TY - JOUR
T1 - Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane
AU - Salanenka, Yuliya
AU - Verstraeten, Inge
AU - Löfke, Christian
AU - Tabata, Kaori
AU - Naramoto, Satoshi
AU - Glanc, Matouš
AU - Friml, Jirí
N1 - Funding Information:
ACKNOWLEDGMENTS. 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; M. Muszkowski and M. Adamowski for help with data analysis; Arabidopsis Stock Centre for providing seed stocks; M. Fendrych for scientific discussions and technical help in confocal imaging; and M. De Cock for help in preparing the manuscript. The research leading to these results has received funding from the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant Agreement 282300.
Funding Information:
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; M. Muszkowski and M. Adamowski for help with data analysis; Arabidopsis Stock Centre for providing seed stocks; M. Fendrych for scientific discussions and technical help in confocal imaging; and M. De Cock for help in preparing the manuscript. The research leading to these results has received funding from the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant Agreement 282300.
Publisher Copyright:
© 2018 National Academy of Sciences. All Rights Reserved.
PY - 2018/4/3
Y1 - 2018/4/3
N2 - 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. Photoconver-tible 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 coregulat-ing multiple processes, including PIN-dependent auxin fluxes during tropic responses.
AB - 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. Photoconver-tible 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 coregulat-ing multiple processes, including PIN-dependent auxin fluxes during tropic responses.
KW - DELLA
KW - Gibberellin
KW - Microtubules
KW - Polar auxin transport
KW - Vesicle trafficking
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U2 - 10.1073/pnas.1721760115
DO - 10.1073/pnas.1721760115
M3 - Article
C2 - 29463731
AN - SCOPUS:85044822385
VL - 115
SP - 3716
EP - 3721
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 14
ER -