Crossing over, in addition to its strictly genetic role, also performs a critical mechanical function, by bonding homologues in meiosis. Hence, it is responsible for an orderly reduction of the chromosome number. As such, it is strictly controlled in frequency and distribution. The well-known crossover control is positive crossover interference which reduces the probability of a crossover in the vicinity of an already formed crossover. A poorly studied aspect of the control is chromatid interference. Such analyses are possible in very few organisms as they require observation of all four products of a single meiosis. Here, we provide direct evidence of chromatid interference. Using in situ probing in two interspecific plant hybrids (Lolium multiflorum×Festuca pratensis and Allium cepa×A. roylei) during anaphase I, we demonstrate that the involvement of four chromatids in double crossovers is significantly more frequent than expected (64% versus 25%). We also provide a physical measure of the crossover interference distance, covering ~30-40% of the relative chromosome arm length, and show that the centromere acts as a barrier for crossover interference. The two arms of a chromosome appear to act as independent units in the process of crossing over. Chromatid interference has to be seriously addressed in genetic mapping approaches and further studies.

Department of Biology Federal University of Lavras Lavras MG Brazil

Department of Botany and Plant Sciences University of California Riverside CA USA

Department of Botany Faculty of Science Palacký University Olomouc Czech Republic

Institute of Experimental Botany Czech Academy of Sciences Centre of the Region Haná for Biotechnological and Agricultural Research Olomouc Czech Republic

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

Plant Breeding Wageningen University and Research Wageningen The Netherlands

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Anderson LK, Lohmiller LD, Tang X, Hammond DB, Javernick L, Shearer L, Basu-Roy S, Martin OC, Falque M. 2014. Combined fluorescent and electron microscopic imaging unveils the specific properties of two classes of meiotic crossovers. Proceedings of the National Academy of Sciences, USA 111, 13415–13420. PubMed PMC

Auger DL, Sheridan WF. 2001. Negative crossover interference in maize translocation heterozygotes. Genetics 159, 1717–1726. PubMed PMC

Barlow AL, Hultén MA. 1998. Crossing over analysis at pachytene in man. European Journal of Human Genetics 6, 350–358. PubMed

Berchowitz LE, Copenhaver GP. 2008. Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nature Protocols 3, 41–50. PubMed

Berchowitz LE, Copenhaver GP. 2010. Genetic interference: don’t stand so close to me. Current Genomics 11, 91–102. PubMed PMC

Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. 2007. The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genetics 3, e132. PubMed PMC

Börner GV, Kleckner N, Hunter N. 2004. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117, 29–45. PubMed

Broman KW, Rowe LB, Churchill GA, Paigen K. 2002. Crossover interference in the mouse. Genetics 160, 1123–1131. PubMed PMC

Broman KW, Weber JL. 2000. Characterization of human crossover interference. American Journal of Human Genetics 66, 1911–1926. PubMed PMC

Callan HG, Montalenti G. 1947. Chiasma interference in mosquitoes. Journal of Genetics 48, 119–134. PubMed

Colombo PC, Jones GH. 1997. Chiasma interference is blind to centromeres. Heredity 79, 214–227. PubMed

Cooper TJ, Garcia V, Neale MJ. 2016. Meiotic DSB patterning: a multifaceted process. Cell Cycle 15, 13–21. PubMed PMC

Copenhaver GP, Keith KC, Preuss D. 2000. Tetrad analysis in higher plants. A budding technology. Plant Physiology 124, 7–16. PubMed PMC

Creighton HB, McClintock B. 1931. A correlation of cytological and genetical crossing-over in Zea mays. Proceedings of the National Academy of Sciences, USA 17, 492–497. PubMed PMC

Datta A, Hendrix M, Lipsitch M, Jinks-Robertson S. 1997. Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proceedings of the National Academy of Sciences, USA 94, 9757–9762. PubMed PMC

Dawe RK 1998. Meiotic chromosome organization and segregation in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49, 371–395. PubMed

Dolezel J, Sgorbati S, Lucretti S. 1992. Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiologia Plantarum 85, 625–631.

