Browse > Article
http://dx.doi.org/10.14348/molcells.2022.2054

Fast and Precise: How to Measure Meiotic Crossovers in Arabidopsis  

Kim, Heejin (Department of Life Sciences, Pohang University of Science and Technology)
Choi, Kyuha (Department of Life Sciences, Pohang University of Science and Technology)
Publication Information
Molecules and Cells / v.45, no.5, 2022 , pp. 273-283 More about this Journal
Abstract
During meiosis, homologous chromosomes (homologs) pair and undergo genetic recombination via assembly and disassembly of the synaptonemal complex. Meiotic recombination is initiated by excess formation of DNA double-strand breaks (DSBs), among which a subset are repaired by reciprocal genetic exchange, called crossovers (COs). COs generate genetic variations across generations, profoundly affecting genetic diversity and breeding. At least one CO between homologs is essential for the first meiotic chromosome segregation, but generally only one and fewer than three inter-homolog COs occur in plants. CO frequency and distribution are biased along chromosomes, suppressed in centromeres, and controlled by pro-CO, anti-CO, and epigenetic factors. Accurate and high-throughput detection of COs is important for our understanding of CO formation and chromosome behavior. Here, we review advanced approaches that enable precise measurement of the location, frequency, and genomic landscapes of COs in plants, with a focus on Arabidopsis thaliana.
Keywords
crossover; fluorescence-tagged lines; genotyping-by-sequencing; interference; meiosis; synaptonemal complex;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Yelina, N.E., Gonzalez-Jorge, S., Hirsz, D., Yang, Z., and Henderson, I.R. (2021). CRISPR targeting of MEIOTIC-TOPOISOMERASE VIB-dCas9 to a recombination hotspot is insufficient to increase crossover frequency in Arabidopsis. BioRxiv, https://doi.org/10.1101/2021.02.01.429210   DOI
2 Yokoo, R., Zawadzki, K.A., Nabeshima, K., Drake, M., Arur, S., and Villeneuve, A.M. (2012). COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149, 75-87.   DOI
3 Zickler, D. and Kleckner, N. (1999). Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603-754.   DOI
4 Chelysheva, L., Diallo, S., Vezon, D., Gendrot, G., Vrielynck, N., Belcram, K., Rocques, N., Marquez-Lema, A., Bhatt, A.M., Horlow, C., et al. (2005). AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J. Cell Sci. 118, 4621-4632.   DOI
5 Crismani, W., Girard, C., Froger, N., Pradillo, M., Santos, J.L., Chelysheva, L., Copenhaver, G.P., Horlow, C., and Mercier, R. (2012). FANCM limits meiotic crossovers. Science 336, 1588-1590.   DOI
6 France, M.G., Enderle, J., Rohrig, S., Puchta, H., Franklin, F.C.H., and Higgins, J.D. (2021). ZYP1 is required for obligate cross-over formation and cross-over interference in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 118, e2021671118.   DOI
7 Francis, K.E., Lam, S.Y., Harrison, B.D., Bey, A.L., Berchowitz, L.E., and Copenhaver, G.P. (2007). Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 104, 3913-3918.   DOI
8 Gao, C. (2021). Genome engineering for crop improvement and future agriculture. Cell 184, 1621-1635.   DOI
9 Seguela-Arnaud, M., Choinard, S., Larcheveque, C., Girard, C., Froger, N., Crismani, W., and Mercier, R. (2017). RMI1 and TOP3α limit meiotic CO formation through their C-terminal domains. Nucleic Acids Res. 45, 1860-1871.
