ARGONAUTE10 controls cell fate specification and formative cell divisions in the Arabidopsis root

A key question in plant biology is how oriented cell divisions are integrated with patterning mechanisms to generate organs with adequate cell type allocation. In the root vasculature, a gradient of miRNA165/6 controls the abundance of HD-ZIP III transcription factors, which in turn control cell fate and spatially restrict vascular cell proliferation to specific cells. Here, we show that vascular development requires the presence of ARGONAUTE10, which is thought to sequester miRNA165/6 and protect HD-ZIP III transcripts from degradation. Our results suggest that the miR165/6-AGO10-HDZIP III module acts by buffering cytokinin responses and restricting xylem differentiation. Mutants of AGO10 show faster growth rates and strongly enhanced survival under severe drought conditions. However, this superior performance is offset by markedly increased variation and phenotypic plasticity in sub-optimal carbon supply conditions. Thus, AGO10 is required for the control of formative cell division and coordination of robust cell fate specification of the vasculature, while altering its expression provides a means to adjust phenotypic plasticity. In the Arabidopsis root vascular tissue, a gradient of miRNA165/6 controls the abundance of HD-ZIP III transcription factors, which in turn control cell fate and spatially restrict vascular cell proliferation to specific cells. This work shows that vascular development requires ARGONAUTE10 to sequester miRNA165/6, thus protecting HD-ZIP III transcripts from degradation.AGO10 controls formative cell divisions in the centre of the root stele, with its loss leading to ectopic xylem strands, increased procambial cell number, and enhanced root growth. Consistent with a role in protecting HD-ZIP III transcripts from miRNA165/6-mediated degradation, AGO10 is mostly expressed in the centre of the meristematic stele. AGO10 promotes HD-ZIP III activity to suppress cytokinin responses in the stele. AGO10 mutants outperform the wild type under water-limiting conditions. However, AGO10 is required for phenotypic robustness upon reduced carbon availability. AGO10 sequesters miRNA165/6 to suppress cytokinin-dependent responses in the root apical meristem.