{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,3]],"date-time":"2026-03-03T18:48:07Z","timestamp":1772563687287,"version":"3.50.1"},"reference-count":93,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,4,11]],"date-time":"2023-04-11T00:00:00Z","timestamp":1681171200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"the Russian Scientific Foundation","doi-asserted-by":"publisher","award":["20-46-07005"],"award-info":[{"award-number":["20-46-07005"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Meiotic crossovers\/chiasmata are not randomly distributed and strictly controlled. The mechanisms behind crossover (CO) patterning remain largely unknown. In Allium cepa, as in the vast majority of plants and animals, COs predominantly occur in the distal 2\/3 of the chromosome arm, while in Allium fistulosum they are strictly localized in the proximal region. We investigated the factors that may contribute to the pattern of COs in A. cepa, A. fistulosum and their F1 diploid (2n = 2x = 8C + 8F) and F1 triploid (2n = 3x = 16F + 8C) hybrids. The genome structure of F1 hybrids was confirmed using genomic in situ hybridization (GISH). The analysis of bivalents in the pollen mother cells (PMCs) of the F1 triploid hybrid showed a significant shift in the localization of COs to the distal and interstitial regions. In F1 diploid hybrid, the COs localization was predominantly the same as that of the A. cepa parent. We found no differences in the assembly and disassembly of ASY1 and ZYP1 in PMCs between A. cepa and A. fistulosum, while F1 diploid hybrid showed a delay in chromosome pairing and a partial absence of synapsis in paired chromosomes. Immunolabeling of MLH1 (class I COs) and MUS81 (class II COs) proteins showed a significant difference in the class I\/II CO ratio between A. fistulosum (50%:50%) and A. cepa (73%:27%). The MLH1:MUS81 ratio at the homeologous synapsis of F1 diploid hybrid (70%:30%) was the most similar to that of the A. cepa parent. F1 triploid hybrid at the A. fistulosum homologous synapsis showed a significant increase in MLH1:MUS81 ratio (60%:40%) compared to the A. fistulosum parent. The results suggest possible genetic control of CO localization. Other factors affecting the distribution of COs are discussed.<\/jats:p>","DOI":"10.3390\/ijms24087066","type":"journal-article","created":{"date-parts":[[2023,4,12]],"date-time":"2023-04-12T02:57:08Z","timestamp":1681268228000},"page":"7066","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["The Control of the Crossover Localization in Allium"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9790-6567","authenticated-orcid":false,"given":"Natalia","family":"Kudryavtseva","sequence":"first","affiliation":[{"name":"All-Russian Research Institute of Agricultural Biotechnology, 42 Timiryazevskaya Str., Moscow 127550, Russia"},{"name":"Center of Molecular Biotechnology, Russian State Agrarian University\u2014Moscow Timiryazev Agricultural Academy, 49 Timiryazevskaya Str., Moscow 127550, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9789-8694","authenticated-orcid":false,"given":"Aleksey","family":"Ermolaev","sequence":"additional","affiliation":[{"name":"All-Russian Research Institute of Agricultural Biotechnology, 42 Timiryazevskaya Str., Moscow 127550, Russia"},{"name":"Center of Molecular Biotechnology, Russian State Agrarian University\u2014Moscow Timiryazev Agricultural Academy, 49 Timiryazevskaya Str., Moscow 127550, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1840-1561","authenticated-orcid":false,"given":"Anton","family":"Pivovarov","sequence":"additional","affiliation":[{"name":"All-Russian Research Institute of Agricultural Biotechnology, 42 Timiryazevskaya Str., Moscow 127550, Russia"},{"name":"Center of Molecular Biotechnology, Russian State Agrarian University\u2014Moscow Timiryazev Agricultural Academy, 49 Timiryazevskaya Str., Moscow 127550, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0830-7977","authenticated-orcid":false,"given":"Sergey","family":"Simanovsky","sequence":"additional","affiliation":[{"name":"All-Russian Research Institute of Agricultural Biotechnology, 42 Timiryazevskaya Str., Moscow 127550, Russia"},{"name":"Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninsky Prosp., Moscow 119071, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6785-8373","authenticated-orcid":false,"given":"Sergey","family":"Odintsov","sequence":"additional","affiliation":[{"name":"All-Russian Research Institute of Agricultural Biotechnology, 42 Timiryazevskaya Str., Moscow 127550, Russia"},{"name":"Center of Molecular Biotechnology, Russian State Agrarian University\u2014Moscow Timiryazev Agricultural Academy, 49 Timiryazevskaya Str., Moscow 