Low inorganic phosphate (Pi) availability causes terminal differentiation of the root apical meristem (RAM), a phenomenon known as root meristem exhaustion or determined growth. Here, we report that the CLE14 peptide acts as a key player in this process. Low Pi stress induces iron mobilization in the RAM through the action of LPR1/LPR2, causing expression of CLE14 in the proximal meristem region. CLV2 and PEPR2 receptors perceive CLE14 and trigger RAM differentiation, with concomitant downregulation of SHR/SCR and PIN/AUXIN pathway. Our results reveal multiple steps of the molecular mechanism of one of the most physiologically important root nutrient responses. Display omitted •CLE14 peptide is a component of the Pi starvation response•CLE14 is the signal that triggers full root meristem differentiation in low Pi•CLE14 acts downstream of LOW PHOSPHATE ROOT1/LOW PHOSPHATE ROOT2 (LPR1/LPR2)•CLE14 triggers full root meristem differentiation through CLV2/PEPR2 receptors Phosphorus limitation profoundly affects root development in Arabidopsis thaliana. Gutiérrez-Alanís et al. show that in response to low Pi, CLE14 peptide is expressed in proximal meristem, is perceived by CLV2 and PEPR2 receptors, and causes differentiation of surrounding RAM, leading to root meristem exhaustion.