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Heterochromatin-binding proteins regulate male X polytene chromosome morphology and dosage compensation: an evidence from a variegated rearranged strain [In (1)BM 2,(rv)] and its interactions with hyperploids and mle mutation in Drosophila melanogaster

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Abstract

The reinverted In(1)BM 2 strain of Drosophila melanogaster alter the global architecture of the male X chromosome in ~30 % salivary nuclei, while rest of the nuclei show a perfectly normal haplo-X morphology. We show that, in the aberrant morphology of male X chromosome bearing nuclei, the chromocenter was grossly abnormal, exhibiting either loose morphology or reduced in size. Rearing flies at lower temperature (16 °C) enhanced both frequency and severity of variegated phenotype in the X chromosome and chromocenter. In variegated X chromosome, many intercalary heterochromatic sites showed cytologically visible link (ectopic pairing) at higher frequencies than the X chromosome of Oregon R males. When duplication for the segment 18A-20F, 16F-20F, 8C-20F and 1A-17F were combined with rearranged X chromosome of male, the rearranged X chromosome ceases to show variegating phenotype. Similarly, when a seperate maleless mutation (either mle 1 or mle ts—a dosage compensation regulatory gene mutation) was introduced in homozygous condition in the rearranged strain, variegated phenotypes of the male X chromosome were not only modified, bloated appearance of male X chromosome was also partially reduced. On the basis of the results, we suggest that (1) like many other re-arrangements involving pericentric heterochromatin, reinverted In(1)BM 2 X chromosome induce long-distance heterochromatin spreading into juxtraposed euchromatic sequences of the X chromosome, (2) X limited distribution of intercalary heterochromatin (either SR sequences or transposable elements bearing heterochromatic sites) function as relay elements for ‘spreading’ of heterochromatic factors to the entire X chromosome, and (3) the termination of heterochromatin spreading on the male X chromosome by different genomic context indicate that there is an inherent mechanism for movement of heterochromatin-binding proteins in the X chromosome from one class of site to another and back, for regulation of X chromosome organization.

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Acknowledgments

We are thankful to Bloomington Drosophila stock center, for generously sending the Drosophila stocks. The work has been supported by UGC Emeritus Fellowship [Sanction No. F. 6-6/2015-17/EMERITUS-2015-17-GEN-5478(SA-II) dt.21.09.2015] to RNC.

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The paper is dedicated to Prof. A. K. Sharma, as inspirational and integrative leader in the field of chromosome research.

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Chatterjee, R.N., Chatterjee, R. & Ghosh, S. Heterochromatin-binding proteins regulate male X polytene chromosome morphology and dosage compensation: an evidence from a variegated rearranged strain [In (1)BM 2,(rv)] and its interactions with hyperploids and mle mutation in Drosophila melanogaster . Nucleus 59, 141–154 (2016). https://doi.org/10.1007/s13237-016-0177-0

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