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The cyclin CYCA3;4 is a postprophase target of the APC/CCCS52A2 E3-ligase controlling formative cell divisions in Arabidopsis

Alex Willems (UGent) , Jefri Heyman (UGent) , Thomas Eekhout (UGent) , Ignacio Achón (UGent) , José Antonio Pedroza-Garcia (UGent) , Tingting Zhu (UGent) , Lei Li (UGent) , Ilse Vercauteren (UGent) , Hilde Van Den Daele (UGent) , Brigitte Van De Cotte (UGent) , et al.
(2020) PLANT CELL. 32(9). p.2979-2996
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Abstract
The Anaphase Promoting Complex/Cyclosome (APC/C) controls unidirectional progression through the cell cycle by marking key cell cycle proteins for proteasomal turnover. Its activity is temporally regulated by the docking of different activating subunits, known in plants as CELL DIVISION PROTEIN 20 (CDC20) and CELL CYCLE SWITCH 52 (CCS52). Despite the importance of the APC/C during cell proliferation, the number of identified targets in the plant cell cycle is limited. Here, we used the growth and meristem phenotypes of Arabidopsis thaliana CCS52A2-deficient plants in a suppressor mutagenesis screen to identify APC/CCCS52A2 substrates or regulators, resulting in the identification of a mutant cyclin CYCA3;4 allele. CYCA3;4 deficiency partially rescues the ccs52a2-1 phenotypes, whereas increased CYCA3;4 levels enhance the ccs52a2-1 phenotypes. Furthermore, whereas CYCA3;4 proteins are promptly broken down after prophase in wild-type plants, they remain present in later stages of mitosis in ccs52a2-1 mutant plants, marking them as APC/CCCS52A2 substrates. Strikingly, increased CYCA3;4 levels result in aberrant root meristem and stomatal divisions, mimicking phenotypes of plants with reduced RETINOBLASTOMA-RELATED PROTEIN 1 (RBR1) activity. Correspondingly, RBR1 hyperphosphorylation was observed in CYCA3;4 gain-of-function plants. Our data thus demonstrate that an inability to timely destroy CYCA3;4 contributes to disorganized formative divisions, possibly in part caused by the inactivation of RBR1.
Keywords
Plant Science, Cell Biology, ANAPHASE-PROMOTING COMPLEX, MULTIPLE MECHANISMS, ENDOCYCLE, ENDOREDUPLICATION, DIFFERENTIATION, MAINTENANCE, COMPLEX/CYCLOSOME, IDENTIFICATION, PROLIFERATION, ACTIVATORS

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MLA
Willems, Alex, et al. “The Cyclin CYCA3;4 Is a Postprophase Target of the APC/CCCS52A2 E3-Ligase Controlling Formative Cell Divisions in Arabidopsis.” PLANT CELL, vol. 32, no. 9, 2020, pp. 2979–96, doi:10.1105/tpc.20.00208.
APA
Willems, A., Heyman, J., Eekhout, T., Achón, I., Pedroza-Garcia, J. A., Zhu, T., … De Veylder, L. (2020). The cyclin CYCA3;4 is a postprophase target of the APC/CCCS52A2 E3-ligase controlling formative cell divisions in Arabidopsis. PLANT CELL, 32(9), 2979–2996. https://doi.org/10.1105/tpc.20.00208
Chicago author-date
Willems, Alex, Jefri Heyman, Thomas Eekhout, Ignacio Achón, José Antonio Pedroza-Garcia, Tingting Zhu, Lei Li, et al. 2020. “The Cyclin CYCA3;4 Is a Postprophase Target of the APC/CCCS52A2 E3-Ligase Controlling Formative Cell Divisions in Arabidopsis.” PLANT CELL 32 (9): 2979–96. https://doi.org/10.1105/tpc.20.00208.
