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

Author:

Ilyin Artem A1,Kononkova Anna D23,Golova Anastasia V2,Shloma Viktor V4,Olenkina Oxana M1,Nenasheva Valentina V1,Abramov Yuri A1,Kotov Alexei A1,Maksimov Daniil A4,Laktionov Petr P45,Pindyurin Alexey V4,Galitsyna Aleksandra A2ORCID,Ulianov Sergey V67ORCID,Khrameeva Ekaterina E2,Gelfand Mikhail S23,Belyakin Stepan N45,Razin Sergey V67ORCID,Shevelyov Yuri Y1ORCID

Affiliation:

1. Institute of Molecular Genetics of National Research Centre “Kurchatov Institute”, Moscow 123182, Russia

2. Skolkovo Institute of Science and Technology, Skolkovo 143026, Russia

3. A.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow 127051, Russia

4. Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia

5. Novosibirsk State University, Novosibirsk 630090, Russia

6. Institute of Gene Biology, Russian Academy of Sciences, Moscow119334, Russia

7. Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119992, Russia

Abstract

Abstract 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.

Funder

Russian Foundation for Basic Research

Russian Program for Basic Research

Ministry of Education and Science of Russian Federation

Russian Science Foundation

Interdisciplinary Scientific and Educational School of Moscow University

Publisher

Oxford University Press (OUP)

Subject

Genetics

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