Rapid auxin-mediated phosphorylation of Myosin regulates trafficking and polarity in Arabidopsis

Abstract

The signaling molecule auxin controls plant development through a well-known transcriptional mechanism that regulates many genes. However, auxin also triggers cellular responses within seconds or minutes, and mechanisms mediating such fast responses have remained elusive. Here, we identified an ultrafast auxin-mediated protein phosphorylation response in Arabidopsis roots that is largely independent of the canonical TIR1/AFB receptors. Among targets of this novel response are Myosin XI and its adaptor protein MadB2. We show that their auxin-mediated phosphorylation regulates trafficking and polar, subcellular distribution of PIN auxin transporters. This phosphorylation-based auxin signaling module is indispensable during developmental processes that rely on auxin-mediated PIN repolarization, such as termination of shoot gravitropic bending or vasculature formation and regeneration. Hence, we identified a fast, non-canonical auxin response targeting multiple cellular processes and revealed auxin-triggered phosphorylation of a myosin complex as the mechanism for feedback regulation of directional auxin transport, a central component of auxin canalization, which underlies self-organizing plant development.

Xyloglucan Remodeling Defines Auxin-Dependent Differential Tissue Expansion in Plants

“…Phosphorylation of CELLULOSE SYNTHASE A (CESA) is a known regulation of cellulose biosynthesis [52,53]. Considering the ultrafast auxin-mediated protein phosphorylation response [54] a similar post-translational regulation could be envisioned to directly or indirectly impact on XyG-related enzymes.…”

Fourteen Stations of Auxin

“…Transcriptomics, now approaching the single-cell resolution limit (Seyfferth et al 2021), is changing the way we approach questions related to auxin functions in transcriptional reprogramming (Bargmann et al 2013;Wendrich et al 2020). Similar developments in proteomics and phosphoproteomics (Smith et al 2020;Han et al 2021) promise to advance our knowledge of nontranscriptional aspects of auxin signaling. Further improvements in metabolomics, especially allowing subcellular resolution, will boost our knowledge on compartmentalization of auxin and its metabolism (Pěnčík et al 2018).…”

“…PIN proteins undergo constant endocytic cycling and are degraded in the vacuole (for review, see Adamowski and Friml 2015). Auxin influences these processes by an unclear mechanism involving myosin phosphorylation (Han et al 2021). So-called short PINs and PILS mediate auxin in-and efflux in the endoplasmic reticulum (ER) (for review, see Abdollahi Sisi and Růžička 2020).…”

“…Another rapid, nontranscriptional, and indeed TIR1/AFB-independent process is the auxin effect on endocytic trafficking of PIN auxin transporters (Paciorek et al 2005;Robert et al 2010). As a potential mechanism involved in the auxin feedback regulation of its own transport and its polarization (Mazur et al 2020a;Han et al 2021), this response has received substantial attention. Recently, the original interpretation that involves auxin inhibiting endocytosis has been revised with new tools and approaches (Narasimhan et al 2021) and it appears that auxin rather targets actin/myosin-related aspects of endocytic PIN trafficking (Arieti and Staiger 2020;Han et al 2021).…”

PIN‐mediated polar auxin transport regulations in plant tropic responses

“…When auxin gradually accumulates on the lower hypocotyl side, this triggers PIN3 repolarization to the inner side of endodermal cells which (re)establishes a symmetric PIN localization and restoration of the symmetric auxin distribution across the organ, resulting in bending termination. This auxin‐triggered feedback on PIN repolarization requires the SCF TIR1/AFB auxin signaling (Han et al ., 2020), clathrin‐mediated endocytosis, GNOM‐mediated trafficking, PID‐mediated phosphorylation (Rakusová et al ., 2016), actin cytoskeleton (Rakusová et al ., 2019) and Myosin XI activity (Han et al ., 2021). Such an auxin feedback mechanism ensures the fine‐tuning of auxin fluxes for termination of asymmetric growth during shoot gravitropic and phototropic responses.…”