The Cyclin CYCA3;4 Is a Postprophase Target of the APC/C^CCS52A2 E3-Ligase Controlling Formative Cell Divisions in Arabidopsis

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/C CCS52A2 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/C CCS52A2 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.

The Arabidopsis GRAS-type SCL28 transcription factor controls the mitotic cell cycle and division plane orientation

“…CYCAs of the subgroups 1 and 2 were also enriched in G2/M cells, including CYCA2;4, which was not detected previously in CSCs. By contrast, two CYCAs of subgroup 3, CYCA3;1 and CYCA3;2, were depleted in G2/M cells, whereas CYCA3;4 showed no significant enrichment in G2/M cells, confirming recent data (36). CYCA3;3 was not detected, as expected for a meiosis-specific cyclin gene (33).…”

Leaf Size Development Differences and Comparative Transcriptome Analyses of Two Poplar Genotypes

“…For example, triploid poplar can promote the leaf size by affecting the expression of growth hormone, transcription factors and cell differentiation-related genes [38,39]. The complexity of anaphase promoting complex (APC) and the cell cycle switch (CCS52B) can selectively degrade regulatory protein factors that limit cell division, thus regulating the cell cycle [40,41]. We have identified that the Arabidopsis PCNA2 homologous gene is highly expressed in Pd, which can form a complex PCNA/CycD with D-cyclin to regulate the cell cycle [42].…”

Plant CDKs—Driving the Cell Cycle through Climate Change

“…SAMBA is an APC/C negative regulator that also interacts with A-type cyclins (CYCA2;2 and CYCA2;3, weakly with CYCA1;1) and promoted plant growth when mutated [ 89 ]. CYCA3;4 is targeted for proteasomal degradation by APC/C CCS52A2 , and plants with increased CYCA3;4 levels showed disorganized formative divisions, with defects in root meristem and leaf cell differentiation [ 90 ].…”