Meiosis is a specialized cell division that halves the number of chromosomes in two consecutive rounds of chromosome segregation. In angiosperm plants is meiosis followed by mitotic divisions to form rudimentary haploid gametophytes. In Arabidopsis, termination of meiosis and transition to gametophytic development are governed by TDM1 and SMG7 that mediate inhibition of translation. Mutants deficient in this mechanism do not form tetrads but instead undergo multiple cycles of aberrant nuclear divisions that are likely caused by the failure to downregulate cyclin dependent kinases during meiotic exit. A suppressor screen to identify genes that contribute to meiotic exit uncovered a mutation in cyclin-dependent kinase D;3 (CDKD;3) that alleviates meiotic defects in smg7 deficient plants. The CDKD;3 deficiency prevents aberrant meiotic divisions observed in smg7 mutants or delays their onset after initiation of cytokinesis, which permits formation of functional microspores. Although CDKD;3 acts as an activator of cyclin-dependent kinase A;1 (CDKA;1), the main cyclin dependent kinase that regulates meiosis, cdkd;3 mutation appears to promote meiotic exit independently of CDKA;1. Furthermore, analysis of CDKD;3 interactome revealed enrichment for proteins implicated in cytokinesis, suggesting a more complex function of CDKD;3 in cell cycle regulation.

Central European Institute of Technology Masaryk University Brno Czech Republic

Department of Developmental Biology University of Hamburg Hamburg Germany

Gregor Mendel Institute Austrian Academy of Sciences Vienna Austria

National Centre for Biomolecular Research Faculty of Science Masaryk University Brno Czech Republic

Zobrazit více v PubMed

Ahn, H. K. , Kang, Y. W. , Lim, H. M. , Hwang, I. , & Pai, H. S. (2015). Physiological functions of the COPI complex in higher plants. Molecules and Cells, 38, 866–875. PubMed PMC

Alexander, M. P. (1969). Differential staining of aborted and nonaborted pollen. Stain Technology, 44, 117–122. PubMed

Azumi, Y. , Liu, D. , Zhao, D. , Li, W. , Wang, G. , Hu, Y. , & Ma, H. (2002). Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin‐like protein. The EMBO Journal, 21, 3081–3095. PubMed PMC

Benjamini, Y. , & Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics, 29, 1165–1188. 10.1214/aos/1013699998 DOI

Bulankova, P. , Akimcheva, S. , Fellner, N. , & Riha, K. (2013). Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes. PLoS Genetics, 9, e1003508. PubMed PMC

Bulankova, P. , Riehs‐Kearnan, N. , Nowack, M. K. , Schnittger, A. , & Riha, K. (2010). Meiotic progression in Arabidopsis is governed by complex regulatory interactions between SMG7, TDM1, and the meiosis I‐specific cyclin TAM. Plant Cell, 22, 3791–3803. 10.1105/tpc.110.078378 PubMed DOI PMC

Cairo, A. , Vargova, A. , Shukla, N. , Capitao, C. , Mikulkova, P. , Valuchova, S. , Pecinkova, J. , Bulankova, P. , & Riha, K. (2022). Meiotic exit in Arabidopsis is driven by P‐body‐mediated inhibition of translation. Science, 377, 629–634. PubMed

Calixto, C. P. G. , Guo, W. , James, A. B. , Tzioutziou, N. A. , Entizne, J. C. , Panter, P. E. , Knight, H. , Nimmo, H. G. , Zhang, R. , & Brown, J. W. S. (2018). Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome. Plant Cell, 30, 1424–1444. PubMed PMC

Capitao, C. , Tanasa, S. , Fulnecek, J. , Raxwal, V. K. , Akimcheva, S. , Bulankova, P. , Mikulkova, P. , Crhak Khaitova, L. , Kalidass, M. , Lermontova, I. , Mittelsten Scheid, O. , & Riha, K. (2021). A CENH3 mutation promotes meiotic exit and restores fertility in SMG7‐deficient Arabidopsis. PLoS Genetics, 17, e1009779. PubMed PMC

Chen, X. Y. , Liu, L. , Lee, E. , Han, X. , Rim, Y. , Chu, H. , Kim, S. W. , Sack, F. , & Kim, J. Y. (2009). The Arabidopsis callose synthase gene GSL8 is required for cytokinesis and cell patterning. Plant Physiology, 150, 105–113. PubMed PMC

Chu, T. , Henrion, G. , Haegeli, V. , & Strickland, S. (2001). Cortex, a Drosophila gene required to complete oocyte meiosis, is a member of the Cdc20/fizzy protein family. Genesis, 29, 141–152. PubMed