127550, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0614-4641","authenticated-orcid":false,"given":"Ludmila","family":"Khrustaleva","sequence":"additional","affiliation":[{"name":"All-Russian Research Institute of Agricultural Biotechnology, 42 Timiryazevskaya Str., Moscow 127550, Russia"},{"name":"Center of Molecular Biotechnology, Russian State Agrarian University\u2014Moscow Timiryazev Agricultural Academy, 49 Timiryazevskaya Str., Moscow 127550, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/BF03020823","article-title":"Meiosis in diploid and tetraploid Primula sinensis","volume":"24","author":"Darlington","year":"1931","journal-title":"J. Genet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1146\/annurev-genet-120213-092509","article-title":"Factors underlying restricted crossover localization in barley meiosis","volume":"48","author":"Higgins","year":"2014","journal-title":"Annu. Rev. Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"a016634","DOI":"10.1101\/cshperspect.a016634","article-title":"Mechanism and regulation of meiotic recombination initiation","volume":"7","author":"Lam","year":"2015","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1146\/annurev-arplant-050213-035923","article-title":"The molecular biology of meiosis in plants","volume":"66","author":"Mercier","year":"2015","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1146\/annurev-genet-120215-035111","article-title":"Control of meiotic crossovers: From double-strand break formation to designation","volume":"50","author":"Gray","year":"2016","journal-title":"Annu. Rev. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2477","DOI":"10.1111\/mec.14699","article-title":"Meta-analysis of chromosome-scale crossover rate variation in eukaryotes and its significance to evolutionary genomics","volume":"27","author":"Haenel","year":"2018","journal-title":"Mol. Ecol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13059-019-1675-6","article-title":"Analysis of the recombination landscape of hexaploid bread wheat reveals genes controlling recombination and gene conversion frequency","volume":"20","author":"Gardiner","year":"2019","journal-title":"Genome Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3644","DOI":"10.1038\/s41467-022-31438-6","article-title":"FANCM promotes class I interfering crossovers and suppresses class II non-interfering crossovers in wheat meiosis","volume":"13","author":"Desjardins","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1126\/science.81.2109.543","article-title":"A Gene for Control of Interstitial Localization of Chiasmata in Allium fistulosum L.","volume":"81","author":"Emsweller","year":"1935","journal-title":"Science"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"275","DOI":"10.3733\/hilg.v09n05p275","article-title":"Meiosis in Allium fistulosum, Allium cepa, and their hybrid","volume":"9","author":"Emsweller","year":"1935","journal-title":"Hilgardia"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1038\/hdy.1976.45","article-title":"Heterochromatic patterns in Allium","volume":"36","author":"Vosa","year":"1976","journal-title":"Heredity"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1038\/272823a0","article-title":"Cytological detection of crossing-over in BUdR substituted meiotic chromosomes using the fluorescent plus Giemsa technique","volume":"272","author":"Tease","year":"1978","journal-title":"Nature"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/BF00329915","article-title":"Analysis of exchanges in differentially stained meiotic chromosomes of Locusta migratoria after BrdU-substitution and FPG staining","volume":"69","author":"Tease","year":"1978","journal-title":"Chromosoma"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/S0092-8674(04)00297-1","article-title":"Early decision: Meiotic crossover interference prior to stable strand exchange and synapsis","volume":"117","author":"Bishop","year":"2004","journal-title":"Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"R1036","DOI":"10.1016\/j.cub.2004.11.038","article-title":"Crossover interference","volume":"14","author":"Hillers","year":"2004","journal-title":"Curr. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"12592","DOI":"10.1073\/pnas.0402724101","article-title":"A mechanical basis for chromosome function","volume":"101","author":"Kleckner","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1611","DOI":"10.1242\/jcs.115.8.1611","article-title":"The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination","volume":"115","author":"Moens","year":"2002","journal-title":"J. Cell Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.cell.2006.05.044","article-title":"Crossover homeostasis in yeast meiosis","volume":"126","author":"Martini","year":"2006","journal-title":"Cell"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"681123","DOI":"10.3389\/fcell.2021.681123","article-title":"Meiotic crossover patterning","volume":"9","author":"Pazhayam","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1038\/ng.2766","article-title":"Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters","volume":"45","author":"Choi","year":"2013","journal-title":"Nat. Genet."