ANAPHASE-PROMOTING COMPLEX/CYCLOSOME coactivators maintain AURORA1 kinase homeostasis during meiotic chromosome segregation

Abstract Faithful chromosome segregation is essential for both mitotic and meiotic cell division. The Anaphase Promoting Complex/Cyclosome (APC/C) and its coactivators are required for meiotic chromosome segregation, but their potential targets and regulatory mechanisms remain unclear in plants. Here, we performed a ubiquitinome analysis and show that Arabidopsis thaliana Aurora 1 (AUR1) is over-ubiquitinated at lysine 102 in the coactivator Cell Division Cycle 20.1 (cdc20.1) mutants and that AUR1 overexpression can partially rescue the cdc20.1 meiotic defect. We also demonstrate that APC/C ubiquitinates AUR1, leading to its degradation through the 26S proteasome pathway. Moreover, the APC/C subunit and coactivators Cell Cycle Switch 52 A2/B (CCS52A2/B) and CDC20.1 interact with AUR1 both in vitro and in vivo. Intriguingly, CCS52A2/B promotes AUR1 ubiquitination and degradation, while CDC20.1 prevents AUR1 degradation. Consistent with this finding, AUR1 levels are lower in cdc20.1 and higher in ccs52 mutants relative to Col-0, and mutation of CCS52A2/B causes defects in meiotic spindle assembly and homologous chromosome segregation. Genetic analyses demonstrate that Arabidopsis Anaphase-Promoting Complex/Cyclosome subunit 8 (APC8), CDC20.1, CCS52 and AUR1 act in the same pathway to control meiotic spindle assembly and homologous chromosome segregation. Thus, this work provides mechanistic insight into the role of APC/C coactivators in regulating AUR1 homeostasis during meiosis in plants.