Life as a moving fluid: fate of cytoplasmic macromolecules in dynamic fungal syncytia
Introduction
Biomechanicians have studied extensively the adaptations that enable organisms including plants, insects, larvae and bacteria, to deal with external fluid flows, from wind to water currents in rivers and the ocean [1]. However cells encounter a parallel challenge of creating and shaping internal flows. Filamentous fungi have especially dynamic cellular interiors: in Neurospora crassa mycelia continuous transport of cytoplasm from the mycelial interior to its growing edges carries nuclei, cytoplasm and organelles at speeds of 10s of microns per second [2]. Even in slower growing fungi nuclei and organelles may be in constant motion [3, 4]. Although these flows allow long range transport of nutrients and organelles over the colony, mechanisms are needed to localize the mRNAs and proteins that direct spatially regulated processes, for example, cytokinesis [5] or cell–cell communication [6]. In this review we will highlight primarily the role of physical mechanisms that allow ascomycete fungi to localize macromolecules against both diffusion and cytoplasmic flow. We will also discuss how mRNA and protein homogenization between may allow the fungus to tolerate internal genetic and epigenetic diversity. Increasing data suggests that these cellular-level dynamics are a motor for virulence and for the ability of the fungus to adapt to new hosts and changing environments.
Section snippets
Fungal models for dynamic syncytia
In this review we focus on filamentous ascomycete fungi. There are multiple reasons for choosing filamentous fungi as syncytial models: first, fungal compartments are among the largest of syncytia, capable of forming cytoplasmically connected networks that extend several centimeters [7•]. Second, transport within these networks is associated with rapid and long-ranged cytoplasmic flow. For example single nuclei may travel several centimeters through a N. crassa mycelium [8•] at speeds of up to
Physical mechanisms for the localization of proteins and mRNAs within the fungal syncytium
Proteins and mRNAs may travel through a continuous cytoplasm either by diffusion or by flow. In common with other cells [20, 21•], filamentous fungi use active transport along the cytoskeleton to localize some mRNAs, for example those associated with polarity establishment [22]. For some proteins (e.g., the protein-rich Spitzenkörper at growing hyphal tips [3]) localization seems to involve protein-cell membrane interactions. However for many macromolecules there is no known cytoskeletal
Discussion — an heterogeneous or homogeneous cellular interior?
We have physically organized the known adaptations used by fungi to localize macromolecules at specific points in the cell and highlighted evidence that these macromolecules are controllably and heterogeneously patterned through the syncytium. At the same time, dispersal of macromolecules through a shared cytoplasm endows fungi with tolerance for internal genetic diversity [7•]. In addition to providing a source of phenotypic plasticity [17•], shielding of deleterious mutations may facilitate
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
Acknowledgements
MR and PCH are supported by the NSF (DMS-1351860) and the Alfred P. Sloan Foundation. ASG is supported by the NIH (NIGMS R01GM081506) and the NSF (MCB-507511).
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