{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,16]],"date-time":"2026-07-16T21:58:26Z","timestamp":1784239106308,"version":"3.55.0"},"reference-count":44,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2015,8,20]],"date-time":"2015-08-20T00:00:00Z","timestamp":1440028800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2015,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>We designed a system to determine whether dicentric chromosomes in Drosophila melanogaster break at random or at preferred sites. Sister chromatid exchange in a Ring-X chromosome produced dicentric chromosomes with two bridging arms connecting segregating centromeres as cells divide. This double bridge can break in mitosis. A genetic screen recovered chromosomes that were linearized by breakage in the male germline. Because the screen required viability of males with this X chromosome, the breakpoints in each arm of the double bridge must be closely matched to produce a nearly euploid chromosome. We expected that most linear chromosomes would be broken in heterochromatin because there are no vital genes in heterochromatin, and breakpoint distribution would be relatively unconstrained. Surprisingly, approximately half the breakpoints are found in euchromatin, and the breakpoints are clustered in just a few regions of the chromosome that closely match regions identified as intercalary heterochromatin. The results support the Laird hypothesis that intercalary heterochromatin can explain fragile sites in mitotic chromosomes, including fragile X. Opened rings also were recovered after male larvae were exposed to X-rays. This method was much less efficient and produced chromosomes with a strikingly different array of breakpoints, with almost all located in heterochromatin. A series of circularly permuted linear X chromosomes was generated that may be useful for investigating aspects of chromosome behavior, such as crossover distribution and interference in meiosis, or questions of nuclear organization and function.<\/jats:p>","DOI":"10.1534\/genetics.115.181156","type":"journal-article","created":{"date-parts":[[2015,8,21]],"date-time":"2015-08-21T02:49:11Z","timestamp":1440125351000},"page":"563-572","source":"Crossref","is-referenced-by-count":11,"title":["Preferential Breakpoints in the Recovery of Broken Dicentric Chromosomes in<i>Drosophila melanogaster<\/i>"],"prefix":"10.1093","volume":"201","author":[{"given":"Hunter","family":"Hill","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kent G","family":"Golic","sequence":"additional","affiliation":[{"name":"Department of Biology , University of Utah, Salt Lake City, Utah 84112"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2015,8,20]]},"reference":[{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1093\/genetics\/148.2.775","article-title":"The transmission of fragmented chromosomes in Drosophila melanogaster.","volume":"148","author":"Ahmad","year":"1998","journal-title":"Genetics"},{"key":"2023030906395528100_","volume-title":"Drosophila: A Laboratory Handbook","author":"Ashburner","year":"2005"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1534\/genetics.112.138818","article-title":"Multiple pathways suppress telomere addition to DNA breaks in the Drosophila germline.","volume":"191","author":"Beaucher","year":"2012","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0030035","article-title":"Late replication domains in polytene and non-polytene cells of Drosophila melanogaster.","author":"Belyaeva","year":"2012"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1093\/genetics\/43.1.48","article-title":"A comparison of crossover relationships in a Drosophila ring X chromosome and a rod X derivative.","volume":"43","author":"Bender","year":"1958","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"1758","DOI":"10.1073\/pnas.87.5.1758","article-title":"Chromosome ends in Drosophila without telomeric DNA sequences.","volume":"87","author":"Biessmann","year":"1990","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1093\/oxfordjournals.jhered.a104022","article-title":"Salivary chromosome maps.","volume":"26","author":"Bridges","year":"1935","journal-title":"J. Hered."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/BF02989035","article-title":"Dominant lethals and chromosome breaks in ring X-chromosomes of Drosophila melanogaster.","volume":"7","author":"Catcheside","year":"1945","journal-title":"J. Genet."