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1086\/279534","article-title":"The mechanism of crossing-over","volume":"50","author":"Muller","year":"1916","journal-title":"Am. Nat."},{"key":"ref_22","first-page":"234","article-title":"The behavior of the chromosomes as studied through linkage","volume":"13","author":"Sturtevant","year":"1915","journal-title":"Z. F\u00dcR Indukt. Abstammungs Und Vererbungslehre"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3645","DOI":"10.1242\/jcs.00048","article-title":"Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica","volume":"115","author":"Armstrong","year":"2002","journal-title":"J. Cell Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"13647","DOI":"10.1073\/pnas.1921055117","article-title":"ASY1 acts as a dosage-dependent antagonist of telomere-led recombination and mediates crossover interference in Arabidopsis","volume":"117","author":"Lambing","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"e2023613118","DOI":"10.1073\/pnas.2023613118","article-title":"The synaptonemal complex imposes crossover interference and heterochiasmy in Arabidopsis","volume":"118","author":"Durand","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e2021671118","DOI":"10.1073\/pnas.2021671118","article-title":"ZYP1 is required for obligate cross-over formation and cross-over interference in Arabidopsis","volume":"118","author":"France","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"9043","DOI":"10.1073\/pnas.93.17.9043","article-title":"Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes","volume":"93","author":"Storlazzi","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s00497-022-00445-4","article-title":"Crossover patterning in plants","volume":"36","author":"Lloyd","year":"2022","journal-title":"Plant Reprod."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1007\/s10577-007-1150-1","article-title":"ZMM proteins during meiosis: Crossover artists at work","volume":"15","author":"Lynn","year":"2007","journal-title":"Chromosome Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.cell.2012.03.023","article-title":"Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase","volume":"149","author":"Zakharyevich","year":"2012","journal-title":"Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1101\/gad.1165904","article-title":"The Mus81 solution to resolution: Generating meiotic crossovers without Holliday junctions","volume":"18","author":"Hollingsworth","year":"2004","journal-title":"Genes Dev."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.molcel.2012.02.020","article-title":"BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism","volume":"46","author":"Jessop","year":"2012","journal-title":"Mol. Cell"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Berchowitz, L.E., Francis, K.E., Bey, A.L., and Copenhaver, G.P. (2007). The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet., 3.","DOI":"10.1371\/journal.pgen.0030132"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1588","DOI":"10.1126\/science.1220381","article-title":"FANCM limits meiotic crossovers","volume":"336","author":"Crismani","year":"2012","journal-title":"Science"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1111\/j.1365-313X.2008.03403.x","article-title":"Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over","volume":"54","author":"Higgins","year":"2008","journal-title":"Plant J."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/j.tibs.2003.08.011","article-title":"Holliday junctions in the eukaryotic nucleus: Resolution in sight?","volume":"28","author":"Heyer","year":"2003","journal-title":"Trends Biochem. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1016\/S1097-2765(03)00343-5","article-title":"Generating crossovers by resolution of nicked Holliday junctions: A role for Mus81-Eme1 in meiosis","volume":"12","author":"Osman","year":"2003","journal-title":"Mol. Cell"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1105\/tpc.17.00745","article-title":"Arabidopsis thaliana FANCD2 promotes meiotic crossover formation","volume":"30","author":"Kurzbauer","year":"2018","journal-title":"Plant Cell"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1159\/000314096","article-title":"An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: Immunodetection of cohesins, histones and MLH1","volume":"129","author":"Chelysheva","year":"2010","journal-title":"Cytogenet. Genome Res."