Ssd1-2 RNA binding protein directs sporulation in response to stress

From the Breeden Lab, Basic Sciences Division

“When nutrients are lacking, yeast must stop expending the energy it takes to divide. To survive, they either enter a non-dividing, quiescent state, or they differentiate into spores,” stated Dr. Linda Breeden, Professor Emeritus in the Basic Sciences Division at Fred Hutchinson Cancer Center. The SSD1 gene expressed by the yeast Saccharomyces cerevisiae is involved in making this decision between quiescence or sporulation. While studying a prominent ssd1 truncation mutant, termed ssd1-2, Dr. Breeden and her research technician Shawna Miles made a pivotal discovery that the Ssd1-2 protein causes cell toxicity when another RNA binding protein, Mpt5, is not expressed. This phenotype was not observed when both ssd1 and mpt5 genes were absent. They also found that a diploid ssd1-2/ssd1-2 strain fails to enter quiescence and promotes sporulation compared to a ssd1∆/ssd1∆ strain, in which Ssd1 protein is completely absent. Therefore, the Ssd1-2 protein that was previously thought to be without function can influence this key decision cells make when they are forced to stop dividing under conditions of stress. Their work characterizing the role of Ssd1-2 was published recently in microPublication Biology.

“I spent my early career studying how yeast cells initiate the cell division process,” commented Dr. Breeden. “The yeast we study is a free living, single-celled organism, with the same general architecture and duplication process as human cells.” For this reason, yeast are used to dissect conserved cellular processes, such as, cell division. “These yeast can be easily propagated as “wild type” or normal cells, and then engineered to have mutations in a single gene. Direct comparison of mutant and wild type has been extremely useful for understanding how each gene product contributes to the mechanics of cell division. However, Ssd1-2 is an example of how environmental changes influence cell division and select for mutations that promote survival in that environment. The Ssd1-2 truncation has arisen independently in several wild yeast strains.” A previous survey of wild yeast strains carried out by the Breeden lab showed that there are wild strains that only sporulate and others that only enter quiescence. This indicates that there are natural habitats in which spores survive better than quiescent cells and others where quiescence is more advantageous. Ssd1-2 is one of many naturally occurring mutations that enables yeast cells to survive nutrient limitation by forming spores.

Interestingly, Ssd1-2 is deleterious in many stressful conditions in addition to nutrient deprivation. For example, incubation at high temperature, use of detergents, treatment with drugs and many other environmental insults are highly toxic to Ssd1-2 cells compared to cells carrying the full-length Ssd1 protein or no Ssd1 protein at all. Stress sensitivity and interference with quiescence are recessive traits of the Ssd1-2 protein which means that they can be rescued by the presence of a full length Ssd1 protein. In contrast, the presence of a full length Ssd1 protein does not prevent the dominant function of Ssd1-2 in promoting spore formation. Together, these findings highlight a newfound function of the Ssd1-2 truncation protein to drive sporulation and restrict quiescence in response to stress. Understanding the nature and function of Ssd1-2 could provide new insight into how cells read and respond to environmental influences.

The full length Ssd1 protein (SSD1-1/SSD1-1), the deletion of the ssd1 gene (ssd1∆/ssd1∆), and the truncation mutant (ssd1-2/ssd1-2) were studied in the context of diploid S. cerevisiae cells for their roles in promoting quiescence or sporulation under nutrient deprivation stress. Yeast strain ssd1-2/ssd1-2 blocks cells from entering quiescence and increases sporulation in response to stress.
The full length Ssd1 protein (SSD1-1/SSD1-1), the deletion of the ssd1 gene (ssd1∆/ssd1∆), and the truncation mutant (ssd1-2/ssd1-2) were studied in the context of diploid S. cerevisiae cells for their roles in promoting quiescence or sporulation under nutrient deprivation stress. Yeast strain ssd1-2/ssd1-2 blocks cells from entering quiescence and increases sporulation in response to stress. Image modified from the primary publication

The spotlighted research was funded by the National Institutes of General Medical Sciences.

Breeden L, Miles S. 2022. A common SSD1 truncation is toxic to cells entering quiescence and promotes sporulation. MicroPubl Biol. 2022:10.17912/micropub.biology.000671.