Baixiao Niu

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.

Seed dormancy, an essential trait for plant adaptation, is determined by the embryo itself and the surrounding tissues. Here, we found that rice (Oryza sativa) FERTILIZATION INDEPENDENT ENDOSPERM1 (OsFIE1) regulates endosperm-imposed dormancy and the dorsal aleurone thickness in a manner dependent on the parent of origin. Maternally expressed OsFIE1 suppresses gibberellin (GA) biosynthesis in the endosperm by depositing trimethylation of lysine 27 on histone H3 (H3K27me3) marks on GA biosynthesis-related genes, thus inhibiting germination and aleurone differentiation. Knockout of rice GA 20-oxidase1 (OsGA20ox1) alleviated the phenotypic defects in osfie1. The aleurone-positive determinant Crinkly 4 (OsCR4) is another target of the OsFIE1-containing Polycomb repressive complex 2 (PRC2). We found that OsFIE1 plays an important role in genomic imprinting in the endosperm of germinating seeds, particularly for paternally expressed genes associated with H3K27me3. The increased aleurone thickness of osfie1 substantially improved grain nutritional quality, indicating that the osfie1 gene may be utilized for breeding nutrient-enriched rice. The findings provide insights into the essential roles of PRC2-mediated H3K27me3 methylation in the acquisition of seed dormancy and endosperm cell differentiation in rice.