AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization

Meiotic crossovers (COs) are important for reshuffling genetic information between homologous chromosomes and they are essential for their correct segregation. COs are unevenly distributed along chromosomes and the underlying mechanisms controlling CO localization are not well understood. We previously showed that meiotic COs are mis-localized in the absence of AXR1, an enzyme involved in the neddylation/rubylation protein modification pathway inArabidopsis thaliana. Here, we report that inaxr1(-/-), male meiocytes show a strong defect in chromosome pairing whereas the formation of the telomere bouquet is not affected. COs are also redistributed towards subtelomeric chromosomal ends where they frequently form clusters, in contrast to large central regions depleted in recombination. The CO suppressed regions correlate with DNA hypermethylation of transposable elements (TEs) in the CHH context inaxr1(-/-)meiocytes. Through examining somatic methylomes, we foundaxr1(-/-)affects DNA methylation in a plant, causing hypermethylation in all sequence contexts (CG, CHG and CHH) in TEs. Impairment of the main pathways involved in DNA methylation is epistatic overaxr1(-/-)for DNA methylation in somatic cells but does not restore regular chromosome segregation during meiosis. Collectively, our findings reveal that the neddylation pathway not only regulates hormonal perception and CO distribution but is also, directly or indirectly, a major limiting pathway of TE DNA methylation in somatic cells. Author summary In sexually reproducing organisms, each parent transmits one and only one copy of each chromosome to their progeny via their packaging in haploid gametes. To ensure the proper transmission of the chromosomes, pairs of homologous chromosomes must associate and exchange genetic information (also called reciprocal recombination) during a special division called meiosis that lead to the formation of the gametes. The recombination process is highly controlled in terms of number and localization of the events along the chromosomes. Disruption of this control may cause an inappropriate transmission of the chromosomes in the gametes leading to abnormal chromosome numbers in the offspring which is usually deleterious. In the plantArabidopis thaliana, we show that when the pathway modifying proteins through ubiquitination/neddylation is impaired, the number of reciprocal recombination events is maintained but they are delocalized toward the ends of the chromosomes and some chromosomes do not exchange material. We also detected changes of patterns for DNA methylation, an epigenetic modification localised on DNA cytosines. Furthermore, we demonstrate that the methylation of cytosines is not causal to the localization change of meiotic recombination events.