Esch E, Weber W. 2002. Investigation of crossover interference in barley (Hordeum vulgare L.) using the coefficient of coincidence. Theoretical and Applied Genetics 104, 786–796. PubMed

Fernandes JB, Séguéla-Arnaud M, Larchevêque C, Lloyd AH, Mercier R. 2018. Unleashing meiotic crossovers in hybrid plants. Proceedings of the National Academy of Sciences, USA 115, 2431–2436. PubMed PMC

Foss E, Lande R, Stahl FW, Steinberg CM. 1993. Chiasma interference as a function of genetic distance. Genetics 133, 681–691. PubMed PMC

Fowler KR, Hyppa RW, Cromie GA, Smith GR. 2018. Physical basis for long-distance communication along meiotic chromosomes. Proceedings of the National Academy of Sciences, USA 115, E9333–E9342. PubMed PMC

Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ. 2015. Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation. Nature 520, 114–118. PubMed PMC

Harte C 1956. Die Variabilität der Chiasmenbildung bei Paeonia tenuifolia. Chromosoma 8, 152–182.

Hawthorne DC, Mortimer RK. 1960. Chromosome mapping in Saccharomyces: centromere-linked genes. Genetics 45, 1085–1110. PubMed PMC

Higgins JD, Osman K, Jones GH, Franklin FC. 2014. Factors underlying restricted crossover localization in barley meiosis. Annual Review of Genetics 48, 29–47. PubMed

Hillers KJ 2004. Crossover interference. Current Biology 14, R1036–R1037. PubMed

Hou Y, Fan W, Yan L, et al. . 2013. Genome analyses of single human oocytes. Cell 155, 1492–1506. PubMed

Jauhar PP 1975. Chromosome relationships between Lolium and Festuca (Gramineae). Chromosoma 52, 103–121.

John B 1990. Meiosis. Cambridge University Press,

Jones G 1987. Chiasmata. In: Moens PB, ed. Meiosis. Orlando: Academic Press, 213–244.

Jones GH 1984. The control of chiasma distribution. Symposia of the Society for Experimental Biology 38, 293–320. PubMed

Jones GH, Franklin FC. 2006. Meiotic crossing-over: obligation and interference. Cell 126, 246–248. PubMed

Jordan KW, Wang S, He F, et al. . 2018. The genetic architecture of genome-wide recombination rate variation in allopolyploid wheat revealed by nested association mapping. The Plant Journal 95, 1039–1054. PubMed PMC

Kaback DB, Barber D, Mahon J, Lamb J, You J. 1999. Chromosome size-dependent control of meiotic reciprocal recombination in Saccharomyces cerevisiae: the role of crossover interference. Genetics 152, 1475–1486. PubMed PMC

Karp A, Jones RN. 1983. Cytogenetics of Lolium perenne. Part 2. Chiasma distribution in inbred lines. Theoretical and Applied Genetics 64, 137–145. PubMed

Khrustaleva LI, Kik C. 2000. Introgression of Allium fistulosum into A.cepa mediated by A.roylei. Theoretical and Applied Genetics 100, 17–26.

King JS, Mortimer RK. 1990. A polymerization model of chiasma interference and corresponding computer simulation. Genetics 126, 1127–1138. PubMed PMC

Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R, Henle J, Hutchinson J. 2004. A mechanical basis for chromosome function. Proceedings of the National Academy of Sciences, USA 101, 12592–12597. PubMed PMC

Kopecký D, Havránková M, Loureiro J, Castro S, Lukaszewski AJ, Bartos J, Kopecká J, Dolezel J. 2010. Physical distribution of homoeologous recombination in individual chromosomes of Festuca pratensis in Lolium multiflorum. Cytogenetic and Genome Research 129, 162–172. PubMed

Kopecký D, Lukaszewski AJ, Dolezel J. 2008. Meiotic behaviour of individual chromosomes of Festuca pratensis in tetraploid Lolium multiflorum. Chromosome Research 16, 987–998. PubMed

Labani R, Elkington R. 1987. Nuclear DNA variation in the genus Allium L. (Liliaceae). Heredity 59, 119–128.

