CDKG1 Is Required for Meiotic and Somatic Recombination Intermediate Processing in Arabidopsis[CC-BY]

The cyclin-dependent kinase CDKG1 stabilizes recombination intermediates during male meiosis and DNA damage-induced somatic homologous recombination. The Arabidopsis (Arabidopsis thaliana) cyclin-dependent kinase G1 (CDKG1) is necessary for recombination and synapsis during male meiosis at high ambient temperature. In the cdkg1-1 mutant, synapsis is impaired and there is a dramatic reduction in the number of class I crossovers, resulting in univalents at metaphase I and pollen sterility. Here, we demonstrate that CDKG1 is necessary for the processing of recombination intermediates in the canonical ZMM recombination pathway and that loss of CDKG1 results in increased class II crossovers. While synapsis and events associated with class I crossovers are severely compromised in a cdkg1-1 mutant, they can be restored by increasing the number of recombination intermediates in the double cdkg1-1 fancm-1 mutant. Despite this, recombination intermediates are not correctly resolved, leading to the formation of chromosome aggregates at metaphase I. Our results show that CDKG1 acts early in the recombination process and is necessary to stabilize recombination intermediates. Finally, we show that the effect on recombination is not restricted to meiosis and that CDKG1 is also required for normal levels of DNA damage-induced homologous recombination in somatic tissues.

[1]  P. Kaldis,et al.  Diverse roles for CDK‐associated activity during spermatogenesis , 2019, FEBS letters.

[2]  A. Schnittger,et al.  The Arabidopsis Cdk1/Cdk2 homolog CDKA;1 controls chromosome axis assembly during plant meiosis , 2019, The EMBO journal.

[3]  A. Schnittger,et al.  The Cdk1/Cdk2 homolog CDKA;1 controls the recombination landscape in Arabidopsis , 2019, Proceedings of the National Academy of Sciences.

[4]  A. Lloyd,et al.  Modelling Sex-Specific Crossover Patterning in Arabidopsis , 2018, Genetics.

[5]  Luguang Jiang,et al.  The Number of Meiotic Double-Strand Breaks Influences Crossover Distribution in Arabidopsis[OPEN] , 2018, Plant Cell.

[6]  Zhukuan Cheng,et al.  HEIP1 regulates crossover formation during meiosis in rice , 2018, Proceedings of the National Academy of Sciences.

[7]  N. Christophorou,et al.  A cytological approach to studying meiotic recombination and chromosome dynamics in Arabidopsis thaliana male meiocytes in three dimensions , 2018, The Plant journal : for cell and molecular biology.

[8]  J. Doonan,et al.  The cyclin‐dependent kinase G group defines a thermo‐sensitive alternative splicing circuit modulating the expression of Arabidopsis ATU2AF65A , 2018, The Plant journal : for cell and molecular biology.

[9]  C. Kerzendorfer,et al.  Arabidopsis thaliana FANCD2 Promotes Meiotic Crossover Formation[OPEN] , 2018, Plant Cell.

[10]  I. Henderson,et al.  Massive crossover elevation via combination of HEI10 and recq4a recq4b during Arabidopsis meiosis , 2017, Proceedings of the National Academy of Sciences.

[11]  J. Doonan,et al.  The cyclin‐dependent kinase G group defines a thermo‐sensitive alternative splicing circuit modulating the expression of Arabidopsis ATU2AF65A , 2018, The Plant journal : for cell and molecular biology.

[12]  R. Guérois,et al.  FIGL1 and its novel partner FLIP form a conserved complex that regulates homologous recombination , 2017, bioRxiv.

[13]  Blanca Gómez-Escoda,et al.  Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities , 2017, Genes.

[14]  F. C. H. Franklin,et al.  Understanding and Manipulating Meiotic Recombination in Plants[OPEN] , 2017, Plant Physiology.

[15]  R. Guérois,et al.  Concerted action of the MutLβ heterodimer and Mer3 helicase regulates the global extent of meiotic gene conversion , 2017, eLife.

[16]  R. Mercier,et al.  RMI1 and TOP3α limit meiotic CO formation through their C-terminal domains , 2016, Nucleic acids research.

[17]  P. Cohen,et al.  Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation. , 2016, Annual review of genetics.

[18]  Martin A White,et al.  Quantitative Modeling and Automated Analysis of Meiotic Recombination , 2016, bioRxiv.

[19]  N. Kleckner,et al.  A few of our favorite things: Pairing, the bouquet, crossover interference and evolution of meiosis. , 2016, Seminars in cell & developmental biology.