Cromer, L. , Heyman, J. , Touati, S. , Harashima, H. , Araou, E. , Girard, C. , Horlow, C. , Wassmann, K. , Schnittger, A. , De Veylder, L. , & Mercier, R. (2012). OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLoS Genetics, 8, e1002865. PubMed PMC

De Storme, N. , & Geelen, D. (2013). Cytokinesis in plant male meiosis. Plant Signaling & Behavior, 8, e23394. PubMed PMC

Dissmeyer, N. , Nowack, M. K. , Pusch, S. , Stals, H. , Inze, D. , Grini, P. E. , & Schnittger, A. (2007). T‐loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. Plant Cell, 19, 972–985. PubMed PMC

Dissmeyer, N. , Weimer, A. K. , Pusch, S. , De Schutter, K. , Kamei, C. L. , Nowack, M. K. , Novak, B. , Duan, G. L. , Zhu, Y. G. , De Veylder, L. , & Schnittger, A. (2009). Control of cell proliferation, organ growth, and DNA damage response operate independently of dephosphorylation of the Arabidopsis Cdk1 homolog CDKA;1. Plant Cell, 21, 3641–3654. PubMed PMC

Fisher, R. P. (2019). Cdk7: A kinase at the core of transcription and in the crosshairs of cancer drug discovery. Transcription, 10, 47–56. PubMed PMC

Fourest‐Lieuvin, A. , Peris, L. , Gache, V. , Garcia‐Saez, I. , Juillan‐Binard, C. , Lantez, V. , & Job, D. (2006). Microtubule regulation in mitosis: Tubulin phosphorylation by the cyclin‐dependent kinase Cdk1. Molecular Biology of the Cell, 17, 1041–1050. PubMed PMC

Francis, K. E. , Lam, S. Y. , & Copenhaver, G. P. (2006). Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiology, 142, 1004–1013. PubMed PMC

Gloggnitzer, J. , Akimcheva, S. , Srinivasan, A. , Kusenda, B. , Riehs, N. , Stampfl, H. , Bautor, J. , Dekrout, B. , Jonak, C. , Jimenez‐Gomez, J. M. , Parker, J. E. , & Riha, K. (2014). Nonsense‐mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host & Microbe, 16, 376–390. PubMed

Hajheidari, M. , Farrona, S. , Huettel, B. , Koncz, Z. , & Koncz, C. (2012). CDKF;1 and CDKD protein kinases regulate phosphorylation of serine residues in the C‐terminal domain of Arabidopsis RNA polymerase II. Plant Cell, 24, 1626–1642. PubMed PMC

Harashima, H. , Shinmyo, A. , & Sekine, M. (2007). Phosphorylation of threonine 161 in plant cyclin‐dependent kinase A is required for cell division by activation of its associated kinase. The Plant Journal, 52, 435–448. PubMed

Izawa, D. , Goto, M. , Yamashita, A. , Yamano, H. , & Yamamoto, M. (2005). Fission yeast Mes1p ensures the onset of meiosis II by blocking degradation of cyclin Cdc13p. Nature, 434, 529–533. PubMed

Javorka, P. , Raxwal, V. K. , Najvarek, J. , & Riha, K. (2019). artMAP: A user‐friendly tool for mapping ethyl methanesulfonate‐induced mutations in Arabidopsis. Plant Direct, 3, e00146. PubMed PMC

Joubes, J. , Chevalier, C. , Dudits, D. , Heberle‐Bors, E. , Inze, D. , Umeda, M. , & Renaudin, J. P. (2000). CDK‐related protein kinases in plants. Plant Molecular Biology, 43, 607–620. PubMed

Lopez‐Aviles, S. , Kapuy, O. , Novak, B. , & Uhlmann, F. (2009). Irreversibility of mitotic exit is the consequence of systems‐level feedback. Nature, 459, 592–595. PubMed PMC

Nakagawa, T. , Suzuki, T. , Murata, S. , Nakamura, S. , Hino, T. , Maeo, K. , Tabata, R. , Kawai, T. , Tanaka, K. , Niwa, Y. , Watanabe, Y. , Nakamura, K. , Kimura, T. , & Ishiguro, S. (2007). Improved gateway binary vectors: High‐performance vectors for creation of fusion constructs in transgenic analysis of plants. Bioscience, Biotechnology, and Biochemistry, 71(2095–2), 100. PubMed

Paez Valencia, J. , Goodman, K. , & Otegui, M. S. (2016). Endocytosis and endosomal trafficking in plants. Annual Review of Plant Biology, 67, 309–335. PubMed

