Identification of the cytoplasmic motor–LINC complex involved in rapid chromosome movements during meiotic prophase in Arabidopsis thaliana

Homologous pairing and recombination during meiosis are facilitated by rapid prophase movements (RPMs), which depend on chromosome attachment to the nuclear envelope (NE) and on cytoplasmic forces transmitted to the chromosomes through the NE, mediated by Linker of Nucleoskeleton and Cytoskeleton (LINC) complexes. In plants, only the NE-associated SUN-domain proteins SUN1 and SUN2 have been identified as components of the RPM process. Here we show that, during meiosis, SUN1 and SUN2 form a LINC complex with the KASH-domain protein SINE3, which recruits the meiosis-specific kinesin PSS1 to the NE. These proteins accumulate at telomere-binding sites in the NE, and their loss disrupts telomere attachment and bouquet formation and abolishes RPMs. These defects lead to defective synapsis and clustered crossovers, resulting in chromosome mis-segregation. Our results establish that the mechanism underlying RPMs is conserved in Arabidopsis thaliana, with RPMs primarily facilitating homologous recognition rather than preventing non-homologous interactions.