[20]  L. Chelysheva,et al.  Correction: AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM Antagonize Meiotic Crossovers by Distinct Mechanisms , 2015, PLoS genetics.

[21]  L. Chelysheva,et al.  AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM Antagonize Meiotic Crossovers by Distinct Mechanisms , 2015, PLoS genetics.

[22]  M. Grelon,et al.  The molecular biology of meiosis in plants. , 2015, Annual review of plant biology.

[23]  Jelle Van Leene,et al.  Multiple mechanisms limit meiotic crossovers: TOP3α and two BLM homologs antagonize crossovers in parallel to FANCM , 2015, Proceedings of the National Academy of Sciences.

[24]  P. Shaw,et al.  Licensing MLH1 sites for crossover during meiosis , 2014, Nature Communications.

[25]  R. Mercier,et al.  FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers , 2014, Nucleic acids research.

[26]  H. Puchta,et al.  MHF1 plays Fanconi anaemia complementation group M protein (FANCM)-dependent and FANCM-independent roles in DNA repair and homologous recombination in plants. , 2014, The Plant journal : for cell and molecular biology.

[27]  J. Doonan,et al.  CDKG1 protein kinase is essential for synapsis and male meiosis at high ambient temperature in Arabidopsis thaliana , 2014, Proceedings of the National Academy of Sciences.

[28]  N. Kleckner,et al.  Crossover Patterning by the Beam-Film Model: Analysis and Implications , 2014, PLoS genetics.

[29]  Hong Ma,et al.  The Arabidopsis RAD51 paralogs RAD51B, RAD51D and XRCC2 play partially redundant roles in somatic DNA repair and gene regulation. , 2014, The New phytologist.

[30]  N. Manfrini,et al.  Regulation of the DNA damage response by cyclin-dependent kinases. , 2013, Journal of molecular biology.

[31]  O. Martin,et al.  Hot Regions of Noninterfering Crossovers Coexist with a Nonuniformly Interfering Pathway in Arabidopsis thaliana , 2013, Genetics.

[32]  Thomas J. Hardcastle,et al.  Nature Genetics Advance Online Publication Arabidopsis Meiotic Crossover Hot Spots Overlap with H2a.z Nucleosomes at Gene Promoters , 2022 .

[33]  Molly C. Kottemann,et al.  Fanconi anaemia and the repair of Watson and Crick DNA crosslinks , 2013, Nature.

[34]  Jun Zhu,et al.  CYCLIN-DEPENDENT KINASE G1 Is Associated with the Spliceosome to Regulate CALLOSE SYNTHASE5 Splicing and Pollen Wall Formation in Arabidopsis , 2013 .

[35]  M. Novatchkova,et al.  The Arabidopsis HEI10 Is a New ZMM Protein Related to Zip3 , 2012, PLoS genetics.

[36]  Zhukuan Cheng,et al.  The Role of Rice HEI10 in the Formation of Meiotic Crossovers , 2012, PLoS genetics.

[37]  G. Copenhaver,et al.  FANCM Limits Meiotic Crossovers , 2012, Science.

[38]  J. Higgins,et al.  The Fanconi Anemia Ortholog FANCM Ensures Ordered Homologous Recombination in Both Somatic and Meiotic Cells in Arabidopsis[W] , 2012, Plant Cell.

[39]  Alexandra M. E. Jones,et al.  The Ph1 Locus Suppresses Cdk2-Type Activity during Premeiosis and Meiosis in Wheat[W][OA] , 2012, Plant Cell.

[40]  H. Puchta,et al.  The role of DNA helicases and their interaction partners in genome stability and meiotic recombination in plants. , 2011, Journal of experimental botany.

[41]  L. Chelysheva,et al.  An Easy Protocol for Studying Chromatin and Recombination Protein Dynamics during Arabidopsisthaliana Meiosis: Immunodetection of Cohesins, Histones and MLH1 , 2010, Cytogenetic and Genome Research.

[42]  R. Waugh,et al.  Development of a Molecular Cytogenetic Recombination Assay for Barley , 2010, Cytogenetic and Genome Research.

[43]  M. Whitby The FANCM family of DNA helicases/translocases. , 2010, DNA repair.

[44]  A. Britt,et al.  Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage , 2009, Proceedings of the National Academy of Sciences.

[45]  J. Doonan,et al.  Functional Evolution of Cyclin-Dependent Kinases , 2009, Molecular biotechnology.

