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Cells can maintain their functions despite fluctuations in intracellular parameters, such as protein activities and gene expression levels. This commonly observed biological property of cells is called robustness. On the other hand, these parameters have different limitations, each reflecting the property of the subsystem containing the parameter. The budding yeast cell cycle is quite fragile upon overexpression of  CDC14 , but is robust upon overexpression of  ESP1 . The gene products of both  CDC14  and  ESP1  are regulated by 1∶1 binding with their inhibitors (Net1 and Pds1), and a mathematical model predicts the extreme fragility of the cell cycle upon overexpression of  CDC14  and  ESP1  caused by dosage imbalance between these genes. However, it has not been experimentally shown that dosage imbalance causes fragility of the cell cycle. In this study, we measured the quantitative genetic interactions of these genes by performing combinatorial “genetic tug-of-war” experiments. We first showed experimental evidence that dosage imbalance between  CDC14  and  NET1  causes fragility. We also showed that fragility arising from dosage imbalance between  ESP1  and  PDS1  is masked by  CDH1  and  CLB2 . The masking function of  CLB2  was stabilization of Pds1 by its phosphorylation. We finally modified Chen's model according to our findings. We thus propose that dosage imbalance causes fragility in biological systems.

Fragilities Caused by Dosage Imbalance in Regulation of the Budding Yeast Cell Cycle