10 Serra, H., Lambing, C., Griffin, C.H., Topp, S.D., Nageswaran, D.C., Underwood, C.J., Ziolkowski, P.A., Seguela-Arnaud, M., Fernandes, J.B., Mercier, R., et al. (2018a). Massive crossover elevation via combination of HEI10 and recq4a recq4b during Arabidopsis meiosis. Proc. Natl. Acad. Sci. U. S. A. 115, 2437-2442.   DOI
11 Kim, J. and Choi, K. (2019). Signaling-mediated meiotic recombination in plants. Curr. Opin. Plant Biol. 51, 44-50.   DOI
12 Girard, C., Chelysheva, L., Choinard, S., Froger, N., Macaisne, N., Lehmemdi, A., Mazel, J., Crismani, W., and Mercier, R. (2015). AAA-ATPase FIDGETINLIKE 1 and helicase FANCM antagonize meiotic crossovers by distinct mechanisms. PLoS Genet. 11, e1005369.   DOI
13 Giraut, L., Falque, M., Drouaud, J., Pereira, L., Martin, O.C., and Mezard, C. (2011). Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet. 7, e1002354.   DOI
14 Hurel, A., Phillips, D., Vrielynck, N., Mezard, C., Grelon, M., and Christophorou, N. (2018). A cytological approach to studying meiotic recombination and chromosome dynamics in Arabidopsis thaliana male meiocytes in three dimensions. Plant J. 95, 385-396.   DOI
15 Kim, J., Park, J., Kim, H., Son, N., Lambing, C., Kim, E.J., Kim, J., Byun, D., Lee, Y., Park, Y.M., et al. (2021). HEAT SHOCK FACTOR BINDING PROTEIN limits meiotic crossovers by repressing HEI10 transcription. BioRxiv, https://doi.org/10.1101/2021.10.17.464477   DOI
16 Berchowitz, L.E. and Copenhaver, G.P. (2010). Genetic interference: don't stand so close to me. Curr. Genomics 11, 91-102.   DOI
17 Drouaud, J., Camilleri, C., Bourguignon, P.Y., Canaguier, A., Berard, A., Vezon, D., Giancola, S., Brunel, D., Colot, V., Prum, B., et al. (2006). Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination "hot spots". Genome Res. 16, 106-114.   DOI
18 Seguela-Arnaud, M., Crismani, W., Larcheveque, C., Mazel, J., Froger, N., Choinard, S., Lemhemdi, A., Macaisne, N., Van Leene, J., Gevaert, K., et al. (2015). Multiple mechanisms limit meiotic crossovers: TOP3α and two BLM homologs antagonize crossovers in parallel to FANCM. Proc. Natl. Acad. Sci. U. S. A. 112, 4713-4718.   DOI
19 Serra, H., Choi, K., Zhao, X., Blackwell, A.R., Kim, J., and Henderson, I.R. (2018b). Interhomolog polymorphism shapes meiotic crossover within the Arabidopsis RAC1 and RPP13 disease resistance genes. PLoS Genet. 14, e1007843.   DOI
20 Albert, P.S., Zhang, T., Semrau, K., Rouillard, J.M., Kao, Y.H., Wang, C.J.R., Danilova, T.V., Jiang, J., and Birchler, J.A. (2019). Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. Proc. Natl. Acad. Sci. U. S. A. 116, 1679-1685.   DOI
21 Sims, J., Changbin, C., Schlogelhofer, P., and Kurzbauer, M.T. (2020b). Targeted analysis of chromatin events (TACE). Methods Mol. Biol. 2061, 47-58.   DOI
22 Armstrong, S.J., Caryl, A.P., Jones, G.H., and Franklin, F.C.H. (2002). Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115, 3645-3655.   DOI
23 Barton, N.H. and Charlesworth, B. (1998). Why sex and recombination? Science 281, 1986-1990.   DOI
24 Sidhu, G.K., Fang, C., Olson, M.A., Falque, M., Martin, O.C., and Pawlowski, W.P. (2015). Recombination patterns in maize reveal limits to crossover homeostasis. Proc. Natl. Acad. Sci. U. S. A. 112, 15982-15987.   DOI
25 Blackwell, A.R., Dluzewska, J., Szymanska-Lejman, M., Desjardins, S., Tock, A.J., Kbiri, N., Lambing, C., Lawrence, E.J., Bieluszewski, T., Rowan, B., et al. (2020). MSH 2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism in Arabidopsis. EMBO J. 39, e104858.   DOI
