Nuclear autonomy in multinucleate fungi

Abstract

Within many fungal syncytia, nuclei behave independently despite sharing a common cytoplasm. Creation of independent nuclear zones of control in one cell is paradoxical considering random protein synthesis sites, predicted rapid diffusion rates, and well-mixed cytosol. In studying the surprising fungal nuclear autonomy, new principles of cellular organization are emerging. We discuss the current understanding of nuclear autonomy, focusing on asynchronous cell cycle progression where most work has been directed. Mechanisms underlying nuclear autonomy are diverse including mRNA localization, ploidy variability, and nuclear spacing control. With the challenges fungal syncytia face due to cytoplasmic size and shape, they serve as powerful models for uncovering new subcellular organization modes, variability sources among isogenic uninucleate cells, and the evolution of multicellularity.

Figure 1

Mitotic strategies utilized by different filamentous fungi. Synchronous: All nuclei divide at the same time. Parasynchronous: Nuclei divide in waves, with one neighbor dividing after another. Asynchronous: Nuclei divide independently of their neighbors.

Figure 2

Potential models for regulation of nuclear autonomy. Top: Nuclear regulation of division autonomy. Nuclei carry with them the signals controlling their cell cycle stage. Nuclear movement and proximity to neighbors does not influence cell cycle stage. Bottom: Cytoplasmic regulation of division autonomy. Regulators are spatially organized in the cytoplasm so that each nucleus is only exposed to the appropriate cell cycle signals. Bypassing and/or closely positioned nuclei may influence each others’ states.