TY - JOUR

T1 - Similarity in replication timing between polytene and diploid cells is associated with the organization of the drosophila genome

AU - Kolesnikova, Tatyana D.

AU - Goncharov, Fedor P.

AU - Zhimulev, Igor F.

N1 - Publisher Copyright: © 2018 Kolesnikova et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2018/4/16

Y1 - 2018/4/16

N2 - Morphologically, polytene chromosomes of Drosophila melanogaster consist of compact “black” bands alternating with less compact “grey” bands and interbands. We developed a comprehensive approach that combines cytological mapping data of FlyBase-annotated genes and novel tools for predicting cytogenetic features of chromosomes on the basis of their protein composition and determined the genomic coordinates for all black bands of polytene chromosome 2R. By a PCNA immunostaining assay, we obtained the replication timetable for all the bands mapped. The results allowed us to compare replication timing between polytene chromosomes in salivary glands and chromosomes from cultured diploid cell lines and to observe a substantial similarity in the global replication patterns at the band resolution level. In both kinds of chromosomes, the intervals between black bands correspond to early replication initiation zones. Black bands are depleted of replication initiation events and are characterized by a gradient of replication timing; therefore, the time of replication completion correlates with the band length. The bands are characterized by low gene density, contain predominantly tissue-specific genes, and are represented by silent chromatin types in various tissues. The borders of black bands correspond well to the borders of topological domains as well as to the borders of the zones showing H3K27me3, SUUR, and LAMIN enrichment. In conclusion, the characteristic pattern of polytene chromosomes reflects partitioning of the Drosophila genome into two global types of domains with contrasting properties. This partitioning is conserved in different tissues and determines replication timing in Drosophila.

AB - Morphologically, polytene chromosomes of Drosophila melanogaster consist of compact “black” bands alternating with less compact “grey” bands and interbands. We developed a comprehensive approach that combines cytological mapping data of FlyBase-annotated genes and novel tools for predicting cytogenetic features of chromosomes on the basis of their protein composition and determined the genomic coordinates for all black bands of polytene chromosome 2R. By a PCNA immunostaining assay, we obtained the replication timetable for all the bands mapped. The results allowed us to compare replication timing between polytene chromosomes in salivary glands and chromosomes from cultured diploid cell lines and to observe a substantial similarity in the global replication patterns at the band resolution level. In both kinds of chromosomes, the intervals between black bands correspond to early replication initiation zones. Black bands are depleted of replication initiation events and are characterized by a gradient of replication timing; therefore, the time of replication completion correlates with the band length. The bands are characterized by low gene density, contain predominantly tissue-specific genes, and are represented by silent chromatin types in various tissues. The borders of black bands correspond well to the borders of topological domains as well as to the borders of the zones showing H3K27me3, SUUR, and LAMIN enrichment. In conclusion, the characteristic pattern of polytene chromosomes reflects partitioning of the Drosophila genome into two global types of domains with contrasting properties. This partitioning is conserved in different tissues and determines replication timing in Drosophila.

KW - Animals

KW - Chromosomes, Insect/chemistry

KW - DNA Replication

KW - DNA Replication Timing/physiology

KW - Diploidy

KW - Drosophila melanogaster/genetics

KW - Genome, Insect

KW - Physical Chromosome Mapping

KW - Polytene Chromosomes/genetics

KW - Salivary Glands/metabolism

KW - GIANT CHROMOSOMES

KW - NUCLEAR LAMINA

KW - DNA-REPLICATION

KW - GENETIC ORGANIZATION

KW - MELANOGASTER GENOME

KW - OVARIAN PSEUDONURSE CELLS

KW - GENERAL-CHARACTERISTICS

KW - INTERCALARY HETEROCHROMATIN

KW - CHROMATIN INTERACTIONS

KW - OTU MUTANTS

UR - http://www.scopus.com/inward/record.url?scp=85045508585&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0195207

DO - 10.1371/journal.pone.0195207

M3 - Article

C2 - 29659604

AN - SCOPUS:85045508585

VL - 13

SP - e0195207

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 4

M1 - 0195207

ER -