Laurie DA, Hultén MA. 1985. Further studies on bivalent chiasma frequency in human males with normal karyotypes. Annals of Human Genetics 49, 189–201. PubMed

Lawrie NM, Tease C, Hultén MA. 1995. Chiasma frequency, distribution and interference maps of mouse autosomes. Chromosoma 104, 308–314. PubMed

Li Q, Saito TT, Martinez-Garcia M, Deshong AJ, Nadarajan S, Lawrence KS, Checchi PM, Colaiacovo MP, Engebrecht J. 2018. The tumor suppressor BRCA1–BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans. PLoS Genetics 14, e1007701. PubMed PMC

Li X, Li L, Yan J. 2015. Dissecting meiotic recombination based on tetrad analysis by single-microspore sequencing in maize. Nature Communications 6, 6648. PubMed PMC

Lim EC, Kim J, Park J, et al. . 2020. DeepTetrad: high-throughput image analysis of meiotic tetrads by deep learning in Arabidopsis thaliana. The Plant Journal 101, 473–483. PubMed

Lindegren CC, Lindegren G. 1942. Locally specific patterns of chromatid and chromosome interference in Neurospora. Genetics 27, 1–24. PubMed PMC

Lukaszewski AJ 2008. Unexpected behavior of an inverted rye chromosome arm in wheat. Chromosoma 117, 569–578. PubMed

Lukaszewski AJ, Curtis CA. 1993. Physical distribution of recombination in B-genome chromosomes of tetraploid wheat. Theoretical and Applied Genetics 86, 121–127. PubMed

Lukaszewski AJ, Kopecky D, Linc G. 2012. Inversions of chromosome arms 4AL and 2BS in wheat invert the patterns of chiasma distribution. Chromosoma 121, 201–208. PubMed

Lukaszewski AJ, Lapinski B, Rybka K. 2005. Limitations of in situ hybridization with total genomic DNA in routine screening for alien introgressions in wheat. Cytogenetic and Genome Research 109, 373–377. PubMed

Malkova A, Swanson J, German M, McCusker JH, Housworth EA, Stahl FW, Haber JE. 2004. Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168, 49–63. PubMed PMC

Martins LDV, Yu F, Zhao H, et al. . 2019. Meiotic crossovers characterized by haplotype-specific chromosome painting in maize. Nature Communications 10, 4604. PubMed PMC

Masoudi-Nejad A, Nasuda S, McIntosh RA, Endo TR. 2002. Transfer of rye chromosome segments to wheat by a gametocidal system. Chromosome Research 10, 349–357. PubMed

Mather K 1938. Crossing-over. Biological Reviews 13, 252–292.

Meneely PM, Farago AF, Kauffman TM. 2002. Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans. Genetics 162, 1169–1177. PubMed PMC

Mercier R, Jolivet S, Vezon D, et al. . 2005. Two meiotic crossover classes cohabit in Arabidopsis. Current Biology 15, 692–701. PubMed

Modliszewski JL, Wang H, Albright AR, Lewis SM, Bennett AR, Huang J, Ma H, Wang Y, Copenhaver GP. 2018. Elevated temperature increases meiotic crossover frequency via the interfering (Type I) pathway in Arabidopsis thaliana. PLoS Genetics 14, e1007384. PubMed PMC

Muller HJ 1916. The mechanism of crossing-over. The American Naturalist 50, 193–221.

Nambiar M, Chuang YC, Smith GR. 2019. Distributing meiotic crossovers for optimal fertility and evolution. DNA Repair 81, 102648. PubMed PMC

Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FC. 2011. Pathways to meiotic recombination in Arabidopsis thaliana. New Phytologist 190, 523–544. PubMed

Otto SP, Payseur BA. 2019. Crossover interference: shedding light on the evolution of recombination. Annual Review of Genetics 53, 19–44. PubMed PMC

Peng J, Korol AB, Fahima T, Röder MS, Ronin YI, Li YC, Nevo E. 2000. Molecular genetic maps in wild emmer wheat, Triticum dicoccoides: genome-wide coverage, massive negative interference, and putative quasi-linkage. Genome Research 10, 1509–1531. PubMed PMC

Perkins DD 1962. The frequency in Neurospora tetrads of multiple exchanges within short intervals. Genetical Research 3, 315–327.

