The AUX1-AFB1-CNGC14 module establishes a longitudinal root surface pH profile

Abstract

Plant roots navigate in the soil environment following the gravity vector. Cell divisions in the meristem and rapid cell growth in the elongation zone propel the root tips through the soil. Actively elongating cells acidify their apoplast to enable cell wall extension by the activity of plasma membrane AHA H+-ATPases. The phytohormone auxin, central regulator of gravitropic response and root development, inhibits root cell growth, likely by rising the pH of the apoplast. However, the role of auxin in the regulation of the apoplastic pH gradient along the root tip is unclear. Here we show, by using an improved method for visualization and quantification of root surface pH, that the Arabidopsis thaliana root surface pH shows distinct acidic and alkaline zones, which are not primarily determined by the activity of AHA H+-ATPases. Instead, the distinct domain of alkaline pH in the root transition zone is controlled by a rapid auxin response module, consisting of the AUX1 auxin influx carrier, the AFB1 auxin co-receptor and the CNCG14 calcium channel. We demonstrate that the rapid auxin response pathway is required for an efficient navigation of the root tip.

Auxin co‐receptor IAA17/AXR3 controls cell elongation in Arabidopsis thaliana root solely by modulation of nuclear auxin pathway

“…As we showed, NAP inhibits root cell elongation through transcription of genes by the activator ARF5/MP and its inhibitor IAA17/AXR3. At the same time, CAP regulates cell expansion and alkalinization of the apoplast by the AFB1‐CNGC14 module (Dubey et al ., 2023; Serre et al ., 2023). Do these pathways depend on each other?…”

“…Next, we focused on analyzing the longitudinal root surface pH profile. To study the effect of altered NAP on root pH profile, we visualized root surface pH of vertically growing iAXR3‐1 and iMPΔ 4 h after induction using a pH‐sensitive fluorescent dye fluorescein‐5‐(and‐6)‐sulfonic acid (Serre et al ., 2023). Overexpression of AXR3‐1 led to root surface acidification, whereas iMPΔ roots showed a more alkaline surface pH.…”

“…Additionally, auxin‐modulated apoplastic pH changes serve as one of the drivers of growth (Monshausen et al ., 2011; Barbez et al ., 2017; Serre et al ., 2023), by the regulation the activity of cell wall proteins (Rayle & Cleland, 1992). Our results show the tight correlation of root surface pH with the overall root growth rate: while alkaline pH corresponds to slowed growth of iMPΔ , surface acidification correlates with growth promotion of iAXR3‐1 .…”

“…However, Serre et al . (2023) revealed that root surface pH does not fully correlate with local growth rates, showing distinct acidic and alkaline domains on the Arabidopsis root surface. They found the lowest pH values at the very tip of the root and in the maturation zone, with an alkaline domain in the transition zone and partially covering the early elongation zone.…”

“…The change in apoplastic pH and the creation of pH domains are crucial during the gravitropic response (Monshausen et al ., 2011; Shih et al ., 2015; Serre et al ., 2023). Upon gravistimulation, the alkaline domain on the lower nongrowing side of the root rapidly increased, while on the upper elongating side, the alkaline domain diminished, and the root surface became acidic.…”