Termination of Shoot Gravitropic Responses by Auxin Feedback on PIN3 Polarity

Abstract

Plants adjust their growth according to gravity. Gravitropism involves gravity perception, signal transduction, and asymmetric growth response, with organ bending as a consequence [1]. Asymmetric growth results from the asymmetric distribution of the plant-specific signaling molecule auxin [2] that is generated by lateral transport, mediated in the hypocotyl predominantly by the auxin transporter PIN-FORMED3 (PIN3) [3-5]. Gravity stimulation polarizes PIN3 to the bottom sides of endodermal cells, correlating with increased auxin accumulation in adjacent tissues at the lower side of the stimulated organ, where auxin induces cell elongation and, hence, organ bending. A curvature response allows the hypocotyl to resume straight growth at a defined angle [6], implying that at some point auxin symmetry is restored to prevent overbending. Here, we present initial insights into cellular and molecular mechanisms that lead to the termination of the tropic response. We identified an auxin feedback on PIN3 polarization as underlying mechanism that restores symmetry of the PIN3-dependent auxin flow. Thus, two mechanistically distinct PIN3 polarization events redirect auxin fluxes at different time points of the gravity response: first, gravity-mediated redirection of PIN3-mediated auxin flow toward the lower hypocotyl side, where auxin gradually accumulates and promotes growth, and later PIN3 polarization to the opposite cell side, depleting this auxin maximum to end the bending. Accordingly, genetic or pharmacological interference with the late PIN3 polarization prevents termination of the response and leads to hypocotyl overbending. This observation reveals a role of auxin feedback on PIN polarity in the termination of the tropic response.

Genetic screen for factors mediating PIN polarization in gravistimulated Arabidopsis thaliana hypocotyls

“…This bending termination is triggered by the auxin‐mediated feedback regulation of PIN3 polar localization in endodermal cells at the lower side of the hypocotyls. After the increased auxin accumulation at the lower side of the hypocotyl, PIN3 at the outer PMs is specifically targeted for lytic degradation, whereas PIN3 at the inner cell sides persists (Rakusová et al ., ). Due to the activity of PIN3 at the inner cell sides, the auxin accumulation in the lower epidermis dissipates, asymmetric elongation stops and bending terminates (Rakusová et al ., ).…”

“…PINs are plasma membrane (PM)‐based auxin transporters of which the cellular polar localization controls auxin flow and thus asymmetric auxin distribution in various developmental processes, including tropic responses (Wiśniewska et al ., ; Kleine‐Vehn and Friml, ; Kleine‐Vehn et al ., ). Based on mutant phenotype, expression and localization pattern, as well as polarity change after tropic stimuli, PIN3 appears to be the main mediator of the lateral directional auxin transport during hypocotyl tropic responses (Friml et al ., ; Harrison and Masson, ; Ding et al ., ; Rakusová et al ., , ). Following gravistimulation, PIN3 in hypocotyl endodermal cells polarizes to the bottom PMs, which mediates auxin flow to and corresponding auxin accumulation at the lower organ side leading to growth promotion there and hypocotyl bending (Figure a,b; Rakusová et al ., , ).…”

“…Based on mutant phenotype, expression and localization pattern, as well as polarity change after tropic stimuli, PIN3 appears to be the main mediator of the lateral directional auxin transport during hypocotyl tropic responses (Friml et al ., ; Harrison and Masson, ; Ding et al ., ; Rakusová et al ., , ). Following gravistimulation, PIN3 in hypocotyl endodermal cells polarizes to the bottom PMs, which mediates auxin flow to and corresponding auxin accumulation at the lower organ side leading to growth promotion there and hypocotyl bending (Figure a,b; Rakusová et al ., , ). At the later stage of gravitropic bending, auxin distribution equalizes and hypocotyl terminates bending (Figure a,b; Rakusová et al ., ).…”

“…Following gravistimulation, PIN3 in hypocotyl endodermal cells polarizes to the bottom PMs, which mediates auxin flow to and corresponding auxin accumulation at the lower organ side leading to growth promotion there and hypocotyl bending (Figure a,b; Rakusová et al ., , ). At the later stage of gravitropic bending, auxin distribution equalizes and hypocotyl terminates bending (Figure a,b; Rakusová et al ., ). This bending termination is triggered by the auxin‐mediated feedback regulation of PIN3 polar localization in endodermal cells at the lower side of the hypocotyls.…”

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

“…Our data suggest a model in which subcellular PIN3 localization shifts from basal to apical membranes in vascular cells near the wound to redirect auxin flow backward and thus maintaining high auxin levels in the proximal petiole vasculature. Interestingly, an auxin-dependent switch in PIN3 polarization contributing to auxin-flow reversal is involved in the shoot gravitropic response (Rakusová et al, 2016), where basal-to-apical shift in PIN localization has been described to depend on phosphorylation (Dai et al, 2012). It is thus tempting to speculate that auxin-dependent phosphorylation of PIN3 would be involved in maintaining high auxin levels in the petiole base vasculature during root regeneration.…”