Cell Cycle Control by Nuclear Sequestration of CDC20 and CDH1 mRNA in Plant Stem Cells

Abstract

In eukaryotic cells, most RNA molecules are exported into the cytoplasm after being transcribed in the nucleus. Long noncoding RNAs (lncRNAs) have been found to reside and function primarily inside the nucleus, but nuclear localization of protein-coding messenger RNAs (mRNAs) has been considered rare in both animals and plants. Here we show that two mRNAs, transcribed from the CDC20 and CCS52B (plant orthologue of CDH1) genes, are specifically sequestered inside the nucleus during the cell cycle. CDC20 and CDH1 both function as coactivators of the anaphase-promoting complex or cyclosome (APC/C) E3 ligase to trigger cyclin B (C YCB) destruction. In the Arabidopsis thaliana shoot apical meristem (SAM), we find CDC20 and CCS52B are co-expressed with CYCBs in mitotic cells. CYCB transcripts can be exported and translated, whereas CDC20 and CCS52B mRNAs are strictly confined to the nucleus at prophase and the cognate proteins are not translated until the redistribution of the mRNAs to the cytoplasm after nuclear envelope breakdown (NEBD) at prometaphase. The 5' untranslated region (UTR) is necessary and sufficient for CDC20 mRNA nuclear localization as well as protein translation. Mitotic enrichment of CDC20 and CCS52B transcripts enables the timely and rapid activation of APC/C, while their nuclear sequestration at prophase appears to protect cyclins from precocious degradation.