Cell Cycle Control by Nuclear Sequestration of CDC20 and CDH1 mRNA in Plant Stem Cells
Abstract
In eukaryotes, most RNA molecules are exported into the cytoplasm after transcription. Long noncoding RNAs (lncRNAs) reside and function primarily inside the nucleus, but nuclear localization of mRNAs has been considered rare in both animals and plants. Here we show that Arabidopsis anaphase-promoting complex/cyclosome (APC/C) coactivator genes CDC20 and CCS52B (CDH1 ortholog) are co-expressed with their target cyclin B genes (CYCBs) during mitosis. CYCB transcripts can be exported and translated; however, CDC20 and CCS52B mRNAs are 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) plays dual roles in CDC20 mRNA nuclear localization and translation. Mitotic accumulation of CDC20 and CCS52B transcripts enables the timely and rapid activation of APC/C, while the nuclear sequestration of these transcripts at prophase appears to protect cyclins from precocious degradation.
Additional Information
© 2017 Elsevier Inc. Received 24 February 2017, Revised 21 September 2017, Accepted 7 November 2017, Available online 7 December 2017. Published: December 7, 2017. We would like to thank Jonathon Pines (The Institute of Cancer Research, London), David Ron (Cambridge Institute for Medical Research, University of Cambridge), Yrjö Helariutta and Henrik Jönsson (The Sainsbury Laboratory at Cambridge University), and Olivier Hamant (Plant Reproduction and Development Laboratory, INRA, ENS Lyon) for advice and insightful discussions. We also thank David E. Evans (Oxford Brookes University), Susan Armstrong (University of Birmingham), and Xinnian Dong (Duke University) for sharing seeds. We are grateful to Christoph Schuster for support with in situ hybridization; Benoit Landrein for suggestions for confocal microscope analysis; Pawel Roszak for help with root sectioning; and Alexis Peaucelle, Charles Melnyk, Paul Tarr, Pau Formosa Jordan, and all members of the Meyerowitz Lab at the California Institute of Technology for helpful conversations. We appreciate Barbara Di Fiore and Anja Hagting (The Gurdon Institute, University of Cambridge), and Lisa Willis (The Sainsbury Laboratory at Cambridge University) for comments and careful reading of the manuscript. This work was funded by the Gatsby Charitable Foundation (through fellowship GAT3395/DAA). E.M.M. is supported by the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through grant GBMF3406). R.W. and W.Y. are supported by the Leverhulme Trust (grant RPG-2015-285). Author Contributions: W.Y. and R.W. conceived the project; W.Y. and R.W. designed and performed the experiments; W.Y., R.W., and E.M.M. analyzed and interpreted the data; W.Y., R.W., and E.M.M. wrote the manuscript.Attached Files
Submitted - 198978.full.pdf
Supplemental Material - mmc1.pdf
Supplemental Material - mmc2.xlsx
Supplemental Material - mmc3.xlsx
Supplemental Material - mmc4.xlsx
Files
| Name | Size | Download all |
|---|---|---|
|
md5:753bf0777bcc9e8a3fcded82209888c0
|
1.7 MB | Preview Download |
|
md5:0fc83f62f310d03f86b821e1fcb2a02b
|
28.3 kB | Download |
|
md5:482137c17611dd7826fe527ef299bae2
|
17.0 kB | Download |
|
md5:c575caf132822d2b3e3532b5ed66af59
|
16.5 MB | Download |
|
md5:bfd3b60f57a959aa6d6bb31fca3ad2e9
|
3.3 MB | Preview Download |
Additional details
- PMCID
- PMC6013263
- Eprint ID
- 83755
- Resolver ID
- CaltechAUTHORS:20171208-113651906
- Gatsby Charitable Foundation
- GAT3395/DAA
- Howard Hughes Medical Institute (HHMI)
- Gordon and Betty Moore Foundation
- GBMF3406
- Leverhulme Trust
- RPG-2015-285
- Created
-
2017-12-13Created from EPrint's datestamp field
- Updated
-
2022-03-18Created from EPrint's last_modified field