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Edited by David C. Baulcombe, University of Cambridge, Cambridge, United Kingdom, and approved July 29, 2019 (received for review November 11, 2018)
Significance
The Arabidopsis R2R3-MYB transcription factor FOUR LIPS (FLP) is the first identified key transcription factor regulating stomatal development. By screening and analyzing a genetic suppressor of flp stomatal defects, we found that FSP1/RPA2a, which encodes a core subunit of Replication Protein A (RPA) complexes, acts downstream of B1-type Cyclin-Dependent Kinases (CDKB1s). This ensures that terminal division during stomatal development will produce a pair of kidney-shaped guard cells to compose a functional stomatal complex. We demonstrate that the CDK-mediated phosphorylation at the N terminus of RPA2a is essential for the RPA functions in cell cycle control and response to DNA damage. We provide direct evidence for the existence of an evolutionarily conserved, but plant-specific, RPA regulatory pathway in plants.
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 RPA2aS11,21/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.
Footnotes
- ↵1To whom correspondence may be addressed. Email: lejie{at}ibcas.ac.cn.
Author contributions: K.Y., X.H., and J.L. designed research; K.Y., L.Z., and H.W. performed research; K.Y., L.Z., H.W., and M.J. analyzed data; and K.Y., C.X., X.H., S.V., J.D., and J.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1819345116/-/DCSupplemental.
Published under the PNAS license.
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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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