{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,6,5]],"date-time":"2025-06-05T04:07:40Z","timestamp":1749096460365,"version":"3.41.0"},"reference-count":28,"publisher":"Institute of Cytology and Genetics, SB RAS","issue":"3","license":[{"start":{"date-parts":[[2025,6,3]],"date-time":"2025-06-03T00:00:00Z","timestamp":1748908800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/vavilov.elpub.ru\/jour\/about\/editorialPolicies#openAccessPolicy"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Vestn. VOGiS"],"abstract":"The achaete-scute<\/jats:italic> complex (AS-C<\/jats:italic>) is a locus approximately 90 kbp in length, containing multiple en hancers. The local expression of the achaete<\/jats:italic> and scute<\/jats:italic> genes in proneural clusters of Drosophila melanogaster<\/jats:italic> imaginal discs results in the formation of a well-defined pattern of macrochaetae in adult flies. A wide variety of easily analyzed phenotypes, along with the direct connection between individual regulatory elements and the development of specific setae make this locus a classic model in developmental genetics. One classic AS-C<\/jats:italic> allele is sc<\/jats:italic>8<\/jats:italic>, which arose as a result of the In(1)<\/jats:italic> sc8<\/jats:italic> inversion. One breakpoint of this inversion lies between the ac<\/jats:italic> and sc<\/jats:italic> genes, while the second is in the pericentromeric heterochromatin of chromosome X, within satellite block 1.688. The heterochromatic position of the breakpoint raised the question of whether position effect variegation contributes to the disruption of normal locus function in the In(1)sc<\/jats:italic>8<\/jats:italic> flies. However, conflicting results were obtained. Previously, we found that a secondary inversion, In(1)19EHet<\/jats:italic>, arose spontaneously in one of the stocks of the In(1)sc<\/jats:italic>8<\/jats:italic> BDSC line, transferring most of the heterochromatin from the ac<\/jats:italic> gene to the 19E region of the X chromosome. Here, we demonstrate that the In(1)19EHet<\/jats:italic> inversion leads to complete rescue of the number of posterior supraalar (PSA) and partial rescue of the number of dorsocentral (DC) macrochaetes observed in the original In(1)sc<\/jats:italic>8<\/jats:italic> line. The same rescue of the macrochaetes pattern was observed when the In(1)sc<\/jats:italic>8<\/jats:italic> inversion was introduced into a strain with the Su(var)3-9<\/jats:italic>06 <\/jats:italic>position effect modifier. Combining the inversion with the Rif11<\/jats:sup><\/jats:italic> mutation, a conserved factor determining late replication and underreplication, does not restore the normal pattern of bristles. Our data indicate that the phenotype of flies carrying the In(1)<\/jats:italic> sc8<\/jats:italic> inversion, associated with a disturbance in bristle development, is determined by the effect of heterochromatin on the distal part of the locus. This model can be used to test the influence of various factors on the position effect variegation caused by heterochromatin. Another phenotypic manifestation of In(1)sc<\/jats:italic>8<\/jats:italic>, a decreased proportion of males in the offspring, was independent of the proximity of the distal part of AS-C<\/jats:italic> to heterochromatin and was not affected by the Rif1<\/jats:italic>1<\/jats:italic> mutation.