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1534\/genetics.110.123265","article-title":"A new resource for characterizing X-linked genes in Drosophila melanogaster: systematic coverage and subdivision of the X chromosome with nested, Y-linked duplications.","volume":"186","author":"Cook","year":"2010","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"2263","DOI":"10.1242\/dev.125.12.2263","article-title":"Identifying loci required for follicular patterning using directed mosaics.","volume":"125","author":"Duffy","year":"1998","journal-title":"Development"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1534\/genetics.113.161075","article-title":"Heterochromatin position effects on circularized sex chromosomes cause filicidal embryonic lethality in Drosophila melanogaster.","volume":"196","author":"Ferree","year":"2014","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1038\/emboj.2009.394","article-title":"HipHop interacts with HOAP and HP1 to protect Drosophila telomeres in a sequence-independent manner.","volume":"29","author":"Gao","year":"2010","journal-title":"EMBO J."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1007\/BF00285858","article-title":"Cytological and genetic analysis of the Y chromosome of Drosophila melanogaster.","volume":"88","author":"Gatti","year":"1983","journal-title":"Chromosoma"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/0092-8674(89)90033-0","article-title":"The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome.","volume":"59","author":"Golic","year":"1989","journal-title":"Cell"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1007\/s00412-010-0297-2","article-title":"A simple and rapid method for constructing ring-X chromosomes in Drosophila melanogaster.","volume":"120","author":"Golic","year":"2010","journal-title":"Chromosoma"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"3665","DOI":"10.1093\/nar\/25.18.3665","article-title":"FLP-mediated DNA mobilization to specific target sites in Drosophila chromosomes.","volume":"25","author":"Golic","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1007\/BF00328223","article-title":"Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila melanogaster.","volume":"91","author":"Hammond","year":"1985","journal-title":"Chromosoma"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"4587","DOI":"10.1073\/pnas.94.9.4587","article-title":"A variable domain of delayed replication in FRAXA fragile X chromosomes: X inactivation-like spread of late replication.","volume":"94","author":"Hansen","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1016\/0092-8674(93)90365-W","article-title":"Association of fragile X syndrome with delayed replication of the FMR1 gene.","volume":"73","author":"Hansen","year":"1993","journal-title":"Cell"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1093\/genetics\/40.6.951","article-title":"The behavior of an unstable ring chromosome of Drosophila melanogaster.","volume":"40","author":"Hinton","year":"1955","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1073\/pnas.25.11.571","article-title":"Distribution of induced breaks along the X-chromosome of Drosophila melanogaster.","volume":"25","author":"Kaufmann","year":"1939","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/0168-9525(87)90268-X","article-title":"Fragile sites in human chromosomes as regions of late-replicating DNA.","volume":"3","author":"Laird","year":"1987","journal-title":"Trends Genet."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1002\/ajmg.1320300170","article-title":"Intercalary heterochromatin of Drosophila as a potential model for human fragile sites.","volume":"30","author":"Laird","year":"1988","journal-title":"Am. J. Med. Genet."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1007\/BF00294779","article-title":"Three euchromatic DNA sequences under-replicated in polytene chromosomes of Drosophila are localized in constrictions and ectopic fibers.","volume":"95","author":"Lamb","year":"1987","journal-title":"Chromosoma"},{"key":"2023030906395528100_","first-page":"32","article-title":"A photographic representation and interpretation of the polytene chromosomes of Drosophila melanogaster salivary glands","volume-title":"The Genetics and Biology of Drosophila","author":"Lefevre","year":"1976"},{"key":"2023030906395528100_","first-page":"505","article-title":"Ring chromosomes and radiation induced chromosome loss","volume-title":"The Genetics and Biology of Drosophila","author":"Leigh","year":"1976"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1016\/0092-8674(89)90112-8","article-title":"Viable deletions of a telomere from a Drosophila chromosome.","volume":"58","author":"Levis","year":"1989","journal-title":"Cell"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1101\/gad.254664.114","article-title":"Cytokinesis breaks dicentric chromosomes preferentially at pericentromeric regions and telomere fusions.","volume":"29","author":"Lopez","year":"2015","journal-title":"Genes Dev."