Phillips D, Wnetrzak J, Nibau C, Barakate A, Ramsay L, Wright F, Higgins JD, Perry RM, Jenkins G. 2013. Quantitative high resolution mapping of HvMLH3 foci in barley pachytene nuclei reveals a strong distal bias and weak interference. Journal of Experimental Botany 64, 2139–2154. PubMed PMC

Portin P 2012. Further evidence for the theory that crossover interference in Drosophila melanogaster is dependent on genetic rather than physical distance between adjacent crossover points. Open Journal of Genetics 02, 155–162.

R Core Team 2019. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Säll T, Bengtsson BO. 1989. Apparent negative interference due to variation in recombination frequencies. Genetics 122, 935–942. PubMed PMC

Scholten OE, van Kaauwen MP, Shahin A, Hendrickx PM, Keizer LC, Burger K, van Heusden AW, van der Linden CG, Vosman B. 2016. SNP-markers in Allium species to facilitate introgression breeding in onion. BMC Plant Biology 16, 187. PubMed PMC

Sekhon JS 2011. Multivariate and propensity score matching software with automated balance optimization: the matching package for R. Journal of Statistical Software 42, 1–52.

Shen P, Huang HV. 1986. Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112, 441–457. PubMed PMC

Shen P, Huang HV. 1989. Effect of base pair mismatches on recombination via the RecBCD pathway. Molecular & General Genetics 218, 358–360. PubMed

Snow R 1979. Maximum likelihood estimation of linkage and interference from tetrad data. Genetics 92, 231–245. PubMed PMC

Smith GR, Nambiar M. 2020. New solutions to old problems: molecular mechanisms of meiotic crossover control. Trends in Genetics 36, 337–346. PubMed PMC

Strickland WN 1958. An analysis of interference in Aspergillus nidulans. Proceedings of the Royal Society B: Biological Sciences 149, 82–101. PubMed

Strickland WN 1961. Tetrad analysis of short chromosome regions of Neurospora crassa. Genetics 46, 1125–1141. PubMed PMC

Sturtevant AH 1913. A third group of linked genes in Drosophila ampelophila. Science 37, 990–992. PubMed

Teuscher F, Brockmann GA, Rudolph PE, Swalve HH, Guiard V. 2000. Models for chromatid interference with applications to recombination data. Genetics 156, 1449–1460. PubMed PMC

Wang P, Jiang L, Ye M, Zhu X, Wu R. 2019. The genomic landscape of crossover interference in the desert tree Populus euphratica. Frontiers in Genetics 10, 440. PubMed PMC

Wang Y, Copenhaver GP. 2018. Meiotic recombination: mixing it up in plants. Annual Review of Plant Biology 69, 577–609. PubMed

Whitehouse HLK 1958. Use of loosely linked genes to estimate chromatid interference by tetrad analysis. Nature 182, 1173–1174.

Zhang L, Kim KP, Kleckner NE, Storlazzi A. 2011. Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. Proceedings of the National Academy of Sciences, USA 108, 20036–20041. PubMed PMC

Zhao H, McPeek MS, Speed TP. 1995b Statistical analysis of chromatid interference. Genetics 139, 1057–1065. PubMed PMC

Zhao H, Speed TP, McPeek MS. 1995a Statistical analysis of crossover interference using the chi-square model. Genetics 139, 1045–1056. PubMed PMC

Zickler D, Kleckner N. 2016. A few of our favorite things: pairing, the bouquet, crossover interference and evolution of meiosis. Seminars in Cell & Developmental Biology 54, 135–148. PubMed PMC

Proportion of parental genomes in hybrids Allium cepa × A. roylei determines which one becomes dominant

Genome Dominance in Allium Hybrids (A. cepa × A. roylei)