Delineating the crossover control networks in plants
Final Report Abstract
The collaborative ERA-CAPS DeCOP (Delineating the crossover control networks in plants) project has been a joint effort by six European research groups. It focused on how meiotic recombination, chromosome organisation and remodelling are orchestrated to control the frequency and distribution of exchange of genetic information during meiosis in plants. Meiosis is a specialized type of cell division required for sexual reproduction. It ensures the reduction of the genome and the recombination of maternal and paternal chromosomal segments prior to the formation of generative cells. The process of meiotic recombination is initiated by programmed DNA double-strand breaks (DSBs). Ultimately, the positions of the DSBs define loci of mutual genetic exchange. However, in a single meiotic cell only a small subset of DSBs are destined to form genetic crossovers (COs), while the remainder are repaired via non-CO pathways. In this collaborative project we 1) identified novel factors that modulate CO formation and interference, 2) investigated the role of chromosome axis-associated proteins in CO maturation and interference, 3) determined the role of (ATM/ATR/CK2 mediated) phosphorylation in coordinating DNA repair and 4) identified proteins involved in the final step of meiotic CO formation. Some of the research work has already been published some other aspects are still under investigations. We especially highlight the findings that the protein ASY4 has been identified as a novel meiotic axis protein, that PCH2 has been identified and described as a meiotic axis re-modelling factor in plants, that cross-linking mass spectrometry techniques have been established and employed to characterize a meiotic protein complex, that novel phosphorylation sites on meiotic axis proteins have been identified, that in-depth phospho-proteomic studies established the kinase CK2 as a key mediator of DNA damage response, that local zygosity modulates meiotic interference, that HEI10 dosage positively correlates with CO frequency, that DNA methylation and nucleosome density, identity and modifications define meiotic DSB and hence CO frequency and that AtRMI2 and AtRTEL1 are needed for 45S rDNA stability. In summary, this European research consortium contributed considerably to the understanding of meiotic DSB formation, recombination and cross-over formation in plants. The coordination of research avoided competition and redundancy and, importantly, the regular exchange of ideas, knowhow and research materials and the regular meetings of involved researches stimulated new research directions and collaborations.
Publications
- 2014. The condensin complexes play distinct roles to ensure normal chromosome morphogenesis duirng meiotic división in Arabidopsis. The Plant Journal
Smith SJ, Osman K, Franklin FCH
(See online at https://doi.org/10.1111/tpj.12628) - (2015) Juxtaposition of heterozygous and homozygous regions causes reciprocal crossover remodelling via interference during Arabidopsis meiosis. Elife.;4
Ziolkowski PA, Berchowitz LE, Lambing C, Yelina NE, Zhao X, Kelly KA, Choi K, Ziolkowska L, June V, Sanchez-Moran E, Franklin FC, Copenhaver GP, Henderson IR
(See online at https://doi.org/10.7554/eLife.03708) - 2015. Arabidopsis PCH2 Mediates Meiotic Chromosome Remodeling and Maturation of Crossovers. PloS Genetics 11(7): e1005372
Lambing C, Osman K, Nuntasoontorn K, West A, Higgins JD, Copenhaver GP, Yang J,1, Armstrong SJ, Mechtler K, Roitinger E, Franklin FCH
(See online at https://doi.org/10.1371/journal.pgen.1005372) - Comprehensive Cross-Linking Mass Spectrometry Reveals Parallel Orientation and Flexible Conformations of Plant HOP2-MND1. J Proteome Res. 2015 Dec 4;14(12):5048-62
Rampler E, Stranzl T, Orban-Nemeth Z, Hollenstein DM, Hudecz O, Schloegelhofer P, Mechtler K
(See online at https://doi.org/10.1021/acs.jproteome.5b00903) - DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis. Genes Dev. 2015 Oct 15;29(20):2183-202
Yelina NE, Lambing C, Hardcastle TJ, Zhao X, Santos B, Henderson IR
(See online at https://doi.org/10.1101/gad.270876.115) - Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol Cell Proteomics. 2015 Mar;14(3):556-71
Roitinger E, Hofer M, Köcher T, Pichler P, Novatchkova M, Yang J, Schlögelhofer P, Mechtler K
(See online at https://doi.org/10.1074/mcp.M114.040352) - (2016) The RTR Complex Partner RMI2 and the DNA Helicase RTEL1 Are Both Independently Involved in Preserving the Stability of 45S rDNA Repeats in Arabidopsis thaliana. PLoS Genet 12(10): e1006394
Röhrig S, Schröpfer S, Knoll A, Puchta H
(See online at https://doi.org/10.1371/journal.pgen.1006394) - (2017) Natural variation and dosage of the HEI10 meiotic E3 ligase control Arabidopsis crossover recombination. Genes Dev. 31(3):306-317
Ziolkowski PA, Underwood CJ, Lambing C, Martinez- Garcia M, Lawrence EJ, Ziolkowska L, Griffin C, Choi K, Franklin FC, Martienssen RA, Henderson IR
(See online at https://doi.org/10.1101/gad.295501.116) - (2017) Understanding and Manipulating Meiotic Recombination in Plants. Plant Physiol. 173(3):1530-1542
Lambing C, Franklin FC, Wang CR
(See online at https://doi.org/10.1104/pp.16.01530) - Affinity proteomics reveals extensive phosphorylation of the Brassica chromosome axis protein ASY1 and a network of associated proteins at prophase I of meiosis. Plant J. 2018 Jan;93(1):17-33
Osman K, Yang J, Roitinger E, Lambing C, Heckmann S, Howell E, Cuacos M, Imre R, Dürnberger G, Mechtler K, Armstrong S, Franklin FCH
(See online at https://doi.org/10.1111/tpj.13752) - Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation. Genome Res 2018
Underwood CJ, Choi K, Lambing C, Zhao X, Serra H, Borges F, Simorowski J, Ernst E, Jacob Y, Henderson IR and Martienssen RA
(See online at https://doi.org/10.1101/gr.227116.117) - Identification of ASYNAPTIC4, a component of the meiotic chromosome axis. Plant Physiol. 2018 Jul 12
Chambon A, West A, Vezon D, Horlow C, De Muyt A, Chelysheva L, Ronceret A, Darbyshire AR, Osman K, Heckmann S, Franklin FCH and Grelon M
(See online at https://doi.org/10.1104/pp.17.01725) - Massive crossover elevation via combination of HEI10 and recq4a recq4b during Arabidopsis meiosis. PNAS 2018. 115: 2437-2442
Serra H, Lambing C, Griffin CH, Topp SD, Nageswaran DC, Underwood CJ, Ziolkowski PA, Seguela-Arnaud M, Fernandes JB, Mercier R and Henderson IR
(See online at https://doi.org/10.1073/pnas.1713071115) - Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions. Genome Research 2018
Choi K, Zhao X, Tock AJ, Lambing C, Underwood CJ, Hardcastle TJ, Serra H, Kim J, Cho HS, Kim J, Ziolkowski PA, Yelina NE, Hwang I, Martienssen RA and Henderson IR
(See online at https://doi.org/10.1101/gr.225599.117)