Page, A. W. , & Orr‐Weaver, T. L. (1996). The Drosophila genes grauzone and cortex are necessary for proper female meiosis. Journal of Cell Science, 109(Pt 7), 1707–1715. PubMed

Parry, D. H. , & O'Farrell, P. H. (2001). The schedule of destruction of three mitotic cyclins can dictate the timing of events during exit from mitosis. Current Biology, 11, 671–683. PubMed PMC

Patro, R. , Duggal, G. , Love, M. I. , Irizarry, R. A. , & Kingsford, C. (2017). Salmon provides fast and bias‐aware quantification of transcript expression. Nature Methods, 14, 417–419. PubMed PMC

Potapova, T. A. , Daum, J. R. , Pittman, B. D. , Hudson, J. R. , Jones, T. N. , Satinover, D. L. , Stukenberg, P. T. , & Gorbsky, G. J. (2006). The reversibility of mitotic exit in vertebrate cells. Nature, 440, 954–958. PubMed PMC

Prusicki, M. A. , Keizer, E. M. , van Rosmalen, R. P. , Komaki, S. , Seifert, F. , Muller, K. , Wijnker, E. , Fleck, C. , & Schnittger, A. (2019). Live cell imaging of meiosis in Arabidopsis thaliana . eLife, 8, e42834. 10.7554/eLife.42834 PubMed DOI PMC

Riehs, N. , Akimcheva, S. , Puizina, J. , Bulankova, P. , Idol, R. A. , Siroky, J. , Schleiffer, A. , Schweizer, D. , Shippen, D. E. , & Riha, K. (2008). Arabidopsis SMG7 protein is required for exit from meiosis. Journal of Cell Science, 121, 2208–2216. 10.1242/jcs.027862 PubMed DOI

Riehs‐Kearnan, N. , Gloggnitzer, J. , Dekrout, B. , Jonak, C. , & Riha, K. (2012). Aberrant growth and lethality of Arabidopsis deficient in nonsense‐mediated RNA decay factors is caused by autoimmune‐like response. Nucleic Acids Research, 40, 5615–5624. PubMed PMC

Romeiro Motta, M. , Zhao, X. , Pastuglia, M. , Belcram, K. , Roodbarkelari, F. , Komaki, M. , Harashima, H. , Komaki, S. , Kumar, M. , Bulankova, P. , Heese, M. , Riha, K. , Bouchez, D. , & Schnittger, A. (2022). B1‐type cyclins control microtubule organization during cell division in Arabidopsis . EMBO Reports, 23, e53995. PubMed PMC

Sasabe, M. , Boudolf, V. , De Veylder, L. , Inze, D. , Genschik, P. , & Machida, Y. (2011). Phosphorylation of a mitotic kinesin‐like protein and a MAPKKK by cyclin‐dependent kinases (CDKs) is involved in the transition to cytokinesis in plants. Proceedings of the National Academy of Sciences of the United States of America, 108, 844–849. PubMed PMC

Schindelin, J. , Arganda‐Carreras, I. , Frise, E. , Kaynig, V. , Longair, M. , Pietzsch, T. , Preibisch, S. , Rueden, C. , Saalfeld, S. , Schmid, B. , Tinevez, J. Y. , White, D. J. , Hartenstein, V. , Eliceiri, K. , Tomancak, P. , & Cardona, A. (2012). Fiji: An open‐source platform for biological‐image analysis. Nature Methods, 9, 676–682. PubMed PMC

Sherman, B. T. , Hao, M. , Qiu, J. , Jiao, X. , Baseler, M. W. , Lane, H. C. , Imamichi, T. , & Chang, W. (2022). DAVID: A web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Research, 50, W216–W221. 10.1093/nar/gkac194 PubMed DOI PMC

Shimotohno, A. , Aki, S. S. , Takahashi, N. , & Umeda, M. (2021). Regulation of the plant cell cycle in response to hormones and the environment. Annual Review of Plant Biology, 72, 273–296. PubMed

Shimotohno, A. , Matsubayashi, S. , Yamaguchi, M. , Uchimiya, H. , & Umeda, M. (2003). Differential phosphorylation activities of CDK‐activating kinases in Arabidopsis thaliana . FEBS Letters, 534, 69–74. PubMed

Shimotohno, A. , Ohno, R. , Bisova, K. , Sakaguchi, N. , Huang, J. , Koncz, C. , Uchimiya, H. , & Umeda, M. (2006). Diverse phosphoregulatory mechanisms controlling cyclin‐dependent kinase‐activating kinases in Arabidopsis. The Plant Journal, 47, 701–710. PubMed