},{"key":"ref_40","first-page":"1","article-title":"Licensing MLH1 sites for crossover during meiosis","volume":"5","author":"Shaw","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1105\/tpc.106.049106","article-title":"The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato","volume":"19","author":"Lhuissier","year":"2007","journal-title":"Plant Cell"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"13415","DOI":"10.1073\/pnas.1406846111","article-title":"Combined fluorescent and electron microscopic imaging unveils the specific properties of two classes of meiotic crossovers","volume":"111","author":"Anderson","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1545","DOI":"10.1104\/pp.20.00534","article-title":"MutS homologue 4 and MutS homologue 5 maintain the obligate crossover in wheat despite stepwise gene loss following polyploidization","volume":"183","author":"Desjardins","year":"2020","journal-title":"Plant Physiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e2107543118","DOI":"10.1073\/pnas.2107543118","article-title":"Regulation of interference-sensitive crossover distribution ensures crossover assurance in Arabidopsis","volume":"118","author":"Li","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Holloway, J.K., Booth, J., Edelmann, W., McGowan, C.H., and Cohen, P.E. (2008). MUS81 generates a subset of MLH1-MLH3\u2013independent crossovers in mammalian meiosis. PLoS Genet., 4.","DOI":"10.1371\/journal.pgen.1000186"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1139\/g90-129","article-title":"Synaptonemal complex spreading in Allium cepa and Allium fistulosum. III. The F1 hybrid","volume":"33","author":"Albini","year":"1990","journal-title":"Genome"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1007\/BF00022933","article-title":"Greenhouse technique to evaluate pink root disease caused by Pyrenochaeta terrestris","volume":"34","author":"Netzer","year":"1985","journal-title":"Euphytica"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1023\/A:1002914225154","article-title":"Screening for resistance to anthracnose (Colletotrichum gloeosporioides Penz.) in Allium cepa and its wild relatives","volume":"95","author":"Wietsma","year":"1997","journal-title":"Euphytica"},{"key":"ref_49","unstructured":"Rabinowitch, H.D. (1994, January 14\u201318). Breeding alliaceous crops for pest resistance. Proceedings of the I International Symposium on Edible Alliaceae 433, Mendoza, Argentina."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"jkab243","DOI":"10.1093\/g3journal\/jkab243","article-title":"Insights from the first genome assembly of Onion (Allium cepa)","volume":"11","author":"Finkers","year":"2021","journal-title":"G3"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1006\/anbo.1999.0871","article-title":"Genome size in Allium: In quest of reproducible data","volume":"83","author":"Baranyu","year":"1999","journal-title":"Ann. Bot."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1534\/genetics.109.108688","article-title":"Interlock formation and coiling of meiotic chromosome axes during synapsis","volume":"183","author":"Wang","year":"2009","journal-title":"Genetics"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1105\/tpc.109.070789","article-title":"The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice","volume":"22","author":"Wang","year":"2010","journal-title":"Plant Cell"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1533","DOI":"10.1093\/jxb\/erq292","article-title":"Maize meiotic mutants with improper or non-homologous synapsis due to problems in pairing or synaptonemal complex formation","volume":"62","author":"Golubovskaya","year":"2011","journal-title":"J. Exp. Bot."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1756-0500-5-106","article-title":"The isolation and characterisation of the wheat molecular ZIPper I homologue, TaZYP1","volume":"5","author":"Khoo","year":"2012","journal-title":"Bmc Res. Notes"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2488","DOI":"10.1101\/gad.354705","article-title":"The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over","volume":"19","author":"Higgins","year":"2005","journal-title":"Genes Dev."