[46]  M. Novatchkova,et al.  SHOC1, an XPF Endonuclease-Related Protein, Is Essential for the Formation of Class I Meiotic Crossovers , 2008, Current Biology.

[47]  A. Britt,et al.  Both ATM and ATR promote the efficient and accurate processing of programmed meiotic double-strand breaks. , 2008, The Plant journal : for cell and molecular biology.

[48]  K. Cimprich,et al.  ATR: an essential regulator of genome integrity , 2008, Nature Reviews Molecular Cell Biology.

[49]  J. Higgins,et al.  AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. , 2008, The Plant journal : for cell and molecular biology.

[50]  Xiaoduo Lu,et al.  The Arabidopsis MutS homolog AtMSH5 is required for normal meiosis , 2008, Cell Research.

[51]  J. Higgins,et al.  Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. , 2008, The Plant journal : for cell and molecular biology.

[52]  H. Puchta,et al.  Two closely related RecQ helicases have antagonistic roles in homologous recombination and DNA repair in Arabidopsis thaliana , 2007, Proceedings of the National Academy of Sciences.

[53]  Luke E. Berchowitz,et al.  The Role of AtMUS81 in Interference-Insensitive Crossovers in A. thaliana , 2007, PLoS genetics.

[54]  R. Hasterok,et al.  BAC 'landing' on chromosomes of Brachypodium distachyon for comparative genome alignment , 2007, Nature Protocols.

[55]  H. Puchta,et al.  The role of AtMUS81 in DNA repair and its genetic interaction with the helicase AtRecQ4A , 2006, Nucleic acids research.

[56]  D. Zickler,et al.  From early homologue recognition to synaptonemal complex formation , 2006, Chromosoma.

[57]  E. Sanchez-Moran,et al.  Reduced meiotic crossovers and delayed prophase I progression in AtMLH3‐deficient Arabidopsis , 2006, The EMBO journal.

[58]  I. Colas,et al.  Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat , 2006, Nature.

[59]  E. Sanchez-Moran,et al.  The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. , 2005, Genes & development.

[60]  M. Doutriaux,et al.  Two Meiotic Crossover Classes Cohabit in Arabidopsis One Is Dependent on MER3,whereas the Other One Is Not , 2005, Current Biology.

[61]  J. Higgins,et al.  The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. , 2004, Genes & development.

[62]  E. Hoffmann,et al.  A role for the MutL homologue MLH2 in controlling heteroduplex formation and in regulating between two different crossover pathways in budding yeast , 2004, Cytogenetic and Genome Research.

[63]  Hong Ma,et al.  The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[64]  A. Villeneuve,et al.  A Component of C. elegans Meiotic Chromosome Axes at the Interface of Homolog Alignment, Synapsis, Nuclear Reorganization, and Recombination , 2004, Current Biology.

[65]  S. Bonhoeffer,et al.  Interchromatid and Interhomolog Recombination in Arabidopsis thaliana , 2004, The Plant Cell Online.

[66]  Jean-Yves Bleuyard,et al.  The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis , 2004, The EMBO journal.

[67]  M. Whitby,et al.  Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. , 2003, Molecular cell.

[68]  A. Villeneuve,et al.  Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. , 2003, Developmental cell.

[69]  K. McKim,et al.  Relationship of DNA double-strand breaks to synapsis in Drosophila , 2003, Journal of Cell Science.

[70]  F. Stahl,et al.  Crossover interference in humans. , 2003, American journal of human genetics.

[71]  C. Franklin Faculty Opinions recommendation of AtATM is essential for meiosis and the somatic response to DNA damage in plants. , 2003 .

[72]  F. Franklin,et al.  Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica , 2002, Journal of Cell Science.

[73]  V. Brabec DNA modifications by antitumor platinum and ruthenium compounds: their recognition and repair. , 2002, Progress in nucleic acid research and molecular biology.

[74]  T. Allers,et al.  Differential Timing and Control of Noncrossover and Crossover Recombination during Meiosis , 2001, Cell.

[75]  M. Doutriaux,et al.  Random Chromosome Segregation without Meiotic Arrest in Both Male and Female Meiocytes of a dmc1 Mutant of Arabidopsis , 1999, Plant Cell.

[76]  S. Keeney,et al.  Meiosis-Specific DNA Double-Strand Breaks Are Catalyzed by Spo11, a Member of a Widely Conserved Protein Family , 1997, Cell.

[77]  P. Sung,et al.  DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA , 1995, Cell.

[78]  N. Kleckner,et al.  DMC1: A meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression , 1992, Cell.