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A developmentally controlled cellular decompartmentalization process executes programmed cell death in the Arabidopsis root cap

Jie Wang (UGent) , Norbert Bollier (UGent) , Rafael Andrade Buono (UGent) , Hannah Vahldick (UGent) , Zongcheng Lin (UGent) , Qiang-Nan Feng (UGent) , Roman Hudecek, Qihang Jiang (UGent) , Evelien Mylle (UGent) , Daniël Van Damme (UGent) , et al.
(2024) PLANT CELL. 36(4). p.941-962
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Abstract
Programmed cell death (PCD) is a fundamental cellular process crucial to development, homeostasis, and immunity in multicellular eukaryotes. In contrast to our knowledge on the regulation of diverse animal cell death subroutines, information on execution of PCD in plants remains fragmentary. Here we make use of the accessibility of the Arabidopsis (Arabidopsis thaliana) root cap to visualize the execution process of developmentally controlled PCD. We identify a succession of selective decompartmentalization events and ion fluxes as part of the terminal differentiation program that is orchestrated by the NAC (NO APICAL MERISTEM, ARABIDOPSIS THALIANA ACTIVATING FACTOR, CUP-SHAPED COTYLEDON) transcription factor SOMBRERO. Surprisingly, breakdown of the large central vacuole is a relatively late and variable event, preceded by an increase of intracellular calcium levels and acidification, release of mitochondrial matrix proteins, leakage of nuclear and endoplasmic reticulum lumina, and release of fluorescent membrane reporters into the cytosol. In analogy to animal apoptosis, the plasma membrane remains impermeable for proteins during and after PCD execution. Elevated intracellular calcium levels and acidification are sufficient to trigger cell death execution specifically in terminally differentiated root cap cells, suggesting that these ion fluxes act as PCD-triggering signals. This detailed information on the cellular processes occurring during developmental PCD in plants is a pivotal prerequisite for future research into the molecular mechanisms of cell death execution.
Keywords
PCD, Programmed cell death, calcium, dPCD, development, developmentally controlled programmed cell death, membrane permeabilization, membranes, pH, regulated cell death, root cap, SELF-INCOMPATIBILITY, FLUORESCENT INDICATORS, TRANSCRIPTION FACTORS, TRACHEARY ELEMENTS, CYTOCHROME-C, PLANT, EXPRESSION, MATURATION, REPRODUCTION, DIVISION

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Citation

Please use this url to cite or link to this publication:

MLA
Wang, Jie, et al. “A Developmentally Controlled Cellular Decompartmentalization Process Executes Programmed Cell Death in the Arabidopsis Root Cap.” PLANT CELL, vol. 36, no. 4, 2024, pp. 941–62, doi:10.1093/plcell/koad308.
APA
Wang, J., Bollier, N., Andrade Buono, R., Vahldick, H., Lin, Z., Feng, Q.-N., … Nowack, M. (2024). A developmentally controlled cellular decompartmentalization process executes programmed cell death in the Arabidopsis root cap. PLANT CELL, 36(4), 941–962. https://doi.org/10.1093/plcell/koad308
Chicago author-date
Wang, Jie, Norbert Bollier, Rafael Andrade Buono, Hannah Vahldick, Zongcheng Lin, Qiang-Nan Feng, Roman Hudecek, et al. 2024. “A Developmentally Controlled Cellular Decompartmentalization Process Executes Programmed Cell Death in the Arabidopsis Root Cap.” PLANT CELL 36 (4): 941–62. https://doi.org/10.1093/plcell/koad308.
Chicago author-date (all authors)
Wang, Jie, Norbert Bollier, Rafael Andrade Buono, Hannah Vahldick, Zongcheng Lin, Qiang-Nan Feng, Roman Hudecek, Qihang Jiang, Evelien Mylle, Daniël Van Damme, and Moritz Nowack. 2024. “A Developmentally Controlled Cellular Decompartmentalization Process Executes Programmed Cell Death in the Arabidopsis Root Cap.” PLANT CELL 36 (4): 941–962. doi:10.1093/plcell/koad308.
Vancouver
1.
Wang J, Bollier N, Andrade Buono R, Vahldick H, Lin Z, Feng Q-N, et al. A developmentally controlled cellular decompartmentalization process executes programmed cell death in the Arabidopsis root cap. PLANT CELL. 2024;36(4):941–62.
IEEE
[1]
J. Wang et al., “A developmentally controlled cellular decompartmentalization process executes programmed cell death in the Arabidopsis root cap,” PLANT CELL, vol. 36, no. 4, pp. 941–962, 2024.
@article{01HHJ471R6VTX3TJ7VV81BMQAA,
  abstract     = {{Programmed cell death (PCD) is a fundamental cellular process crucial to development, homeostasis, and immunity in multicellular eukaryotes. In contrast to our knowledge on the regulation of diverse animal cell death subroutines, information on execution of PCD in plants remains fragmentary. Here we make use of the accessibility of the Arabidopsis (Arabidopsis thaliana) root cap to visualize the execution process of developmentally controlled PCD. We identify a succession of selective decompartmentalization events and ion fluxes as part of the terminal differentiation program that is orchestrated by the NAC (NO APICAL MERISTEM, ARABIDOPSIS THALIANA ACTIVATING FACTOR, CUP-SHAPED COTYLEDON) transcription factor SOMBRERO. Surprisingly, breakdown of the large central vacuole is a relatively late and variable event, preceded by an increase of intracellular calcium levels and acidification, release of mitochondrial matrix proteins, leakage of nuclear and endoplasmic reticulum lumina, and release of fluorescent membrane reporters into the cytosol. In analogy to animal apoptosis, the plasma membrane remains impermeable for proteins during and after PCD execution. Elevated intracellular calcium levels and acidification are sufficient to trigger cell death execution specifically in terminally differentiated root cap cells, suggesting that these ion fluxes act as PCD-triggering signals. This detailed information on the cellular processes occurring during developmental PCD in plants is a pivotal prerequisite for future research into the molecular mechanisms of cell death execution.}},
  author       = {{Wang, Jie and Bollier, Norbert and Andrade Buono, Rafael and Vahldick, Hannah and Lin, Zongcheng and Feng, Qiang-Nan and Hudecek, Roman and Jiang, Qihang and Mylle, Evelien and Van Damme, Daniël and Nowack, Moritz}},
  issn         = {{1040-4651}},
  journal      = {{PLANT CELL}},
  keywords     = {{PCD,Programmed cell death,calcium,dPCD,development,developmentally controlled programmed cell death,membrane permeabilization,membranes,pH,regulated cell death,root cap,SELF-INCOMPATIBILITY,FLUORESCENT INDICATORS,TRANSCRIPTION FACTORS,TRACHEARY ELEMENTS,CYTOCHROME-C,PLANT,EXPRESSION,MATURATION,REPRODUCTION,DIVISION}},
  language     = {{eng}},
  number       = {{4}},
  pages        = {{941--962}},
  title        = {{A developmentally controlled cellular decompartmentalization process executes programmed cell death in the Arabidopsis root cap}},
  url          = {{http://doi.org/10.1093/plcell/koad308}},
  volume       = {{36}},
  year         = {{2024}},
}
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