Syncytial Assembly Lines: Consequences of Multinucleate Cellular Compartments for Fungal Protein Synthesis.

Fast growth and prodigious cellular outputs make fungi powerful tools in biotechnology. Recent modeling work has exposed efficiency gains associated with dividing the labor of transcription over multiple nuclei, and experimental innovations are opening new windows on the capacities and adaptations that allow nuclei to behave autonomously or in coordination while sharing a single, common cytoplasm. Although the motivation of our review is to motivate and connect recent work toward a greater understanding of fungal factories, we use the analogy of the assembly line as an organizing idea for studying coordinated gene expression, generally.

Permissiveness and competition within and between Neurospora crassa syncytia.

A multinucleate syncytium is a common growth form in filamentous fungi. Comprehensive functions of the syncytial state remain unknown, but it likely allows for a wide range of adaptations to enable filamentous fungi to coordinate growth, reproduction, responses to the environment, and to distribute nuclear and cytoplasmic elements across a colony. Indeed, the underlying mechanistic details of how syncytia regulate cellular and molecular processes spatiotemporally across a colony are largely unexplored.

Septins coordinate cell wall integrity and lipid metabolism in a sphingolipid-dependent process.

Septins colocalize with membrane sterol-rich regions and facilitate recruitment of cell wall synthases during wall remodeling. We show that null mutants missing an Aspergillus nidulans core septin present in hexamers and octamers (ΔaspAcdc11, ΔaspBcdc3 or ΔaspCcdc12) are sensitive to multiple cell wall-disturbing agents that activate the cell wall integrity MAPK pathway. The null mutant missing the octamer-exclusive core septin (ΔaspDcdc10) showed similar sensitivity, but only to a single cell wall-disturbing agent and the null mutant missing the noncore septin (ΔaspE) showed only very mild sensitivity to a different single agent.

Syncytia in Fungi.

Filamentous fungi typically grow as interconnected multinucleate syncytia that can be microscopic to many hectares in size. Mechanistic details and rules that govern the formation and function of these multinucleate syncytia are largely unexplored, including details on syncytial morphology and the regulatory controls of cellular and molecular processes. Recent discoveries have revealed various adaptations that enable fungal syncytia to accomplish coordinated behaviors, including cell growth, nuclear division, secretion, communication, and adaptation of the hyphal network for mixing nuclear and cytoplasmic organelles.

Septin mutations and phenotypes in S. cerevisiae.

Septins are highly conserved guanosine triphosphate (GTP)-binding proteins that are a component of the cytoskeletal systems of virtually all eukaryotes (except higher plants). Septins play important roles in a multitude of cellular processes, including cytokinesis, establishment of cell polarity, and cellular partitioning. The ease of genetic screens and a fully sequenced genome have made Saccharomyces cerevisiae one of the most extensively studied and well-annotated model organisms in eukaryotic biology.

Internuclear diffusion of histone H1 within cellular compartments of Aspergillus nidulans.

Histone H1 is an evolutionarily conserved linker histone protein that functions in arranging and stabilizing chromatin structure and is frequently fused to a fluorescent protein to track nuclei in live cells. In time-lapse analyses, we observed stochastic exchange of photoactivated Dendra2-histone H1 protein between nuclei within the same cellular compartment. We also observed exchange of histones between genetically distinct nuclei in a heterokaryon derived from fusion of strains carrying histone H1-RFP or H1-GFP.