Sofroni, K. , Takatsuka, H. , Yang, C. , Dissmeyer, N. , Komaki, S. , Hamamura, Y. , Bottger, L. , Umeda, M. , & Schnittger, A. (2020). CDKD‐dependent activation of CDKA;1 controls microtubule dynamics and cytokinesis during meiosis. The Journal of Cell Biology, 219, e201907016. 10.1083/jcb.201907016 PubMed DOI PMC

Takatsuka, H. , Umeda‐Hara, C. , & Umeda, M. (2015). Cyclin‐dependent kinase‐activating kinases CDKD;1 and CDKD;3 are essential for preserving mitotic activity in Arabidopsis thaliana . The Plant Journal, 82, 1004–1017. PubMed

Umeda, M. , Shimotohno, A. , & Yamaguchi, M. (2005). Control of cell division and transcription by cyclin‐dependent kinase‐activating kinases in plants. Plant & Cell Physiology, 46, 1437–1442. 10.1093/pcp/pci170 PubMed DOI

Valuchova, S. , Mikulkova, P. , Pecinkova, J. , Klimova, J. , Krumnikl, M. , Bainar, P. , Heckmann, S. , Tomancak, P. , & Riha, K. (2020). Imaging plant germline differentiation within Arabidopsis flowers by light sheet microscopy. eLife, 9, e52546. 10.7554/eLife.52546 PubMed DOI PMC

Vandepoele, K. , Raes, J. , De Veylder, L. , Rouze, P. , Rombauts, S. , & Inze, D. (2002). Genome‐wide analysis of core cell cycle genes in Arabidopsis. Plant Cell, 14, 903–916. PubMed PMC

Wang, F. , Zhang, R. , Feng, W. , Tsuchiya, D. , Ballew, O. , Li, J. , Denic, V. , & Lacefield, S. (2020). Autophagy of an amyloid‐like translational repressor regulates meiotic exit. Developmental Cell, 52(141–151), e145. PubMed PMC

Wang, G. , Kong, H. , Sun, Y. , Zhang, X. , Zhang, W. , Altman, N. , DePamphilis, C. W. , & Ma, H. (2004). Genome‐wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin‐like proteins. Plant Physiology, 135, 1084–1099. PubMed PMC

Wang, Y. , Magnard, J. L. , McCormick, S. , & Yang, M. (2004). Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A‐type cyclin predominately expressed in prophase I. Plant Physiology, 136, 4127–4135. PubMed PMC

Wijnker, E. , Harashima, H. , Muller, K. , Parra‐Nunez, P. , de Snoo, C. B. , van de Belt, J. , Dissmeyer, N. , Bayer, M. , Pradillo, M. , & Schnittger, A. (2019). The Cdk1/Cdk2 homolog CDKA;1 controls the recombination landscape in Arabidopsis . Proceedings of the National Academy of Sciences of the United States of America, 116, 12534–12539. 10.1073/pnas.1820753116 PubMed DOI PMC

Yamaguchi, M. , Umeda, M. , & Uchimiya, H. (1998). A rice homolog of Cdk7/MO15 phosphorylates both cyclin‐dependent protein kinases and the carboxy‐terminal domain of RNA polymerase II. The Plant Journal, 16, 613–619. PubMed

Yang, C. , Sofroni, K. , Wijnker, E. , Hamamura, Y. , Carstens, L. , Harashima, H. , Stolze, S. C. , Vezon, D. , Chelysheva, L. , Orban‐Nemeth, Z. , Pochon, G. , Nakagami, H. , Schlogelhofer, P. , Grelon, M. , & Schnittger, A. (2020). The Arabidopsis Cdk1/Cdk2 homolog CDKA;1 controls chromosome axis assembly during plant meiosis. The EMBO Journal, 39, e101625. PubMed PMC

Zhang, R. , Calixto, C. P. G. , Marquez, Y. , Venhuizen, P. , Tzioutziou, N. A. , Guo, W. , Spensley, M. , Entizne, J. C. , Lewandowska, D. , Have, S. T. , Frey, N. F. , Hirt, H. , James, A. B. , Nimmo, H. G. , Barta, A. , Kalyna, M. , & Brown, J. W. S. (2017). A high quality Arabidopsis transcriptome for accurate transcript‐level analysis of alternative splicing. Nucleic Acids Research, 45, 5061–5073. 10.1093/nar/gkx267 PubMed DOI PMC

Carboxy-terminal polyglutamylation regulates signaling and phase separation of the Dishevelled protein