<\/jats:p>","DOI":"10.18699\/vjgb-25-44","type":"journal-article","created":{"date-parts":[[2025,6,4]],"date-time":"2025-06-04T06:35:06Z","timestamp":1749018906000},"page":"414-422","source":"Crossref","is-referenced-by-count":0,"title":["The key role of heterochromatin in the phenotypic manifestation of the In(1)sc8 inversion disrupting the achaete-scute complex in Drosophila melanogaster"],"prefix":"10.18699","volume":"29","author":[{"given":"T. D.","family":"Kolesnikova","sequence":"first","affiliation":[{"name":"Institute of Molecular and Cellular Biology of the Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"M. N.","family":"Balantaeva","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology of the Siberian Branch of the Russian Academy of Sciences"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"G. V.","family":"Pokholkova","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology of the Siberian Branch of the Russian Academy of Sciences"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"O. V.","family":"Antonenko","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology of the Siberian Branch of the Russian Academy of Sciences"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"I. F.","family":"Zhimulev","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology of the Siberian Branch of the Russian Academy of Sciences"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"7950","published-online":{"date-parts":[[2025,6,3]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","unstructured":"Belyaeva E.S., Boldyreva L.V., Volkova E.I., Nanayev R.A., Alekseyenko A.A., Zhimulev I.F. Effect of the Suppressor of Underreplication (SuUR) gene on position-effect variegation silencing in Drosophila melanogaster. Genetics. 2003;165(3):1209-1220. doi 10.1093\/genetics\/165.3.1209","DOI":"10.1093\/genetics\/165.3.1209"},{"key":"ref2","doi-asserted-by":"crossref","unstructured":"Bukharina T.A., Furman D.P. The mechanisms determining bristle pattern in Drosophila melanogaster. Russ J Dev Biol. 2015;46(3): 99-110. doi 10.1134\/S1062360415030029","DOI":"10.1134\/S1062360415030029"},{"key":"ref3","doi-asserted-by":"crossref","unstructured":"Bukharina T.A., Golubyatnikov V.P., Furman D.P. The central regulatory circuit in the gene network controlling the morphogenesis of Drosophila mechanoreceptors: an in silico analysis. Vavilovskii Zhur nal Genet Selektsii = Vavilov J Genet Breed. 2023;27(7):746754. doi 10.18699\/VJGB-23-87","DOI":"10.18699\/VJGB-23-87"},{"key":"ref4","doi-asserted-by":"crossref","unstructured":"Child G. Phenogenetic studies on scute-1 of Drosophila melanogaster. I. The associations between the bristles and the effects of genetic modifiers and temperature. Genetics. 1935;20(2):109-126. doi 10.1093\/genetics\/20.2.109","DOI":"10.1093\/genetics\/20.2.109"},{"key":"ref5","doi-asserted-by":"crossref","unstructured":"Demakova O.V., Pokholkova G.V., Kolesnikova T.D., Demakov S.A., Andreyeva E.N., Belyaeva E.S., Zhimulev I.F. The SU(VAR)3-9\/ HP1 complex differentially regulates the compaction state and degree of underreplication of X chromosome pericentric heterochromatin in Drosophila melanogaster. Genetics. 2007;175(2):609-620. doi 10.1534\/genetics.106.062133","DOI":"10.1534\/genetics.106.062133"},{"key":"ref6","doi-asserted-by":"crossref","unstructured":"Elgin S.C.R., Reuter G. Position-effect variegation, heterochromatin formation, and gene silencing in Drosophila. Cold Spring Harb Perspect Biol. 2013;5(8):a017780. doi 10.1101\/cshperspect.a017780","DOI":"10.1101\/cshperspect.a017780"},{"key":"ref7","doi-asserted-by":"crossref","unstructured":"Furman D.P., Bukharina T.V. The bristle pattern development in Drosophila melanogaster: the prepattern and achaete-scute genes. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov J Genet Breed. 2018; 22(8):1046-1054. doi 10.18699\/VJ18.449","DOI":"10.18699\/VJ18.449"},{"key":"ref8","unstructured":"Furman D.P., Ratner V.A. Investigation of the genetic topography of the scute locus in Drosophila melanogaster. II. Thermal effect of mutation manifestation in homozygotes. Genetika = Genetics ( Moscow). 1977;13(4):667-680 (in Russian)"},{"key":"ref9","doi-asserted-by":"crossref","unstructured":"Garc\u00eda-Bellido A. Genetic analysis of the achaete-scute system of Drosophila melanogaster. Genetics. 1979;91(3):491-520. doi 10.1093\/genetics\/91.3.491","DOI":"10.1093\/genetics\/91.3.491"},{"key":"ref10","doi-asserted-by":"crossref","unstructured":"Gatti M., Pimpinelli S. Functional elements in Drosophila melanogaster heterochromatin. Annu Rev Genet. 1992;26:239-275. doi 10.1146\/annurev.ge.26.120192.001323","DOI":"10.1146\/annurev.genet.26.1.239"},{"key":"ref11","doi-asserted-by":"crossref","unstructured":"Golovnin A., Biryukova I., Romanova O., Silicheva M., Parshikov A., Savitskaya E., Pirrotta V., Georgiev P. An endogenous Su(Hw) insulator separates the yellow gene from the Achaete-scute gene complex in Drosophila. Development. 2003;130(14):3249-3258. doi 10.1242\/dev.00543","DOI":"10.1242\/dev.00543"},{"key":"ref12","doi-asserted-by":"crossref","unstructured":"G\u00f3mez-Skarmeta J.L., Rodr\u00edguez I., Mart\u00ednez C., Cul\u00ed J., Ferr\u00e9s-Marc\u00f3 D., Beamonte D., Modolell J. Cis-regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs. Genes Dev. 1995;9(15):1869-1882. doi 10.1101\/gad.9.15.1869","DOI":"10.1101\/gad.9.15.1869"},{"key":"ref13","doi-asserted-by":"crossref","unstructured":"G\u00f3mez-Skarmeta J.L., Campuzano S., Modolell J. Half a century of neural prepatterning: the story of a few bristles and many genes. Nat Rev Neurosci. 2003;4(7):587-598. doi 10.1038\/nrn1142","DOI":"10.1038\/nrn1142"},{"key":"ref14","doi-asserted-by":"crossref","unstructured":"Held L.I., Jr. Animal Anomalies: What Abnormal Anatomies Reveal about Normal Development. Cambridge: Cambridge University Press, 2021. doi 10.1017\/9781108876612","DOI":"10.1017\/9781108876612"},{"key":"ref15","doi-asserted-by":"crossref","unstructured":"Kolesnikova T.D., Kolodyazhnaya A.V., Pokholkova G.V., Schubert V., Dovgan V.V., Romanenko S.A., Prokopov D.Y., Zhimulev I.F. Effects of mutations in the Drosophila melanogaster Rif1 gene on the replication and underreplication of pericentromeric heterochromatin in salivary gland polytene chromosomes. Cells. 2020;9(6):1501. doi 10.3390\/cells9061501","DOI":"10.3390\/cells9061501"},{"key":"ref16","doi-asserted-by":"crossref","unstructured":"Kolesnikova T.D., Klenov M.S., Nokhova A.R., Lavrov S.A., Pokholkova G.V., Schubert V., Maltseva S.V., Cook K.R., Dixon M.J., Zhimulev I.F. A spontaneous inversion of the X chromosome heterochromatin provides a tool for studying the structure and activity of the nucleolus in Drosophila melanogaster. Cells. 