TGA family of transcription factors are nitric oxide sensors in the root stem cell niche

Abstract

Plant root development is tightly regulated and depends on the coordination among different cell types located in the root stem cell niche (SCN). A complex network of regulators includes the gasotransmitter nitric oxide (NO) known to inhibit primary root growth, modify root architecture and alter meristem organisation. However, little is known about the molecular targets of this signalling molecule during root SCN homeostasis. Here, genetic, molecular and physiological evidence support that TGA transcription factors (TFs) of the bZIP family, and specifically PERIANTHIA (PAN), contribute to the regulation of the root SCN through NO sensing. This gasotransmitter induces reversible S-nitrosylation of PAN, thereby inhibiting its binding to DNA and associated transcriptional activation; whilst the protein-SNO reductase activity of TRXh5 can denitrosylate PAN. This switch on and off mechanism for PAN activity modulates gene expression in the SCN and the functioning of the quiescent centre, thereby altering columella stem cell maintenance through a NO-dependent mechanism. Furthermore, PAN interacts selectively with several TGA members which are susceptible to differential S-nitrosylation. Given the functional redundancy within the TGA family, analysis of quadruple and pentuple mutants revealed close coordination between PAN and other members of this family of TFs, which contributes to the NO sensing during the development of the root apical meristem. Collectively, these findings reveal a molecular framework in which the TGA family, primarily coordinated by PAN activity, acts as a master NO sensor in the root SCN.