Rie1 and Sgn1 form an RNA-binding complex that enforces the meiotic entry cell fate decision

• Published in: The Journal of cell biology Vol. 222; no. 11; p. 1
• Main Authors: Gaspary, Alec, Laureau, Raphaelle, Dyatel, Annie, Dursuk, Gizem, Simon, Yael, Berchowitz, Luke E
• Format: Journal Article
• Language: English
• Published: United States Rockefeller University Press 06.11.2023
• Subjects: Binding; Cell activation; Cell cycle and division; Cell Cycle Checkpoints; Cell Differentiation - genetics; Cell fate; Cell Size; Decisions; Desiccation; Development; Environmental conditions; Genetic screening; Genetics; Meiosis; Meiosis - genetics; Membrane Proteins - genetics; Phenotypes; Post-transcription; Proteins; Repressors; Ribonucleic acid; RNA; RNA biology; RNA-binding protein; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae Proteins - genetics; Spores; Sporulation; Transcription activation; Transcription factors; Vegetative cells; Yeast; Yeasts
• ISSN: 0021-9525; 1540-8140
• DOI: 10.1083/jcb.202302074

Budding yeast cells have the capacity to adopt few but distinct physiological states depending on environmental conditions. Vegetative cells proliferate rapidly by budding while spores can survive prolonged periods of nutrient deprivation and/or desiccation. Whether or not a yeast cell will enter meiosis and sporulate represents a critical decision that could be lethal if made in error. Most cell fate decisions, including those of yeast, are understood as being triggered by the activation of master transcription factors. However, mechanisms that enforce cell fates posttranscriptionally have been more difficult to attain. Here, we perform a forward genetic screen to determine RNA-binding proteins that affect meiotic entry at the posttranscriptional level. Our screen revealed several candidates with meiotic entry phenotypes, the most significant being RIE1, which encodes an RRM-containing protein. We demonstrate that Rie1 binds RNA, is associated with the translational machinery, and acts posttranscriptionally to enhance protein levels of the master transcription factor Ime1 in sporulation conditions. We also identified a physical binding partner of Rie1, Sgn1, which is another RRM-containing protein that plays a role in timely Ime1 expression. We demonstrate that these proteins act independently of cell size regulation pathways to promote meiotic entry. We propose a model explaining how constitutively expressed RNA-binding proteins, such as Rie1 and Sgn1, can act in cell fate decisions both as switch-like enforcers and as repressors of spurious cell fate activation.