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1534\/genetics.106.064105","article-title":"Molecular assembly of meiotic proteins Asy1 and Zyp1 and pairing promiscuity in rye (Secale cereale L.) and its synaptic mutant sy10","volume":"174","author":"Mikhailova","year":"2006","journal-title":"Genetics"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Phillips, D., Nibau, C., Wnetrzak, J., and Jenkins, G. (2012). High resolution analysis of meiotic chromosome structure and behaviour in barley (Hordeum vulgare L.). PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0039539"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"773","DOI":"10.3389\/fpls.2019.00773","article-title":"Ultrastructure and dynamics of synaptonemal complex components during meiotic pairing and synapsis of standard (A) and accessory (B) rye chromosomes","volume":"10","author":"Hesse","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_60","unstructured":"Ehmsen, K.T., and Heyer, W.D. (2008). Recombination and Meiosis, Springer."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"3012","DOI":"10.1093\/jxb\/erab035","article-title":"Meiotic chromosome axis remodelling is critical for meiotic recombination in Brassica rapa","volume":"72","author":"Cuacos","year":"2021","journal-title":"J. Exp. Bot."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1448","DOI":"10.1105\/tpc.112.096644","article-title":"The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis","volume":"24","author":"Knoll","year":"2012","journal-title":"Plant Cell"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"e00194-19","DOI":"10.1128\/MCB.00194-19","article-title":"FANCD2 binding to H4K20me2 via a methyl-binding domain is essential for efficient DNA cross-link repair","volume":"39","author":"Paquin","year":"2019","journal-title":"Mol. Cell. Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1007\/s00412-008-0174-4","article-title":"Unexpected behavior of an inverted rye chromosome arm in wheat","volume":"117","author":"Lukaszewski","year":"2008","journal-title":"Chromosoma"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Giraut, L., Falque, M., Drouaud, J., Pereira, L., Martin, O.C., and M\u00e9zard, C. (2011). Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet., 7.","DOI":"10.1371\/journal.pgen.1002354"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/gb-2013-14-9-r103","article-title":"Intraspecific variation of recombination rate in maize","volume":"14","author":"Bauer","year":"2013","journal-title":"Genome Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1111\/j.1601-5223.1941.tb03260.x","article-title":"The cytology of the species hybrid Allium cepa \u00d7 fistulosum and its polyploid derivatives","volume":"27","author":"Levan","year":"1941","journal-title":"Hereditas"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1038\/hdy.1996.26","article-title":"Meiosis in the leek (Allium porrum L.) revisited. II. Metaphase I observations","volume":"76","author":"Jones","year":"1996","journal-title":"Heredity"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"593","DOI":"10.2503\/jjshs.63.593","article-title":"C-banded karyotype analysis of Allium fistulosum and A. altaicum and their phylogenetic relationship","volume":"63","author":"Inada","year":"1994","journal-title":"J. Jpn. Soc. Hortic. Sci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/BF02983364","article-title":"Fritillaria meleagris: Chiasmaformation and distribution","volume":"22","author":"Newton","year":"1930","journal-title":"J. Genet."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1023\/A:1003728808682","article-title":"AFLPs in leek (Allium porrum) are not inherited in large linkage blocks","volume":"110","author":"Smilde","year":"1999","journal-title":"Euphytica"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1023\/A:1016379319030","article-title":"Organization of the 378-bp satellite repeat in terminal heterochromatin of Allium fistulosum","volume":"38","author":"Fesenko","year":"2002","journal-title":"Russ. J. Genet."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"43","DOI":"10.17660\/ActaHortic.2012.969.2","article-title":"The chromosome organization of genes and some types of extragenic DNA in Allium","volume":"969","author":"Khrustaleva","year":"2012","journal-title":"Acta Hortic."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"4096","DOI":"10.1105\/tpc.112.102483","article-title":"Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley","volume":"24","author":"Higgins","year":"2012","journal-title":"Plant Cell"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"5880","DOI":"10.1073\/pnas.1120841109","article-title":"Loss of DNA methylation affects the recombination landscape in Arabidopsis","volume":"109","author":"Mirouze","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1101\/gr.227116.117","article-title":"Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation","volume":"28","author":"Underwood","year":"2018","journal-title":"Genome Res."