The plant hormone gibberellic acid (GA) is a crucial regulator of growth and development. The main paradigm of GA signaling puts forward transcriptional regulation via the degradation of DELLA transcriptional repressors. GA has also been shown to regulate tropic responses by modulation of the plasma membrane incidence of PIN auxin transporters by an unclear mechanism. Here we uncovered the cellular and molecular mechanisms by which GA redirects protein trafficking and thus regulates cell surface functionality. Photoconvertible reporters revealed that GA balances the protein traffic between the vacuole degradation route and recycling back to the cell surface. Low GA levels promote vacuolar delivery and degradation of multiple cargos, including PIN proteins, whereas high GA levels promote their recycling to the plasma membrane. This GA effect requires components of the retromer complex, such as Sorting Nexin 1 (SNX1) and its interacting, microtubule (MT)-associated protein, the Cytoplasmic Linker-Associated Protein (CLASP1). Accordingly, GA regulates the subcellular distribution of SNX1 and CLASP1, and the intact MT cytoskeleton is essential for the GA effect on trafficking. This GA cellular action occurs through DELLA proteins that regulate the MT and retromer presumably via their interaction partners Prefoldins (PFDs). Our study identified a branching of the GA signaling pathway at the level of DELLA proteins, which, in parallel to regulating transcription, also target by a nontranscriptional mechanism the retromer complex acting at the intersection of the degradation and recycling trafficking routes. By this mechanism, GA can redirect receptors and transporters to the cell surface, thus coregulating multiple processes, including PIN-dependent auxin fluxes during tropic responses.
We gratefully acknowledge M. Blázquez (Instituto de Biología Molecular y Celular de Plantas), M. Fendrych, C. Cuesta Moliner (Institute of Science and Technology Austria), M. Vanstraelen, M. Nowack (Center for Plant Systems Biology, Ghent), C. Luschnig (Universitat fur Bodenkultur Wien, Vienna), S. Simon (Central European Institute of Technology, Brno), C. Sommerville (Carnegie Institution for Science), and Y. Gu (Penn State University) for making available the materials used in this study; ...funding from the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant Agreement 282300. CC BY NC ND
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Salanenka Y, Verstraeten I, Löfke C, et al. Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane. PNAS. 2018;115(14):3716-3721. doi:10.1073/pnas.1721760115
Salanenka, Y., Verstraeten, I., Löfke, C., Tabata, K., Naramoto, S., Glanc, M., & Friml, J. (2018). Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane. PNAS, 115(14), 3716–3721. https://doi.org/10.1073/pnas.1721760115
Salanenka, Yuliya, Inge Verstraeten, Christian Löfke, Kaori Tabata, Satoshi Naramoto, Matous Glanc, and Jirí Friml. “Gibberellin DELLA Signaling Targets the Retromer Complex to Redirect Protein Trafficking to the Plasma Membrane.” PNAS 115, no. 14 (2018): 3716–21. https://doi.org/10.1073/pnas.1721760115.
Y. Salanenka et al., “Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane,” PNAS, vol. 115, no. 14, pp. 3716–3721, 2018.
Salanenka Y, Verstraeten I, Löfke C, Tabata K, Naramoto S, Glanc M, Friml J. 2018. Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane. PNAS. 115(14), 3716–3721.
Salanenka, Yuliya, et al. “Gibberellin DELLA Signaling Targets the Retromer Complex to Redirect Protein Trafficking to the Plasma Membrane.” PNAS, vol. 115, no. 14, National Academy of Sciences, 2018, pp. 3716–21, doi:10.1073/pnas.1721760115.
2018_PNAS_Salanenka.pdf 1.92 MB