)

La méiose est une étape clé de la reproduction sexuée. C’est effectivement à l’issue des deux divisions méiotiques que sont produits les gamètes mâles et femelles dont la rencontre formera un nouvel organisme. Chacun de ces gamètes contient un génome unique provenant du brassage génétique des chromosomes maternels et paternels. C’est donc à cette étape que sont produits des nouveaux génomes soumis à la sélection naturelle. L’étude de la méiose intéresse donc de nombreux domaines de la biologie, allant des enjeux médicaux de la reproduction sexuée à l’étude des mécanismes moléculaires de l’évolution. Pour ce séminaire sur l’Evolution et la Diversité de la Méiose, nous avons invité des chercheurs travaillant dans des domaines très différents (évolution, biologie cellulaire, génétique, modélisation, structure…) utilisant des organismes modèles variés (drosophile, souris, plantes, méduse, vers, bombyx, champignons, poisson-zèbre, saumon). Ce séminaire a réuni 17 scientifiques (7 femmes et 3 jeunes chercheurs). Une personne a participé en visio-conférence depuis le NIH (Bethesda, USA). La diversité des approches et des modèles présentés a permis de nombreuses discussions enrichissantes pour tous les participants. Ces échanges vont aussi donner lieu à de futures collaborations entre laboratoires participants. Au terme de ce séminaire a émergé la volonté d’organiser un meeting similaire dans quelques années soit sur le domaine des Treilles, soit aux Etats-Unis comme l’ont proposé certains participants.

Summary

Meiosis is a key step in sexual reproduction. It is indeed at the end of the two meiotic divisions that the male and female gametes are produced, and their fusion will form a new organism. Each of these gametes contains a unique genome resulting from the genetic shuffling of maternal and paternal chromosomes. It is therefore at this stage that new genomes are produced, subject to natural selection. The study of meiosis is therefore of interest to many areas of biology, ranging from the medical issues of sexual reproduction to the study of the molecular mechanisms of evolution. For this seminar on the Evolution and Diversity of Meiosis, we have invited researchers working in very different fields (evolution, cell biology, genetics, modeling, structure, etc.) using various model organisms (Drosophila, mice, plants, jellyfish, worms, bombyx, mushrooms, zebrafish, salmon). This seminar brought together 17 scientists (7 women and 3 young researchers). One person participated by videoconference from the NIH (Bethesda, USA). The diversity of approaches and models presented allowed many stimulating discussions for all participants. These exchanges will also give rise to future collaborations between participating laboratories. At the end of this seminar, the desire emerged to organize a similar meeting in a few years, either in les Treilles or in the United States, as some participants suggested.

 

Report

Scott Hawley (Stowers Institute, Kansas City, USA) presented his work on the formation of the synaptonemal complex in the Silkworm (Bombyx mori). In Bombyx males are ZZ and females are ZW. Male meiosis is relatively regular with the formation of a canonical synaptonemal complex and recombination nodules. In contrast, females are achiasmate and form a modified structure holding chromosomes together.

Jesus Page (Universidad Autonoma de Madrid, Spain) gave an overview of the evolution and behavior of sexual chromosomes during meiosis in many different mammal species. X and Y chromosomes often have a pseudo-autosomal region (PAR), which allows pairing during the early steps of meiosis. This region is a hot-spot for recombination and the entire X and Y are mostly transcriptionally silenced. Dr Page showed how different species of mice have gained or lost a PAR region, greatly modified the sex chromosomes, or lost X and Y chromosomes altogether.

Catriona Munro (Collège de France, Villefranche-sur-mer Marine Station) described the early steps of meiosis in the jellyfish, Clytia hemisphaerica. Clytia is a cnidarian species, which is a sister group to Bilateria, which includes all other laboratories model species. She found that knocking-out Spo11 by CRISPR/Cas9 eliminates all DNA recombination and abolishes the formation of the synaptonemal complex. In the absence of chiasmata, univalents segregate randomly during metaphase I of meiosis.

Leah Rosin (NIH, Bethesda, USA) presented her work on male meiosis in the Silkworm Bombyx mori. In Bombyx, centromeres are holocentric, i.e. present along the chromosome arms and express Cenp-T instead of the classical centromeric histone Cenp-A. Using the Oligopaints DNA FISH technology, she studied the pairing of homologous chromosomes in both male and female germ cells. She showed that homologue chromosomes are oriented by their telomeres to segregate properly during the first meiotic division.