26 Choi, K., Yelina, N.E., Serra, H., and Henderson, I.R. (2017). Quantification and sequencing of crossover recombinant molecules from Arabidopsis pollen DNA. Methods Mol. Biol. 1551, 23-57.   DOI
27 Taagen, E., Bogdanove, A.J., and Sorrells, M.E. (2020). Counting on crossovers: controlled recombination for plant breeding. Trends Plant Sci. 25, 455-465.   DOI
28 Kurzbauer, M.T., Pradillo, M., Kerzendorfer, C., Sims, J., Ladurner, R., Oliver, C., Janisiw, M.P., Mosiolek, M., Schweizer, D., Copenhaver, G.P., et al. (2018). Arabidopsis thaliana FANCD2 promotes meiotic crossover formation. Plant Cell 30, 415-428.   DOI
29 Kurzbauer, M.T., Uanschou, C., Chen, D., and Schlogelhofer, P. (2012). The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell 24, 2058-2070.   DOI
30 Sun, H., Rowan, B.A., Flood, P.J., Brandt, R., Fuss, J., Hancock, A.M., Michelmore, R.W., Huettel, B., and Schneeberger, K. (2019). Linked-read sequencing of gametes allows efficient genome-wide analysis of meiotic recombination. Nat. Commun. 10, 4310.   DOI
31 Sims, J., Chouaref, J., and Schlogelhofer, P. (2020a). Whole-mount immuno-FISH on Arabidopsis meiocytes (WhoMI-FISH). Methods Mol. Biol. 2061, 59-66.   DOI
32 Sims, J., Schlogelhofer, P., and Kurzbauer, M.T. (2021). From microscopy to nanoscopy: defining an Arabidopsis thaliana meiotic atlas at the nanometer scale. Front. Plant Sci. 12, 672914.   DOI
33 Underwood, C.J., Choi, K., Lambing, C., Zhao, X., Serra, H., Borges, F., Simorowski, J., Ernst, E., Jacob, Y., Henderson, I.R., et al. (2018). Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation. Genome Res. 28, 519-531.   DOI
34 Berchowitz, L.E. and Copenhaver, G.P. (2008). Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat. Protoc. 3, 41-50.   DOI
35 Armstrong, S. (2013). Spreading and fluorescence in situ hybridization of male and female meiocyte chromosomes from Arabidopsis thaliana for cytogenetical analysis. Methods Mol. Biol. 990, 3-11.   DOI
36 Armstrong, S.J., Franklin, F.C.H., and Jones, G.H. (2001). Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114, 4207-4217.   DOI
37 Barra, L., Termolino, P., Aiese Cigliano, R., Cremona, G., Paparo, R., Lanzillo, C., Consiglio, M.F., and Conicella, C. (2021). Meiocyte isolation by INTACT and meiotic transcriptome analysis in Arabidopsis. Front. Plant Sci. 12, 638051.   DOI
38 Capilla-Perez, L., Durand, S., Hurel, A., Lian, Q., Chambon, A., Taochy, C., Solier, V., Grelon, M., and Mercier, R. (2021). The synaptonemal complex imposes crossover interference and heterochiasmy in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 118, e2023613118.   DOI
39 Chelysheva, L., Vezon, D., Chambon, A., Gendrot, G., Pereira, L., Lemhemdi, A., Vrielynck, N., Le Guin, S., Novatchkova, M., and Grelon, M. (2012). The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet. 8, e1002799.   DOI
40 Chen, C., Farmer, A.D., Langley, R.J., Mudge, J., Crow, J.A., May, G.D., Huntley, J., Smith, A.G., and Retzel, E.F. (2010). Meiosis-specific gene discovery in plants: RNA-Seq applied to isolated Arabidopsis male meiocytes. BMC Plant Biol. 10, 280.   DOI
41 Lopez, E., Pradillo, M., Oliver, C., Romero, C., Cunado, N., and Santos, J.L. (2012). Looking for natural variation in chiasma frequency in Arabidopsis thaliana. J. Exp. Bot. 63, 887-894.   DOI
42 Albini, S.M., Jones, G.H., and Wallace, B.M.N. (1984). A method for preparing two-dimensional surface-spreads of synaptonemal complexes from plant meiocytes for light and electron microscopy. Exp. Cell Res. 152, 280-285.   DOI
43 Lam, I. and Keeney, S. (2014). Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb. Perspect. Biol. 7, a016634.   DOI
