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

Laurence Cromer, Mariana Tiscareno-Andrade, Sandrine Lefranc, Aurélie Chambon, Aurélie Hurel, Manon Brogniez, Julie Guérin, Ivan Masson, Gabriele Adam, Delphine Charif, Philippe Andrey and Mathilde Grelon ()
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Laurence Cromer: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Mariana Tiscareno-Andrade: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Sandrine Lefranc: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Aurélie Chambon: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Aurélie Hurel: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Manon Brogniez: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Julie Guérin: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Ivan Masson: UMR Agronomie
Gabriele Adam: Institute of Plant Sciences Paris-Saclay (IPS2)
Delphine Charif: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Philippe Andrey: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)
Mathilde Grelon: Institute Jean-Pierre Bourgin for Plant Sciences (IJPB)

Nature Communications, 2024, vol. 15, issue 1, 1-21

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41467-024-50169-4

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