Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen

Abstract

ABSTRACT Multinucleate fungi and oomycetes are phylogenetically distant but structurally similar. To address whether they share similar nuclear dynamics, we carried out time-lapse imaging of fluorescently labeled Phytophthora palmivora nuclei. Nuclei underwent coordinated bidirectional movements during plant infection. Within hyphal networks growing in planta or in axenic culture, nuclei either are dragged passively with the cytoplasm or actively become rerouted toward nucleus-depleted hyphal sections and often display a very stretched shape. Benomyl-induced depolymerization of microtubules reduced active movements and the occurrence of stretched nuclei. A centrosome protein localized at the leading end of stretched nuclei, suggesting that, as in fungi, astral microtubule-guided movements contribute to nuclear distribution within oomycete hyphae. The remarkable hydrodynamic shape adaptations of Phytophthora nuclei contrast with those in fungi and likely enable them to migrate over longer distances. Therefore, our work summarizes mechanisms which enable a near-equal nuclear distribution in an oomycete. We provide a basis for computational modeling of hydrodynamic nuclear deformation within branched tubular networks. IMPORTANCE Despite their fungal morphology, oomycetes constitute a distinct group of protists related to brown algae and diatoms. Many oomycetes are pathogens and cause diseases of plants, insects, mammals, and humans. Extensive efforts have been made to understand the molecular basis of oomycete infection, but durable protection against these pathogens is yet to be achieved. We use a plant-pathogenic oomycete to decipher a key physiological aspect of oomycete growth and infection. We show that oomycete nuclei travel actively and over long distances within hyphae and during infection. Such movements require microtubules anchored on the centrosome. Nuclei hydrodynamically adapt their shape to travel in or against the flow. In contrast, fungi lack a centrosome and have much less flexible nuclei. Our findings provide a basis for modeling of flexible nuclear shapes in branched hyphal networks and may help in finding hard-to-evade targets to develop specific antioomycete strategies and achieve durable crop disease protection.

Keywords

• oomycetes
• Phytophthora palmivora
• nucleus movement
• centrosome
• hydrodynamics