Molecular Basis for a Cell Fate Switch in Response to Impaired Ribosome Biogenesis in the Arabidopsis Root Epidermis

The Arabidopsis (Arabidopsis thaliana) root epidermis consists of a position-dependent pattern of root hair cells and non-hair cells. Underlying this cell type patterning is a network of transcription factors including a central MYB-basic helix-loop-helix-WD40 complex containing WEREWOLF (WER), GLABRA3 (GL3)/ENHANCER OF GLABRA3, and TRANSPARENT TESTA GLABRA1. In this study, we used a genetic enhancer screen to identify apum23-4, a mutant allele of the ribosome biogenesis factor (RBF) gene ARABIDOPSIS PUMILIO23 (APUM23), which caused prospective root hair cells to instead adopt the non-hair cell fate. We discovered that this cell fate switch relied on MYB23, a MYB protein encoded by a WER target gene and acting redundantly with WER. In the apum23-4 mutant, MYB23 exhibited ectopic expression that was WER independent and instead required ANAC082, a recently identified ribosomal stress response mediator. We examined additional RBF mutants that produced ectopic non-hair cells and determined that this cell fate switch is generally linked to defects in ribosome biogenesis. Furthermore, the flagellin peptide flg22 triggers the ANAC082-MYB23-GL2 pathway. Taken together, our study provides a molecular explanation for root epidermal cell fate switch in response to ribosomal defects and, more generally, it demonstrates a novel regulatory connection between stress conditions and cell fate control in plants.