TY - JOUR

T1 - Comparison of genome architecture at two stages of male germline cell differentiation in Drosophila

AU - Ilyin, Artem A.

AU - Kononkova, Anna D.

AU - Golova, Anastasia

AU - Shloma, Viktor V.

AU - Olenkina, Oxana M.

AU - Nenasheva, Valentina V.

AU - Abramov, Yuri A.

AU - Kotov, Alexei A.

AU - Maksimov, Daniil A.

AU - Laktionov, Petr P.

AU - Pindyurin, Alexey

AU - Galitsyna, Aleksandra A.

AU - Ulianov, Sergey

AU - Khrameeva, Ekaterina E.

AU - Gelfand, Mikhail S.

AU - Belyakin, Stepan N.

AU - Razin, Sergey

AU - Shevelyov, Yuri Y.

N1 - Funding Information: Russian Foundation for Basic Research [17-00-00179 to S.V.R., 17-00-00180 to M.S.G., 17-00-00181 to S.N.B., 17- 00-00182 to Y.Y.S., 17-00-00183 to S.V.R., 16-04-01764 to O.M.O., 18-34-00140 to A.A.I., 18-29-13011 to M.S.G.]; Russian Program for Basic Research [0310-2019-0005 to S.N.B.]; Ministry of Education and Science of Russian Federation [14.Y26.31.0024 to S.N.B.]; Russian Science Foundation [21-64-00001 to S.V.U. and S.V.R.]; Interdisciplinary Scientific and Educational School of Moscow University 'Molecular Technologies of the Living Systems and Synthetic Biology' [to S.V.U. and S.V.R.]. Funding for open access charge: internal funding.

PY - 2022/4/8

Y1 - 2022/4/8

N2 - Eukaryotic chromosomes are spatially segregated into topologically associating domains (TADs). Some TADs are attached to the nuclear lamina (NL) through lamina-associated domains (LADs). Here, we identified LADs and TADs at two stages of Drosophila spermatogenesis - in bamΔ86 mutant testes which is the commonly used model of spermatogonia (SpG) and in larval testes mainly filled with spermatocytes (SpCs). We found that initiation of SpC-specific transcription correlates with promoters' detachment from the NL and with local spatial insulation of adjacent regions. However, this insulation does not result in the partitioning of inactive TADs into sub-TADs. We also revealed an increased contact frequency between SpC-specific genes in SpCs implying their de novo gathering into transcription factories. In addition, we uncovered the specific X chromosome organization in the male germline. In SpG and SpCs, a single X chromosome is stronger associated with the NL than autosomes. Nevertheless, active chromatin regions in the X chromosome interact with each other more frequently than in autosomes. Moreover, despite the absence of dosage compensation complex in the male germline, randomly inserted SpG-specific reporter is expressed higher in the X chromosome than in autosomes, thus evidencing that non-canonical dosage compensation operates in SpG.

AB - Eukaryotic chromosomes are spatially segregated into topologically associating domains (TADs). Some TADs are attached to the nuclear lamina (NL) through lamina-associated domains (LADs). Here, we identified LADs and TADs at two stages of Drosophila spermatogenesis - in bamΔ86 mutant testes which is the commonly used model of spermatogonia (SpG) and in larval testes mainly filled with spermatocytes (SpCs). We found that initiation of SpC-specific transcription correlates with promoters' detachment from the NL and with local spatial insulation of adjacent regions. However, this insulation does not result in the partitioning of inactive TADs into sub-TADs. We also revealed an increased contact frequency between SpC-specific genes in SpCs implying their de novo gathering into transcription factories. In addition, we uncovered the specific X chromosome organization in the male germline. In SpG and SpCs, a single X chromosome is stronger associated with the NL than autosomes. Nevertheless, active chromatin regions in the X chromosome interact with each other more frequently than in autosomes. Moreover, despite the absence of dosage compensation complex in the male germline, randomly inserted SpG-specific reporter is expressed higher in the X chromosome than in autosomes, thus evidencing that non-canonical dosage compensation operates in SpG.

KW - CHROMATIN-ASSOCIATED PROTEIN

KW - NUCLEAR LAMINA INTERACTIONS

KW - HISTONE H4 ACETYLATION

KW - BAG-OF-MARBLES

KW - DOSAGE COMPENSATION

KW - PHASE-SEPARATION

KW - PERICENTRIC HETEROCHROMATIN

KW - CHROMOSOME TOPOLOGY

KW - ACTIVE CHROMATIN

KW - X-CHROMOSOME

KW - Male

KW - Germ Cells

KW - Dosage Compensation, Genetic

KW - Drosophila/genetics

KW - Animals

KW - Chromatin/genetics

KW - Cell Differentiation/genetics

UR - http://www.scopus.com/inward/record.url?scp=85128181922&partnerID=8YFLogxK

U2 - 10.1093/nar/gkac109

DO - 10.1093/nar/gkac109

M3 - Article

C2 - 35166842

VL - 50

SP - 3203

EP - 3225

JO - Nucleic Acids Research

JF - Nucleic Acids Research

SN - 0305-1048

IS - 6

ER -