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A conserved but plant-specific CDK-mediated regulation of DNA replication protein A2 in the precise control of stomatal terminal division

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Abstract
The R2R3-MYB transcription factor FOUR LIPS (FLP) controls the stomatal terminal division through transcriptional repression of the cell cycle genes CYCLIN-DEPENDENT KINASE (CDK) B1s (CDKB1s), CDKA; 1, and CYCLIN A2s (CYCA2s). We mutagenized the weak mutant allele flp-1 seeds with ethylmethane sulfonate and screened out a flp-1 suppressor 1 (fsp1) that suppressed the flp-1 stomatal cluster phenotype. FSP1 encodes RPA2a subunit of Replication Protein A (RPA) complexes that play important roles in DNA replication, recombination, and repair. Here, we show that FSP1/RPA2a functions together with CDKB1s and CYCA2s in restricting stomatal precursor proliferation, ensuring the stomatal terminal division and maintaining a normal guard-cell size and DNA content. Furthermore, we provide direct evidence for the existence of an evolutionarily conserved, but plant-specific, CDK-mediated RPA regulatory pathway. Serine-11 and Serine-21 at the N terminus of RPA2a are CDK phosphorylation target residues. The expression of the phosphorylation-mimic variant RPA2a(S11,21/D) partially complemented the defective cell division and DNA damage hypersensitivity in cdkb1;1 1;2 mutants. Thus, our study provides a mechanistic understanding of the CDK-mediated phosphorylation of RPA in the precise control of cell cycle and DNA repair in plants.
Keywords
stomatal development, cell division, replication protein A, CDK, DNA damage, CYCLIN-DEPENDENT KINASE, RPA PHOSPHORYLATION, CELL-PROLIFERATION, DAMAGE RESPONSE, 4 LIPS, SUBUNIT, BINDING, REPAIR, CDC2, MUTATIONS

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MLA
Yang, Kezhen, et al. “A Conserved but Plant-Specific CDK-Mediated Regulation of DNA Replication Protein A2 in the Precise Control of Stomatal Terminal Division.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 36, 2019, pp. 18126–31.
APA
Yang, K., Zhu, L., Wang, H., Jiang, M., Xiao, C., Hu, X., … Le, J. (2019). A conserved but plant-specific CDK-mediated regulation of DNA replication protein A2 in the precise control of stomatal terminal division. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 116(36), 18126–18131.
Chicago author-date
Yang, Kezhen, Lingling Zhu, Hongzhe Wang, Min Jiang, Chunwang Xiao, Xiangyang Hu, Steffen Vanneste, Juan Dong, and Jie Le. 2019. “A Conserved but Plant-Specific CDK-Mediated Regulation of DNA Replication Protein A2 in the Precise Control of Stomatal Terminal Division.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116 (36): 18126–31.
Chicago author-date (all authors)
Yang, Kezhen, Lingling Zhu, Hongzhe Wang, Min Jiang, Chunwang Xiao, Xiangyang Hu, Steffen Vanneste, Juan Dong, and Jie Le. 2019. “A Conserved but Plant-Specific CDK-Mediated Regulation of DNA Replication Protein A2 in the Precise Control of Stomatal Terminal Division.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116 (36): 18126–18131.
Vancouver
1.
Yang K, Zhu L, Wang H, Jiang M, Xiao C, Hu X, et al. A conserved but plant-specific CDK-mediated regulation of DNA replication protein A2 in the precise control of stomatal terminal division. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2019;116(36):18126–31.
IEEE
[1]
K. Yang et al., “A conserved but plant-specific CDK-mediated regulation of DNA replication protein A2 in the precise control of stomatal terminal division,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 36, pp. 18126–18131, 2019.
@article{8625700,
  abstract     = {The R2R3-MYB transcription factor FOUR LIPS (FLP) controls the stomatal terminal division through transcriptional repression of the cell cycle genes CYCLIN-DEPENDENT KINASE (CDK) B1s (CDKB1s), CDKA; 1, and CYCLIN A2s (CYCA2s). We mutagenized the weak mutant allele flp-1 seeds with ethylmethane sulfonate and screened out a flp-1 suppressor 1 (fsp1) that suppressed the flp-1 stomatal cluster phenotype. FSP1 encodes RPA2a subunit of Replication Protein A (RPA) complexes that play important roles in DNA replication, recombination, and repair. Here, we show that FSP1/RPA2a functions together with CDKB1s and CYCA2s in restricting stomatal precursor proliferation, ensuring the stomatal terminal division and maintaining a normal guard-cell size and DNA content. Furthermore, we provide direct evidence for the existence of an evolutionarily conserved, but plant-specific, CDK-mediated RPA regulatory pathway. Serine-11 and Serine-21 at the N terminus of RPA2a are CDK phosphorylation target residues. The expression of the phosphorylation-mimic variant RPA2a(S11,21/D) partially complemented the defective cell division and DNA damage hypersensitivity in cdkb1;1 1;2 mutants. Thus, our study provides a mechanistic understanding of the CDK-mediated phosphorylation of RPA in the precise control of cell cycle and DNA repair in plants.},
  author       = {Yang, Kezhen and Zhu, Lingling and Wang, Hongzhe and Jiang, Min and Xiao, Chunwang and Hu, Xiangyang and Vanneste, Steffen and Dong, Juan and Le, Jie},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keywords     = {stomatal development,cell division,replication protein A,CDK,DNA damage,CYCLIN-DEPENDENT KINASE,RPA PHOSPHORYLATION,CELL-PROLIFERATION,DAMAGE RESPONSE,4 LIPS,SUBUNIT,BINDING,REPAIR,CDC2,MUTATIONS},
  language     = {eng},
  number       = {36},
  pages        = {18126--18131},
  title        = {A conserved but plant-specific CDK-mediated regulation of DNA replication protein A2 in the precise control of stomatal terminal division},
  url          = {http://dx.doi.org/10.1073/pnas.1819345116},
  volume       = {116},
  year         = {2019},
}

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