Early sensing of phosphate deprivation triggers the formation of extra root cap cell layers via SOMBRERO through a process antagonized by auxin signaling

Abstract

Key messageThe role of the root cap in the plant response to phosphate deprivation has been scarcely investigated.Here we describe early structural, physiological and molecular changes prior to the determinate growth program of the primary roots under low Pi and unveil a critical function of the transcription factor SOMBRERO in low Pi sensing. Abstract Mineral nutrient distribution in the soil is uneven and roots efficiently adapt to improve uptake and assimilation of sparingly available resources. Phosphate (Pi) accumulates in the upper layers and thus short and branched root systems proliferate to better exploit organic and inorganic Pi patches. Here we report an early adaptive response of the Arabidopsis primary root that precedes the entrance of the meristem into the determinate developmental program that is a hallmark of the low Pi sensing mechanism. In wild-type seedlings transferred to low Pi medium, the quiescent center domain in primary root tips increases as an early response, as revealed by WOX5:GFP expression and this correlates with a thicker root tip with extra root cap cell layers. The halted primary root growth in WT seedlings could be reversed upon transfer to medium supplemented with 250 µM Pi. Mutant and gene expression analysis indicates that auxin signaling negatively affects the cellular re-specification at the root tip and enabled identification of the transcription factor SOMBRERO as a critical element that orchestrates both the formation of extra root cap layers and primary root growth under Pi scarcity. Moreover, we provide evidence that low Pi-induced root thickening or the loss-of-function of SOMBRERO is associated with expression of phosphate transporters at the root tip. Our data uncover a developmental window where the root tip senses deprivation of a critical macronutrient to improve adaptation and surveillance.

Local and systemic responses conferring acclimation of Brassica napus roots to low phosphorus conditions

“…Local responses are modulated by the external Pi availability in the growth medium, while systemic responses depend on the internal Pi concentrations in the plant (Svistoonoff et al, 2007;Lin et al, 2014). The root cap is positioned at the very end of the root tip and is responsible for sensing Pi availability (Svistoonoff et al, 2007;Ticconi et al, 2009;Ravelo-Ortega et al, 2022). Manipulating local Pi availability through split-root experiments mimics the heterogeneous Pi distribution in soil and allows changes in RSA and local and systemic responses to Pi starvation to be determined (Franco-Zorrilla, 2005;Thibaud et al, 2010).…”

“…PHOSPHATE DEFICIENCY RE-SPONSE 2 (PDR2) and LPR1 may function together in mediating responses of the root meristem to external Pi availability (Ticconi et al, 2009;Ruiz-Herrera et al, 2015). Local low Pi sensing enhances auxin responses and involves mitogen-activated protein kinase 6 (MPK6) signalling within the root tip, particularly the root cap via SOMBRERO (Pérez-Torres et al, 2008;López-Bucio et al, 2019;Ravelo-Ortega et al, 2022). In addition, the SENSITIVE TO PROTON RHIZOTOX-ICITY1-MEDIATOR16-ALUMINUM-ACTIVATED MALATE TRANSPORT1 (STOP1-MED16-ALMT1) signalling module is involved in root system remodelling in response to low Pi availability (Raya-González et al, 2021;).…”