2022;11(23):3872. doi 10.3390\/cells11233872","DOI":"10.3390\/cells11233872"},{"key":"ref17","unstructured":"Lindsley D., Zimm G. The genome of Drosophila melanogaster. San Diego, CA: Academic Press, 1992"},{"key":"ref18","doi-asserted-by":"crossref","unstructured":"Miller D.E., Cook K.R., Yeganeh Kazemi N., Smith C.B., Cockrell A.J., Hawley R.S., Bergman C.M. Rare recombination events generate sequence diversity among balancer chromosomes in Drosophila melanogaster. Proc Natl Acad Sci USA. 2016;113(10):E1352-E1361. doi 10.1073\/pnas.1601232113","DOI":"10.1073\/pnas.1601232113"},{"key":"ref19","unstructured":"Modolell J., Campuzano S. The achaete-scute complex as an integrating device. Int J Dev Biol. 1998;42(3):275-282. doi 10.1387\/IJDB.9654009"},{"key":"ref20","doi-asserted-by":"crossref","unstructured":"Munden A., Rong Z., Sun A., Gangula R., Mallal S., Nordman J.T. Rif1 inhibits replication fork progression and controls DNA copy number in Drosophila. eLife. 2018;7:e39140. doi 10.7554\/eLife.39140","DOI":"10.7554\/eLife.39140"},{"key":"ref21","doi-asserted-by":"crossref","unstructured":"Negre B., Simpson P. Evolution of the achaete-scute complex in insects: convergent duplication of proneural genes. Trends Genet. 2009;25(4):147-152. doi 10.1016\/j.tig.2009.02.001","DOI":"10.1016\/j.tig.2009.02.001"},{"key":"ref22","unstructured":"Ratner V.A., Furman D.P. Investigation of the genetic topography of the scute locus in Drosophila melanogaster. VI. Possible role of chromosome rearrangements and the position effect. Genetika = Genetics (Moscow). 1978;14(9):1662-1664 (in Russian)"},{"key":"ref23","doi-asserted-by":"crossref","unstructured":"Rice C., Beekman D., Liu L., Erives A. The nature, extent, and consequences of genetic variation in the opa repeats of Notch in Drosophila. G3 (Bethesda). 2015;5(11):2405-2419. doi 10.1534\/g3.115.021659","DOI":"10.1534\/g3.115.021659"},{"key":"ref24","doi-asserted-by":"crossref","unstructured":"Richards L., Das S., Nordman J.T. Rif1-dependent control of replication timing. Genes (Basel). 2022;13(3):550. doi 10.3390\/genes 13030550","DOI":"10.3390\/genes13030550"},{"key":"ref25","doi-asserted-by":"crossref","unstructured":"Seller C.A., O\u2019Farrell P.H. Rif1 prolongs the embryonic S phase at the Drosophila mid-blastula transition. PLoS Biol. 2018;16(5): e2005687. doi 10.1371\/journal.pbio.2005687","DOI":"10.1371\/journal.pbio.2005687"},{"key":"ref26","unstructured":"Sidorov B.N. Study of step-allelomorphism in Drosophila melanogaster. Emergence of an allelomorph for scute producing simultaneously hairy wing characters (mutation scute-8). Zhurnal Ekspe rimental\u2019noy Biologii = J Experim Biol. 1931;7(1):28-40 (in Rus sian)"},{"key":"ref27","doi-asserted-by":"crossref","unstructured":"Sreesankar E., Bharathi V., Mishra R.K., Mishra K. Drosophila Rif1 is an essential gene and controls late developmental events by direct interaction with PP1-87B. Sci Rep. 2015;5:10679. doi 10.1038\/srep10679","DOI":"10.1038\/srep10679"},{"key":"ref28","doi-asserted-by":"crossref","unstructured":"Troost T., Schneider M., Klein T. A re-examination of the selection of the sensory organ precursor of the bristle sensilla of Drosophila melanogaster. PLoS Genet. 2015;11:e1004911. doi 10.1371\/journal. pgen.1004911","DOI":"10.1371\/journal.pgen.1004911"}],"container-title":["Vavilov Journal of Genetics and Breeding"],"original-title":[],"link":[{"URL":"https:\/\/vavilov.elpub.ru\/jour\/article\/viewFile\/4607\/1949","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,6,4]],"date-time":"2025-06-04T06:35:32Z","timestamp":1749018932000},"score":1,"resource":{"primary":{"URL":"https:\/\/vavilov.elpub.ru\/jour\/article\/view\/4607"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6,3]]},"references-count":28,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025,6,3]]}},"URL":"https:\/\/doi.org\/10.18699\/vjgb-25-44","relation":{},"ISSN":["2500-3259"],"issn-type":[{"value":"2500-3259","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,3]]}}}