Takeshi Akera (NIH, Bethesda, USA, visioconference) studied how some genetic elements can bias the segregation of chromosomes during mouse meiosis. He described how a non-centromeric selfish element uses the asymmetry of female meiotic divisions to segregate preferentially into the oocyte. He also showed how condensation defects of meiotic chromosomes could underlie sterility of hybrid crosses between different species of mice.

Thomas Robert (CBS, Montpellier, FR) described several new proteins that interact with TOPO6B. TOPO6B is itself in a molecular complex with Spo11, which is required to initiate DNA double strand breaks during meiosis. He showed that these interactions are differentially required in male and female meiosis. Some of these Spo11-partners are involved in meiotic chromosome condensation.

Denis Roze (Roscoff Marine station, SU, CRNS) is an evolutionary biologist studying the evolution of sexual versus asexual reproduction, the evolution of mating systems (selfing versus outcrossing) and the evolution of life cycles. He presented theoretical approaches modelling the effects of meiotic recombination rates on the selection of genetic characters.

Monica Colaiacovo (Harvard University, US) presented her work on the distribution of crossing-over along chromosomes in the worm C. elegans. She showed that there is a bias in the localization of DSBs to the chromosome arms compared to central regions, although C. elegans do not have central centromeres. She also showed that chromatin modifications can influence CO distribution.

Ofer Rog (University of Utah, US) focused on the evolution of synaptonemal complex proteins within worm species. Although these proteins have similar 3D structures, there is very little conservation at the sequence level. He showed several algorithms used to discover in silico potential proteins of the synaptonemal complex.

Cori Cahoon (University of Oregon, US) highlighted the differences between male and female meiosis in the worm C. elegans. Meiotic chromosome length, width and recombination landscape are different. SC proteins also appear more dynamic in male germ cells than in females.

Raphael Mercier (Max Planck Institute, Koln, Germany) presented his work on crossing over interference in plants. CO interference is a phenomenon, which limits the number of CO close to each other. He presented evidence that combining several mutations in genes that modulate different aspects of crossing over leads to vast increase in CO number and disappearance of interference.

Simone Immler (East Anglia University, UK) is an evolutionary biologist interested in natural selection in gamete (haploid state). She described theoretically and experimentally the effect of sperm selection in zebrafish and how this selection can be transmitted across generations.

Denise Zickler (Université Paris-Saclay, FR) discovered that in several species components of the synaptonemal complex are also part of the microtubule organizing center (MTOC). She further showed that mutations in these SC components also affect the formation of MTOCs. She presented a model linking the formation of the bouquet, DSBs, and SCs with MTOC.

Kirsten Bomblies (ETH Zurich, CH) studies meiosis in plants, which have duplicated their genome. These plants can be stable tetraploid or induced by colcemid treatment as neo-tetraploid. She described the consequences of polyploidy on crossing over distribution and CO interference and provided insights into the function of interference.

Gregory Copenhaver (University of North Carolina, US) explored the ways in which environmental conditions can change the rate of recombination in plants. He described the effects of temperature, salinity, or pathogen infection on the rate of recombination in plant meiosis.

Jean-René Huynh (Collège de France, CNRS, FR) described differences in homologue chromosome pairing between male and female Drosophila. Male Drosophila can pair their chromosome without DSBs or the formation of an SC. However, male and female use the same microtubule-driven machinery to move and pair their chromosomes. The dynamics, however, are very different as male chromosome movements are much slower than in females. These slower movements correlate with a longer period of pairing opportunity in males compared to females.

Allan Spradling (Carnegie, Baltimore, US) started by describing the formation of germline cysts in Drosophila and then showed that similar structures formed in mouse female germline. Cysts are formed by series of incomplete divisions and daughter cells remain linked by cytoplasmic bridges. Only a few of these cells will become an oocyte while the other germ cells transfer their cytoplasm into the oocytes. He further proposed that the vast majority of germ cells eliminated during female germline development in mammals are nurse cells.

The meeting allowed lengthy discussions of numerous meiotic processes: such as SC formation and function and Recombination Nodule function (especially as they relate to the control of crossover number and position), the mechanism of pairing, and the regulation of germ cell development.

 

 

 

 

 

 

 


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