The fastest movements and the most extreme deformations of the cell nucleus are driven by microtrubules in the model fungus Podospora anserina

Abstract

A growing number of studies shows that nuclear movement, positioning, and the mechanical constraints applied to the nucleus play important roles in cellular 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 female and male nuclei during sexual reproduction in the model fungus Podospora anserina. After plasmogamy, the two types of nuclei do not immediately undergo karyogamy. Instead, once inside the trichogyne (the female-specific hyphae extending from the ascogonium) the male nuclei migrate over distances of up to several hundred micrometers from the trichogyne tip, where plasmogamy occurs, 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. Both cytoskeletal networks are highly dynamic and abundant in trichogynes, particularly at septa. We demonstrate that while actin depolymerization does not impair male nuclei 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 branched trichogynes.