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"6090","DOI":"10.1073\/pnas.81.19.6090","article-title":"mu-2: mutator gene in Drosophila that potentiates the induction of terminal deficiencies.","volume":"81","author":"Mason","year":"1984","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1007\/s004120050358","article-title":"Broken chromosomal ends can be elongated by conversion in Drosophila melanogaster.","volume":"108","author":"Mikhailovsky","year":"1999","journal-title":"Chromosoma"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1093\/genetics\/18.3.250","article-title":"A closed X chromosome in Drosophila melanogaster.","volume":"18","author":"Morgan","year":"1933","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1101\/gad.571510","article-title":"Dicentric breakage at telomere fusions.","volume":"24","author":"Pobiega","year":"2010","journal-title":"Genes Dev."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.yexcr.2004.09.001","article-title":"When, where and how the bridge breaks: anaphase bridge breakage plays a crucial role in gene amplification and HSR generation.","volume":"302","author":"Shimizu","year":"2005","journal-title":"Exp. Cell Res."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1534\/genetics.113.150144","article-title":"Nonrandom distribution of interhomolog recombination events induced by breakage of a dicentric chromosome in Saccharomyces cerevisiae.","volume":"194","author":"Song","year":"2013","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1093\/genetics\/102.2.245","article-title":"Filicidal ring-Y chromosomes in D. melanogaster.","volume":"102","author":"Stone","year":"1982","journal-title":"Genetics"},{"key":"2023030906395528100_","first-page":"407","article-title":"Large domains of apparent delayed replication timing associated with triplet repeat expansion at FRAXA and FRAXE.","volume":"59","author":"Subramanian","year":"1996","journal-title":"Am. J. Hum. Genet."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"1821","DOI":"10.1534\/genetics.108.093625","article-title":"Telomere loss provokes multiple pathways to apoptosis and produces genomic instability in Drosophila melanogaster.","volume":"180","author":"Titen","year":"2008","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1534\/genetics.109.109934","article-title":"Healing of euchromatic chromosome breaks by efficient de novo telomere addition in Drosophila melanogaster.","volume":"184","author":"Titen","year":"2010","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1004130","article-title":"Chk2 and P53 regulate the transmission of healed chromosomes in the Drosophila male germline.","volume":"10","author":"Titen","year":"2014","journal-title":"PLoS Genet."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1093\/genetics\/133.2.347","article-title":"Preferential transposition of Drosophila P elements to nearby chromosomal sites.","volume":"133","author":"Tower","year":"1993","journal-title":"Genetics"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"8116","DOI":"10.1073\/pnas.85.21.8116","article-title":"A spontaneously opened ring chromosome of Drosophila melanogaster has acquired He-T DNA sequences at both new telomeres.","volume":"85","author":"Traverse","year":"1988","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/S0960-9822(98)70091-0","article-title":"Regulation of zygotic gene expression in Drosophila primordial germ cells.","volume":"8","author":"Van Doren","year":"1998","journal-title":"Curr. Biol."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"1840","DOI":"10.1101\/gad.245811.114","article-title":"Incomplete replication generates somatic DNA alterations within Drosophila polytene salivary gland cells.","volume":"28","author":"Yarosh","year":"2014","journal-title":"Genes Dev."},{"key":"2023030906395528100_","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1007\/BF00338489","article-title":"Intercalary heterochromatin in Drosophila. I. Localization and general characteristics.","volume":"878","author":"Zhimulev","year":"1982","journal-title":"Chromosoma"}],"container-title":["Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/201\/2\/563\/49458519\/genetics0563.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/201\/2\/563\/49458519\/genetics0563.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,13]],"date-time":"2023-08-13T09:09:58Z","timestamp":1691917798000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/genetics\/article\/201\/2\/563\/5930115"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,8,20]]},"references-count":44,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2015,8,20]]},"published-print":{"date-parts":[[2015,10,1]]}},"URL":"https:\/\/doi.org\/10.1534\/genetics.115.181156","relation":{},"ISSN":["1943-2631"],"issn-type":[{"value":"1943-2631","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2015,10,1]]},"published":{"date-parts":[[2015,8,20]]}}}