44 Lambing, C., Kuo, P.C., Tock, A.J., Topp, S.D., and Henderson, I.R. (2020). ASY1 acts as a dosage-dependent antagonist of telomere-led recombination and mediates crossover interference in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 117, 13647-13658.   DOI
45 Lawrence, E.J., Gao, H., Tock, A.J., Lambing, C., Blackwell, A.R., Feng, X., and Henderson, I.R. (2019). Natural variation in TBP-ASSOCIATED FACTOR 4b controls meiotic crossover and germline transcription in Arabidopsis. Curr. Biol. 29, 2676-2686.e3.   DOI
46 Lim, E.C., Kim, J., Park, J., Kim, E.J., Kim, J., Park, Y.M., Cho, H.S., Byun, D., Henderson, I.R., Copenhaver, G.P., et al. (2020). DeepTetrad: high-throughput image analysis of meiotic tetrads by deep learning in Arabidopsis thaliana. Plant J. 101, 473-483.   DOI
47 Luo, C., Li, X., Zhang, Q., and Yan, J. (2019). Single gametophyte sequencing reveals that crossover events differ between sexes in maize. Nat. Commun. 10, 785.   DOI
48 Mair, A. and Bergmann, D.C. (2022). Advances in enzyme-mediated proximity labeling and its potential for plant research. Plant Physiol. 188, 756-768.   DOI
49 Choi, K. and Henderson, I.R. (2015). Meiotic recombination hotspots - a comparative view. Plant J. 83, 52-61.   DOI
50 Choi, K., Reinhard, C., Serra, H., Ziolkowski, P.A., Underwood, C.J., Zhao, X., Hardcastle, T.J., Yelina, N.E., Griffin, C., Jackson, M., et al. (2016). Recombination rate heterogeneity within Arabidopsis disease resistance genes. PLoS Genet. 12, e1006179.   DOI
51 Melamed-Bessudo, C., Yehuda, E., Stuitje, A.R., and Levy, A.A. (2005). A new seed-based assay for meiotic recombination in Arabidopsis thaliana. Plant J. 43, 458-466.   DOI
52 Ur, S.N. and Corbett, K.D. (2021). Architecture and dynamics of meiotic chromosomes. Annu. Rev. Genet. 55, 497-526.   DOI
53 Wijnker, E., Velikkakam James, G., Ding, J., Becker, F., Klasen, J.R., Rawat, V., Rowan, B.A., de Jong, D.F., de Snoo, C.B., Zapata, L., et al. (2013). The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. Elife 2, e01426.   DOI
54 Yelina, N.E., Ziolkowski, P.A., Miller, N., Zhao, X., Kelly, K.A., Munoz, D.F., Mann, D.J., Copenhaver, G.P., and Henderson, I.R. (2013). High-throughput analysis of meiotic crossover frequency and interference via flow cytometry of fluorescent pollen in Arabidopsis thaliana. Nat. Protoc. 8, 2119-2134.   DOI
55 Villeneuve, A.M. and Hillers, K.J. (2001). Whence meiosis? Cell 106, 647-650.   DOI
56 Wang, Y., Zhao, Y., Bollas, A., Wang, Y., and Au, K.F. (2021). Nanopore sequencing technology, bioinformatics and applications. Nat. Biotechnol. 39, 1348-1365.   DOI
57 Wu, G., Rossidivito, G., Hu, T., Berlyand, Y., and Poethig, R.S. (2015). Traffic lines: new tools for genetic analysis in Arabidopsis thaliana. Genetics 200, 35-45.   DOI
58 Xue, M., Wang, J., Jiang, L., Wang, M., Wolfe, S., Pawlowski, W.P., Wang, Y., and He, Y. (2018). The number of meiotic double-strand breaks influencecrossover distribution in arabidopsis[open]. Plant Cell 30, 2628-2638.   DOI
59 Cole, F., Kauppi, L., Lange, J., Roig, I., Wang, R., Keeney, S., and Jasin, M. (2012). Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat. Cell Biol. 14, 424-430.   DOI
60 Choi, K., Zhao, X., Kelly, K.A., Venn, O., Higgins, J.D., Yelina, N.E., Hardcastle, T.J., Ziolkowski, P.A., Copenhaver, G.P., Franklin, F.C.H., et al. (2013). Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat. Genet. 45, 1327-1336.   DOI
