Abstract
Multinucleate cells occur in every biosphere and across the kingdoms of life, including in the human body as muscle cells and bone-forming cells. Data from filamentous fungi suggest that, even when bathed in a common cytoplasm, nuclei are capable of autonomous behaviors, including division. How does this potential for autonomy affect the organization of cellular processes between nuclei? Here we analyze a simplified model of circadian rhythm, a form of cellular oscillator, in a mathematical model of the filamentous fungus Neurospora crassa. Our results highlight a potential role played by mRNA-protein phase separation to keep mRNAs close to the nuclei from which they originate, while allowing proteins to diffuse freely between nuclei. Our modeling shows that syncytism allows for extreme mRNA efficiency-we demonstrate assembly of a robust oscillator with a transcription rate a thousand-fold less than in comparable uninucleate cells. We also show self-organized division of the labor of mRNA production, with one nucleus in a two-nucleus syncytium producing at least twice as many mRNAs as the other in 30% of cycles. This division can occur spontaneously, but division of labor can also be controlled by regulating the amount of cytoplasmic volume available to each nucleus. Taken together, our results show the intriguing richness and potential for emergent organization among nuclei in multinucleate cells. They also highlight the role of previously studied mechanisms of cellular organization, including nuclear space control and localization of mRNAs through RNA-protein phase separation, in regulating nuclear coordination.
Highlights
Syncytia, or multinucleate cells, are present throughout the human body, as muscle cells and bone forming cells, as well as in embryos [1,2,3]
Circadian rhythms are among the most researched cellular processes, but limited work has been done on how these rhythms are coordinated between nuclei in multinucleate cells
We analyze a mathematical model for circadian oscillations in a multinucleate cell, motivated by frequency mRNA and protein data from the filamentous fungus Neurospora crassa
Summary
Multinucleate cells, are present throughout the human body, as muscle cells and bone forming cells, as well as in embryos [1,2,3]. They occur in every biosphere and across the kingdoms of life, including fungi, slime molds, and water molds [4,5,6,7]. Even when bathed in a common cytoplasm, the nuclei of syncytial fungi are capable of dividing autonomously, migrating independently across the syncytium, and expressing different genes [4]. There are many possible ways for a syncytium to divide the labor of making mRNAs among its nuclei. Does coordination of mRNA production require top-down control of nuclei by the organism, or can it emerge spontaneously even when nuclei respond autonomously to cues from the cell’s environment?
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