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Fast and tortuous: extreme deformations and fast movements of the cell nucleus are driven by microtubules in the model fungus Podospora anserina.

Created on 31 Jul 2026

Authors

Marie-Caroline Viron, Zoé Kachaner, Pierre Grognet, Christophe Lalanne, Antoine Guichet, Sylvain Brun

Published in

mBio. Pages e0145526. Jul 31, 2026. Epub Jul 31, 2026.

Abstract

Nuclear movement, positioning, and the mechanical constraints applied to the nucleus play important roles in cellular identity, physiology, and gene regulation. This process, known as nuclear mechanotransduction, is an emerging field of research, and its deregulation can lead to severe human pathologies. In this study, we examine the behavior of male nuclei during sexual reproduction in the model fungus Podospora anserina. Once inside the trichogyne (the hyphal extension of the ascogonium, the female gamete), male nuclei do not undergo karyogamy with the female nuclei present in the trichogyne but migrate from the trichogyne tip, where plasmogamy occurred, to the ascogonium at the center of the protoperithecium. Our study highlights the contrasting behaviors of the two nuclear types: female nuclei remain immobile and spherical, while male nuclei move rapidly and exhibit striking deformations and stretching. Trichogynes are branched and compartmentalized, consisting of articles separated by septa that communicate through the septal pores. We show that during their migration across these compartments, male nuclei undergo the most extreme movements, deformations, and speeds reported to date for nuclei in motion. We also investigated the role of the actin and microtubule (MT) cytoskeletons in male nuclei behavior. We demonstrate that while actin depolymerization does not impair male nucleus migration, MT disruption causes a complete arrest of both nuclear movement and stretching, indicating a critical role for MTs. Finally, we reveal that the MT network in trichogynes is highly polarized, offering new insights into how male nuclei navigate within a complex branched network.IMPORTANCEHere, using live-cell fluorescence imaging, we report the remarkable and complex behavior of male nuclei during sexual reproduction in the model fungus Podospora anserina. In particular, during their migration in female trichogynes, male nuclei undergo the most extreme movements, deformations, and speeds reported to date for nuclei in motion while female nuclei remain immobile. The highest speed reached by male nuclei is 135 µm/min and the most extreme stretching while passing by obstacles is 71 µm, which represents 12 times its size in a resting state. Furthermore, we show that microtubules (MT) are responsible for male nucleus movements and deformations and that the MT network is dense and highly polarized all along trichogynes. This latter discovery gives new insights into how nuclei eventually reach their destination, the protoperithecium, and how they can change direction and orientate in complex, ramified, and compartmentalized cells such as trichogynes.

PMID:
42535912
Bibliographic data and abstract were imported from PubMed on 31 Jul 2026.

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