Chicago author-date (all authors)
Willems, Alex, Jefri Heyman, Thomas Eekhout, Ignacio Achón, José Antonio Pedroza-Garcia, Tingting Zhu, Lei Li, Ilse Vercauteren, Hilde Van Den Daele, Brigitte Van De Cotte, Ive De Smet, and Lieven De Veylder. 2020. “The Cyclin CYCA3;4 Is a Postprophase Target of the APC/CCCS52A2 E3-Ligase Controlling Formative Cell Divisions in Arabidopsis.” PLANT CELL 32 (9): 2979–2996. doi:10.1105/tpc.20.00208.
Vancouver
1.
Willems A, Heyman J, Eekhout T, Achón I, Pedroza-Garcia JA, Zhu T, et al. The cyclin CYCA3;4 is a postprophase target of the APC/CCCS52A2 E3-ligase controlling formative cell divisions in Arabidopsis. PLANT CELL. 2020;32(9):2979–96.
IEEE
[1]
A. Willems et al., “The cyclin CYCA3;4 is a postprophase target of the APC/CCCS52A2 E3-ligase controlling formative cell divisions in Arabidopsis,” PLANT CELL, vol. 32, no. 9, pp. 2979–2996, 2020.
@article{8671124,
  abstract     = {{The Anaphase Promoting Complex/Cyclosome (APC/C) controls unidirectional progression through the cell cycle by marking key cell cycle proteins for proteasomal turnover. Its activity is temporally regulated by the docking of different activating subunits, known in plants as CELL DIVISION PROTEIN 20 (CDC20) and CELL CYCLE SWITCH 52 (CCS52). Despite the importance of the APC/C during cell proliferation, the number of identified targets in the plant cell cycle is limited. Here, we used the growth and meristem phenotypes of Arabidopsis thaliana CCS52A2-deficient plants in a suppressor mutagenesis screen to identify APC/CCCS52A2 substrates or regulators, resulting in the identification of a mutant cyclin CYCA3;4 allele. CYCA3;4 deficiency partially rescues the ccs52a2-1 phenotypes, whereas increased CYCA3;4 levels enhance the ccs52a2-1 phenotypes. Furthermore, whereas CYCA3;4 proteins are promptly broken down after prophase in wild-type plants, they remain present in later stages of mitosis in ccs52a2-1 mutant plants, marking them as APC/CCCS52A2 substrates. Strikingly, increased CYCA3;4 levels result in aberrant root meristem and stomatal divisions, mimicking phenotypes of plants with reduced RETINOBLASTOMA-RELATED PROTEIN 1 (RBR1) activity. Correspondingly, RBR1 hyperphosphorylation was observed in CYCA3;4 gain-of-function plants. Our data thus demonstrate that an inability to timely destroy CYCA3;4 contributes to disorganized formative divisions, possibly in part caused by the inactivation of RBR1.}},
  author       = {{Willems, Alex and Heyman, Jefri and Eekhout, Thomas and Achón, Ignacio and Pedroza-Garcia, José Antonio and Zhu, Tingting and Li, Lei and Vercauteren, Ilse and Van Den Daele, Hilde and Van De Cotte, Brigitte and De Smet, Ive and De Veylder, Lieven}},
  issn         = {{1040-4651}},
  journal      = {{PLANT CELL}},
  keywords     = {{Plant Science,Cell Biology,ANAPHASE-PROMOTING COMPLEX,MULTIPLE MECHANISMS,ENDOCYCLE,ENDOREDUPLICATION,DIFFERENTIATION,MAINTENANCE,COMPLEX/CYCLOSOME,IDENTIFICATION,PROLIFERATION,ACTIVATORS}},
  language     = {{eng}},
  number       = {{9}},
  pages        = {{2979--2996}},
  title        = {{The cyclin CYCA3;4 is a postprophase target of the APC/CCCS52A2 E3-ligase controlling formative cell divisions in Arabidopsis}},
  url          = {{http://dx.doi.org/10.1105/tpc.20.00208}},
  volume       = {{32}},
  year         = {{2020}},
}
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