Cytokinins control secondary cell wall formation in the inflorescence stem of Arabidopsis

Spatiotemporal control over developmental programs is vital to all organisms. Here, we show that deficiency in cytokinin signaling or biosynthesis leads to early secondary cell wall (SCW) formation in Arabidopsis inflorescence stem that associates with precocious upregulation of an SCW transcriptional cascade controlled by NAC transcription factors (NSTs/VNDs). Cytokinin signaling through AHK2/3 and the ARR1/10/12 suppresses the expression of several NST genes and SCW formation. Exogenous cytokinin application led to fast downregulation of NST1 and NST3 (NST1/3) in the wild type and reconstituted both proper development and the apical-basal gradient of NST1/3 expression in a cytokinin-deficient mutant. AHK2 and AHK3 require functional NST1 or NST3 to control SCW initiation in the interfascicular fibers, demonstrating that cytokinins act upstream of NSTs. The premature onset of a rigid SCW biosynthesis and altered expression of NSTs due to cytokinin deficiency led to the formation of smaller tracheary elements and impaired hydraulic conductivity. We conclude that cytokinins downregulate NST genes to inhibit premature SCW formation in the apical part of the inflorescence stem, facilitating thus the development of fully functional tracheary elements and interfascicular fibers.