The kinesin AtPSS1 promotes synapsis and is required for proper crossover distribution in meiosis.

Yann Duroc,Liudmila Chelysheva,Laurence Cromer,Afef Lemhemdi,Raphael Mercier,Aurélie Hurel,Christine Horlow,Susan J Armstrong,Cécile Larchevêque,Maria Cuacos

doi:10.1371/journal.pgen.1004674

Abstract

Meiotic crossovers (COs) shape genetic diversity by mixing homologous chromosomes at each generation. CO distribution is a highly regulated process. CO assurance forces the occurrence of at least one obligatory CO per chromosome pair, CO homeostasis smoothes out the number of COs when faced with variation in precursor number and CO interference keeps multiple COs away from each other along a chromosome. In several organisms, it has been shown that cytoskeleton forces are transduced to the meiotic nucleus via KASH- and SUN-domain proteins, to promote chromosome synapsis and recombination. Here we show that the Arabidopsis kinesin AtPSS1 plays a major role in chromosome synapsis and regulation of CO distribution. In Atpss1 meiotic cells, chromosome axes and DNA double strand breaks (DSBs) appear to form normally but only a variable portion of the genome synapses and is competent for CO formation. Some chromosomes fail to form the obligatory CO, while there is an increased CO density in competent regions. However, the total number of COs per cell is unaffected. We further show that the kinesin motor domain of AtPSS1 is required for its meiotic function, and that AtPSS1 interacts directly with WIP1 and WIP2, two KASH-domain proteins. Finally, meiocytes missing AtPSS1 and/or SUN proteins show similar meiotic defects suggesting that AtPSS1 and SUNs act in the same pathway. This suggests that forces produced by the AtPSS1 kinesin and transduced by WIPs/SUNs, are required to authorize complete synapsis and regulate maturation of recombination intermediates into COs. We suggest that a form of homeostasis applies, which maintains the total number of COs per cell even if only a part of the genome is competent for CO formation.

Highlights

Chromosomes inherited from the mother and father are mixed in a process termed homologous recombination, to generate unique chromosomes that will be transmitted to the generation
During a special cell division called meiosis, these two sets of chromosomes are mixed by homologous recombination to give genetically unique chromosomes that will be transmitted to the generation
Using the model plant Arabidopsis thaliana we reveal here that the AtPSS1 gene is required for proper localization of these homologous recombination events along the genome

Summary

Introduction

Chromosomes inherited from the mother and father are mixed in a process termed homologous recombination, to generate unique chromosomes that will be transmitted to the generation. This genetic mixing has sustained the evolution of eukaryotes. There are typically one to four exchange points – crossovers (COs)- between homologous chromosomes at each meiosis The distribution of these COs is under a series of constraints [1,2]. There is at least one CO per chromosome pair (obligatory CO or CO assurance) Beyond their genetic consequences, COs are essential for holding homologous chromosomes together during meiosis I, ensuring their balanced distribution in daughter cells. Looking at frequencies, COs are not homogenously distributed along the genome; hot and cold regions have been defined at the chromosome scale, and hotspots with a very high CO frequency have been observed at the kb scale [8,9]

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