61 Copenhaver, G.P., Browne, W.E., and Preuss, D. (1998). Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads. Proc. Natl. Acad. Sci. U. S. A. 95, 247-252.   DOI
62 Cremer, T., Lichter, P., Borden, J., Ward, D., and Manuelidis, L. (1988). Detection of chromosome aberrations in metaphase and interphase tumor cells by in situ hybridization using chromosome-specific library probes. Hum. Genet. 80, 235-246.   DOI
63 De Muyt, A., Pereira, L., Vezon, D., Chelysheva, L., Gendrot, G., Chambon, A., Laine-Choinard, S., Pelletier, G., Mercier, R., Nogue, F., et al. (2009). A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet. 5, e1000654.   DOI
64 do Vale Martins, L., Yu, F., Zhao, H., Dennison, T., Lauter, N., Wang, H., Deng, Z., Thompson, A., Semrau, K., Rouillard, J.M., et al. (2019). Meiotic crossovers characterized by haplotype-specific chromosome painting in maize. Nat. Commun. 10, 4604.   DOI
65 Mercier, R., Mezard, C., Jenczewski, E., Macaisne, N., and Grelon, M. (2015). The molecular biology of meiosis in plants. Annu. Rev. Plant Biol. 66, 297-327.   DOI
66 Shilo, S., Melamed-Bessudo, C., Dorone, Y., Barkai, N., and Levy, A.A. (2015). DNA crossover motifs associated with epigenetic modifications delineate open chromatin regions in Arabidopsis. Plant Cell 27, 2427-2436.   DOI
67 Naish, M., Alonge, M., Wlodzimierz, P., Tock, A.J., Abramson, B.W., Schmucker, A., Mandakova, T., Jamge, B., Lambing, C., Kuo, P., et al. (2021). The genetic and epigenetic landscape of the Arabidopsis centromeres. Science 374, eabi7489.   DOI
68 Oh, Y. and Kim, S.G. (2021). RPS5A promoter-driven Cas9 produces heritable virus-induced genome editing in Nicotiana attenuata. Mol. Cells 44, 911-919.   DOI
69 Modliszewski, J.L., Wang, H., Albright, A.R., Lewis, S.M., Bennett, A.R., Huang, J., Ma, H., Wang, Y., and Copenhaver, G.P. (2018). Elevated temperature increases meiotic crossover frequency via the interfering (Type I) pathway in Arabidopsis thaliana. PLoS Genet. 14, e1007384.   DOI
70 Drouaud, J., Khademian, H., Giraut, L., Zanni, V., Bellalou, S., Henderson, I.R., Falque, M., and Mezard, C. (2013). Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLoS Genet. 9, e1003922.   DOI
71 Fernandes, J.B., Seguela-Arnaud, M., Larcheveque, C., Lloyd, A.H., and Mercier, R. (2018). Unleashing meiotic crossovers in hybrid plants. Proc. Natl. Acad. Sci. U. S. A. 115, 2431-2436.   DOI
72 Pinkel, D., Landegent, J., Collins, C., Fuscoe, J., Segraves, R., Lucas, J., and Gray, J. (1988). Fluorescence in situ hybridization with human chromosome-specific libraries: detection of trisomy 21 and translocations of chromosome 4. Proc. Natl. Acad. Sci. U. S. A. 85, 9138-9142.   DOI
73 Moran, E.S., Armstrong, S.J., Santos, J.L., Franklin, F.C.H., and Jones, G.H. (2001). Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res. 9, 121-128.   DOI
74 Morgan, C. and Wegel, E. (2020). Cytological characterization of Arabidopsis arenosa polyploids by SIM. Methods Mol. Biol. 2061, 37-46.   DOI
75 Morgan, C., Fozard, J.A., Hartley, M., Henderson, I.R., Bomblies, K., and Howard, M. (2021). Diffusion-mediated HEI10 coarsening can explain meiotic crossover positioning in Arabidopsis. Nat. Commun. 12, 4674.   DOI
76 Prusicki, M.A., Keizer, E.M., Van Rosmalen, R.P., Komaki, S., Seifert, F., Muller, K., Wijnker, E., Fleck, C., and Schnittger, A. (2019). Live cell imaging of meiosis in arabidopsis thaliana. Elife 8, e42834.   DOI
77 Salome, P.A., Bomblies, K., Fitz, J., Laitinen, R.A.E., Warthmann, N., Yant, L., and Weigel, D. (2012). The recombination landscape in Arabidopsis thaliana F2 populations. Heredity (Edinb.) 108, 447-455.   DOI
