live-imaging-characterization-centromere-movements-during-male

Live Imaging Characterization of Centromere Movements During Male Meiotic Prophase in <em>Arabidopsis thaliana </em>

Meiosis is a cellular division, essential for sexual reproduction. During meiotic prophase, homologous chromosomes of maternal and paternal origin ...

Université Paris-Saclay, INRAE, AgroParisTech, Institute Jean-Pierre Bourgin for Plant Sciences (IJPB), 78000, Versailles, France

The synaptonemal complex (SC) is a proteinaceous structure that forms between homologous chromosomes during meiosis prophase. The SC is widely conserved across species, but its structure and roles during meiotic recombination are still debated. While the SC central region is made up of transverse filaments and central element proteins in mammals and fungi, few central element proteins have been identified in other species. Here we report the identification of two coiled-coil proteins, SCEP1 and SCEP2, that form a complex and localize at the centre of the Arabidopsis thaliana SC. In scep1 and scep2 mutants, chromosomes are aligned but not synapsed (the ZYP1 transverse filament protein is not loaded), crossovers are increased compared with the wild type, interference is lost and heterochiasmy is strongly reduced. We thus report the identification of two plant SC central elements, and homologues of these are found in all major angiosperm clades.

SCEP1 and SCEP2 are two new components of the synaptonemal complex central element.

Meiotic rapid prophase chromosome movements (RPMs) require connections between the chromosomes and the cytoskeleton, involving SUN (Sad1/UNC-84)-domain-containing proteins at the inner nuclear envelope (NE). RPMs remain significantly understudied in plants, with respect to their importance in the regulation of meiosis. Here, we demonstrate that Arabidopsis thaliana meiotic centromeres undergo rapid (up to 500 nm/s) and uncoordinated movements during the zygotene and pachytene stages. These centromere movements are not affected by altered chromosome organization and recombination but are abolished in the double mutant sun1 sun2. We also document the changes in chromosome dynamics and nucleus organization during the transition from leptotene to zygotene, including telomere attachment to SUN-enriched NE domains, bouquet formation, and nucleolus displacement, all of which were defective in sun1 sun2. These results establish A. thaliana as a model species for studying the functional implications of meiotic RPMs and demonstrate the mechanistic conservation of telomere-led RPMs in plants.

Rapid meiotic prophase chromosome movements in Arabidopsis thaliana are linked to essential reorganization at the nuclear envelope.

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.

Article	Year
SCEP1 and SCEP2 are two new components of the synaptonemal complex central element. Nature plants\| PubMed ID: 37973938	2023
Rapid meiotic prophase chromosome movements in Arabidopsis thaliana are linked to essential reorganization at the nuclear envelope. Nature communications\| PubMed ID: 39013853	2024
Identification of the cytoplasmic motor-LINC complex involved in rapid chromosome movements during meiotic prophase in Arabidopsis thaliana. Nature plants\| PubMed ID: 40715639	2025

Mathilde Grelon

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