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"eaau8861","DOI":"10.1126\/science.aau8861","article-title":"Factors influencing meiotic recombination revealed by whole-genome sequencing of single sperm","volume":"363","author":"Hinch","year":"2019","journal-title":"Science"},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Dreissig, S., Fuchs, J., C\u00e1pal, P., Kettles, N., Byrne, E., and Houben, A. (2015). Measuring meiotic crossovers via multi-locus genotyping of single pollen grains in barley. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0137677"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1620","DOI":"10.3389\/fpls.2017.01620","article-title":"Sequencing of single pollen nuclei reveals meiotic recombination events at megabase resolution and circumvents segregation distortion caused by postmeiotic processes","volume":"8","author":"Dreissig","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1007\/s00438-016-1286-9","article-title":"Tandem repeats of Allium fistulosum associated with major chromosomal landmarks","volume":"292","author":"Kirov","year":"2017","journal-title":"Mol. Genet. Genom."},{"key":"ref_81","unstructured":"Jenkins, G., and Rees, H. (1982, January 1\u20134). Synaptonemal complex formation in a Festuca hybrid. Proceedings of the Kew Chromosome Conference II, Kew, UK."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1038\/hdy.1990.6","article-title":"Elimination of synaptonemal complex irregularities in a Lolium hybrid","volume":"64","author":"Jenkins","year":"1990","journal-title":"Heredity"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1038\/nrm3805","article-title":"Mechanisms and principles of homology search during recombination","volume":"15","author":"Renkawitz","year":"2014","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1038\/s41438-021-00672-2","article-title":"Genome-wide unbalanced expression bias and expression level dominance toward Brassica oleracea in artificially synthesized intergeneric hybrids of Raphanobrassica","volume":"8","author":"Zhang","year":"2021","journal-title":"Hortic. Res."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1038\/ncb2451","article-title":"Homeostatic control of recombination is implemented progressively in mouse meiosis","volume":"14","author":"Cole","year":"2012","journal-title":"Nat. Cell Biol."},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Kudryavtseva, N., Havey, M.J., Black, L., Hanson, P., Sokolov, P., Odintsov, S., Divashuk, M., and Khrustaleva, L. (2019). Cytological evaluations of advanced generations of interspecific hybrids between Allium cepa and Allium fistulosum showing resistance to Stemphylium vesicarium. Genes, 10.","DOI":"10.3390\/genes10030195"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1007\/s001220050702","article-title":"Cytogenetical studies in the bridge cross Allium cepa \u00d7 (A. fistulosum \u00d7 A. roylei)","volume":"96","author":"Khrustaleva","year":"1998","journal-title":"Theor. Appl. Genet."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"747","DOI":"10.3897\/compcytogen.v11i4.20830","article-title":"DRAWID: User-friendly java software for chromosome measurements and idiogram drawing","volume":"11","author":"Kirov","year":"2017","journal-title":"Comp. Cytogenet."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/BF00024124","article-title":"Onion chromosome nomenclature and homoeology relationships workshop report","volume":"49","year":"1990","journal-title":"Euphytica"},{"key":"ref_90","unstructured":"De Vries, J., and Jongerius, M. (1988, January 6\u20139). Interstitial C-bands on the chromosomes of Allium-species from the section cepa. Proceedings of the Allium symposium: EUCARPIA-Section Vegetables, Coventry, UK."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"3318","DOI":"10.1105\/tpc.110.078568","article-title":"RAD5A, RECQ4A, and MUS81 have specific functions in homologous recombination and define different pathways of DNA repair in Arabidopsis thaliana","volume":"22","author":"Mannuss","year":"2010","journal-title":"Plant Cell"},{"key":"ref_92","unstructured":"Team, R.C. (2022, January 10). R: A Language and Environment for Statistical Computing. Available online: http:\/\/www.R-project.org\/."},{"key":"ref_93","unstructured":"Mangiafico, S. (Rcompanion: Functions to Support Extension Education Program Evaluation, 2023). Rcompanion: Functions to Support Extension Education Program Evaluation, R package version 2.4.21."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/8\/7066\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:13:58Z","timestamp":1760123638000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/8\/7066"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,11]]},"references-count":93,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["ijms24087066"],"URL":"https:\/\/doi.org\/10.3390\/ijms24087066","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,11]]}}}