78 Rosu, S., Libuda, D.E., and Villeneuve, A.M. (2011). Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334, 1286-1289.   DOI
79 Rowan, B.A., Patel, V., Weigel, D., and Schneeberger, K. (2015). Rapid and inexpensive whole-genome genotyping-by-sequencing for crossover localization and fine-scale genetic mapping. G3 (Bethesda) 5, 385-398.   DOI
80 Saini, R., Singh, A.K., Hyde, G.J., and Baskar, R. (2020). Levels of heterochiasmy during arabidopsis development as reported by fluorescent tagged lines. G3 (Bethesda) 10, 2103-2110.   DOI
81 Sanchez-Moran, E., Armstrong, S.J., Santos, J.L., Franklin, F.C.H., and Jones, G.H. (2002). Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics 162, 1415-1422.   DOI
82 Yelina, N.E., Choi, K., Chelysheva, L., Macaulay, M., de Snoo, B., Wijnker, E., Miller, N., Drouaud, J., Grelon, M., Copenhaver, G.P., et al. (2012). Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet. 8, e1002844.   DOI
83 Mieulet, D., Aubert, G., Bres, C., Klein, A., Droc, G., Vieille, E., Rond-Coissieux, C., Sanchez, M., Dalmais, M., Mauxion, J.P., et al. (2018). Unleashing meiotic crossovers in crops. Nat. Plants 4, 1010-1016.   DOI
84 Zhu, L., Fernandez-Jimenez, N., Szymanska-Lejman, M., Pele, A., Underwood, C.J., Serra, H., Lambing, C., Dluzewska, J., Bieluszewski, T., Pradillo, M., et al. (2021). Natural variation identifies SNI1, the SMC5/6 component, as a modifier of meiotic crossover in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 118, e2021970118.   DOI
85 Yelina, N.E., Lambing, C., Hardcastle, T.J., Zhao, X., Santos, B., and Henderson, I.R. (2015). DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis. Genes Dev. 29, 2183-2202.   DOI
86 Ziolkowski, P.A., Berchowitz, L.E., Lambing, C., Yelina, N.E., Zhao, X., Kelly, K.A., Choi, K., Ziolkowska, L., June, V., Sanchez-Moran, E., et al. (2015). Juxtaposition of heterozygous and homozygous regions causes reciprocal crossover remodelling via interference during Arabidopsis meiosis. Elife 4, e03708.   DOI
87 Ziolkowski, P.A., Underwood, C.J., Lambing, C., Martinez-Garcia, M., Lawrence, E.J., Ziolkowska, L., Griffin, C., Choi, K., Franklin, F.C.H., Martienssen, R.A., et al. (2017). Natural variation and dosage of the HEI10 meiotic E3 ligase control Arabidopsis crossover recombination. Genes Dev. 31, 306-317.   DOI
88 Choi, K. (2017). Advances towards controlling meiotic recombination for plant breeding. Mol. Cells 40, 814-822.   DOI
89 Zhao, Q., Wang, Y., Bi, Y., Zhai, Y., Yu, X., Cheng, C., Wang, P., Li, J., Lou, Q., and Chen, J. (2019). Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis × hytivus with dysploid parental karyotypes. BMC Plant Biol. 19, 471.   DOI
90 Lloyd, A., Morgan, C., Franklin, F., and Bomblies, K. (2018). Plasticity of meiotic recombination rates in response to temperature in Arabidopsis. Genetics 208, 1409-1420.   DOI
91 Martini, E., Diaz, R.L., Hunter, N., and Keeney, S. (2006). Crossover homeostasis in yeast meiosis. Cell 126, 285-295.   DOI
92 Nageswaran, D.C., Kim, J., Lambing, C., Kim, J., Park, J., Kim, E.J., Cho, H.S., Kim, H., Byun, D., Park, Y.M., et al. (2021). HIGH CROSSOVER RATE1 encodes PROTEIN PHOSPHATASE X1 and restricts meiotic crossovers in Arabidopsis. Nat. Plants 7, 452-467.   DOI
93 Chelysheva, L., Grandont, L., Vrielynck, N., le Guin, S., Mercier, R., and Grelon, M. (2010). An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet. Genome Res. 129, 143-153.   DOI
94 Ross, K.J., Fransz, P., and Jones, G.H. (1996). A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 4, 507-516.   DOI