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TPLATE complex‐dependent endocytosis attenuates CLAVATA1 signaling for shoot apical meristem maintenance

(2023) EMBO REPORTS. 24(9).
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Abstract
Endocytosis regulates the turnover of cell surface localized receptors, which are crucial for plants to rapidly respond to stimuli. The evolutionary ancient TPLATE complex (TPC) plays an essential role in endocytosis in Arabidopsis plants. Knockout or knockdown of single TPC subunits causes male sterility and seedling lethality phenotypes, complicating analysis of the roles of TPC during plant development. Partially functional alleles of TPC subunits however only cause mild developmental deviations. Here, we took advantage of the partially functional TPLATE allele, WDXM2, to investigate a role for TPC-dependent endocytosis in receptor-mediated signaling. We discovered that reduced TPC-dependent endocytosis confers a hypersensitivity to very low doses of CLAVATA3 peptide signaling. This hypersensitivity correlated with the abundance of the CLAVATA3 receptor protein kinase CLAVATA1 at the plasma membrane. Genetic and biochemical analysis as well as live-cell imaging revealed that TPC-dependent regulation of CLAVATA3-dependent internalization of CLAVATA1 from the plasma membrane is required for shoot stem cell homeostasis. Our findings provide evidence that TPC-mediated endocytosis and degradation of CLAVATA1 is a mechanism to dampen CLAVATA3-mediated signaling during plant development.
Keywords
Genetics, Molecular Biology, Biochemistry, clathrin-mediated endocytosis, CLAVATA3-CLAVATA1 signaling, shoot apical meristem maintenance, TPLATE complex, CLATHRIN-MEDIATED ENDOCYTOSIS, RECEPTOR KINASE, CLE PEPTIDES, BRASSINOSTEROID INSENSITIVE1, CELL FATE, ARABIDOPSIS, CLV3, PERCEPTION, PROTEIN, TRAFFICKING

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Citation

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MLA
Wang, Jie, et al. “TPLATE Complex‐dependent Endocytosis Attenuates CLAVATA1 Signaling for Shoot Apical Meristem Maintenance.” EMBO REPORTS, vol. 24, no. 9, 2023, doi:10.15252/embr.202254709.
APA
Wang, J., Jiang, Q., Pleskot, R., Grones, P., Bahafid, E., Denay, G., … Van Damme, D. (2023). TPLATE complex‐dependent endocytosis attenuates CLAVATA1 signaling for shoot apical meristem maintenance. EMBO REPORTS, 24(9). https://doi.org/10.15252/embr.202254709
Chicago author-date
Wang, Jie, Qihang Jiang, Roman Pleskot, Peter Grones, Elmehdi Bahafid, Grégoire Denay, Carlos Galván‐Ampudia, et al. 2023. “TPLATE Complex‐dependent Endocytosis Attenuates CLAVATA1 Signaling for Shoot Apical Meristem Maintenance.” EMBO REPORTS 24 (9). https://doi.org/10.15252/embr.202254709.
Chicago author-date (all authors)
Wang, Jie, Qihang Jiang, Roman Pleskot, Peter Grones, Elmehdi Bahafid, Grégoire Denay, Carlos Galván‐Ampudia, Xiangyu Xu, Michaël Vandorpe, Evelien Mylle, Ive De Smet, Teva Vernoux, Rüdiger Simon, Moritz Nowack, and Daniël Van Damme. 2023. “TPLATE Complex‐dependent Endocytosis Attenuates CLAVATA1 Signaling for Shoot Apical Meristem Maintenance.” EMBO REPORTS 24 (9). doi:10.15252/embr.202254709.
Vancouver
1.
Wang J, Jiang Q, Pleskot R, Grones P, Bahafid E, Denay G, et al. TPLATE complex‐dependent endocytosis attenuates CLAVATA1 signaling for shoot apical meristem maintenance. EMBO REPORTS. 2023;24(9).
IEEE
[1]
J. Wang et al., “TPLATE complex‐dependent endocytosis attenuates CLAVATA1 signaling for shoot apical meristem maintenance,” EMBO REPORTS, vol. 24, no. 9, 2023.
@article{01H5VDM6AYJTQ39BVR9YF66ZMY,
  abstract     = {{Endocytosis regulates the turnover of cell surface localized receptors, which are crucial for plants to rapidly respond to stimuli. The evolutionary ancient TPLATE complex (TPC) plays an essential role in endocytosis in Arabidopsis plants. Knockout or knockdown of single TPC subunits causes male sterility and seedling lethality phenotypes, complicating analysis of the roles of TPC during plant development. Partially functional alleles of TPC subunits however only cause mild developmental deviations. Here, we took advantage of the partially functional TPLATE allele, WDXM2, to investigate a role for TPC-dependent endocytosis in receptor-mediated signaling. We discovered that reduced TPC-dependent endocytosis confers a hypersensitivity to very low doses of CLAVATA3 peptide signaling. This hypersensitivity correlated with the abundance of the CLAVATA3 receptor protein kinase CLAVATA1 at the plasma membrane. Genetic and biochemical analysis as well as live-cell imaging revealed that TPC-dependent regulation of CLAVATA3-dependent internalization of CLAVATA1 from the plasma membrane is required for shoot stem cell homeostasis. Our findings provide evidence that TPC-mediated endocytosis and degradation of CLAVATA1 is a mechanism to dampen CLAVATA3-mediated signaling during plant development.}},
  articleno    = {{e54709}},
  author       = {{Wang, Jie and Jiang, Qihang and Pleskot, Roman and Grones, Peter and Bahafid, Elmehdi and Denay, Grégoire and Galván‐Ampudia, Carlos and Xu, Xiangyu and Vandorpe, Michaël and Mylle, Evelien and De Smet, Ive and Vernoux, Teva and Simon, Rüdiger and Nowack, Moritz and Van Damme, Daniël}},
  issn         = {{1469-221X}},
  journal      = {{EMBO REPORTS}},
  keywords     = {{Genetics,Molecular Biology,Biochemistry,clathrin-mediated endocytosis,CLAVATA3-CLAVATA1 signaling,shoot apical meristem maintenance,TPLATE complex,CLATHRIN-MEDIATED ENDOCYTOSIS,RECEPTOR KINASE,CLE PEPTIDES,BRASSINOSTEROID INSENSITIVE1,CELL FATE,ARABIDOPSIS,CLV3,PERCEPTION,PROTEIN,TRAFFICKING}},
  language     = {{eng}},
  number       = {{9}},
  pages        = {{13}},
  title        = {{TPLATE complex‐dependent endocytosis attenuates CLAVATA1 signaling for shoot apical meristem maintenance}},
  url          = {{http://doi.org/10.15252/embr.202254709}},
  volume       = {{24}},
  year         = {{2023}},
}

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