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. 2011;6(10):e25960.
doi: 10.1371/journal.pone.0025960. Epub 2011 Oct 11.

Identical functional organization of nonpolytene and polytene chromosomes in Drosophila melanogaster

Tatyana Yu Vatolina  1 , Lidiya V Boldyreva, Olga V Demakova, Sergey A Demakov, Elena B Kokoza, Valeriy F Semeshin, Vladimir N Babenko, Fedor P Goncharov, Elena S Belyaeva, Igor F Zhimulev
Affiliations

Identical functional organization of nonpolytene and polytene chromosomes in Drosophila melanogaster

Tatyana Yu Vatolina et al. PLoS One. 2011.

Erratum in

  • PLoS One. 2011;6(11). doi:10.1371/annotation/45b44e2a-c751-418b-bbb7-7023998abdfc

Abstract

Salivary gland polytene chromosomes demonstrate banding pattern, genetic meaning of which is an enigma for decades. Till now it is not known how to mark the band/interband borders on physical map of DNA and structures of polytene chromosomes are not characterized in molecular and genetic terms. It is not known either similar banding pattern exists in chromosomes of regular diploid mitotically dividing nonpolytene cells. Using the newly developed approach permitting to identify the interband material and localization data of interband-specific proteins from modENCODE and other genome-wide projects, we identify physical limits of bands and interbands in small cytological region 9F13-10B3 of the X chromosome in D. melanogaster, as well as characterize their general molecular features. Our results suggests that the polytene and interphase cell line chromosomes have practically the same patterns of bands and interbands reflecting, probably, the basic principle of interphase chromosome organization. Two types of bands have been described in chromosomes, early and late-replicating, which differ in many aspects of their protein and genetic content. As appeared, origin recognition complexes are located almost totally in the interbands of chromosomes.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Comparison of several Electron Microscope sections of the region 9F11-12 – 10B (A, B) with revised Bridges map
(C). Vertical lines connect homologous bands. Scale represents 1 µm.
Figure 2
Figure 2. Localization of proteins and DNA elements in 9F13 – 10B3 region of nonpolytene chromosomes (according to data of modENCODE).
The positions of proteins were located as described in Material and Methods. A - physical map of DNA; positions of v and sev genes are taken from FlyBase, arrows 1–4 indicate position of probes for FISH on physical map. B - P-elements density in the region calculated as number of insertions per 1 kb in 10 kb interval (data on insertions are taken from FlyBase) C - interband specific and active chromatin specific proteins in S2 cells , D - DNase I hypersensitivity sites (DHS) in S2, BG3 and Kc cells E - ORC2-binding sites in S2, BG3 and Kc cultural and salivary gland cells F - histone H1 dips localization in Kc cells G - histone H3.3 localization in S2 cells (modENCODE, Henikoff group) H - 30 chromatin states in BG3 and S2 cells , and 5 chromatin types in Kc cells I - nucleosome turnover dynamics in S2 cells , J - D1 localization in Kc cells , K - SUUR localization in Kc cells , L - Lamin localization in Kc cells M - early (up) and late (down) replication in S2, Kc and BG3 cells N - gene density (number of genes per 10 kb of DNA) .
Figure 3
Figure 3. Localization in polytene chromosomes of DNA fragments, which according to modEncode data are located in the predicted interbands flanking the 10A1–2 and 10B1–2 bands of the nonpolytene chromosomes.
Banding pattern in the region under phase contrast microscope (A, D), pairwise FISH mapping of DNA fragments, limiting the bands 10A1–2 (probes CG15208 and Vago) (B, C) and 10B1–2 (CG32668 and l(1)10Bb) (E, F).
Figure 4
Figure 4. Colocalization of DNA probes limiting the 10A1–2 band with the Chriz/CHRO protein.
Localization of the Chriz protein in the 10A–B region (A–C); the bands in the region under phase contrast (A), the Chriz/CHRO protein, asterisk points to the interband 9F13/10A1–2 B), match of Chriz/CHRO location and phase contrast (c), colocalization of the DNA probe CG15208, limiting distal side of the band 10A1–2 and Chriz/CHRO protein (D–F); colocalization of the DNA probe Vago, limiting proximal side of the band 10A1–2 and Chriz/CHRO protein on stretched chromosomes (G–I). Bar represents 2 µm.
Figure 5
Figure 5. Colocalization of DNA probes limiting the band 10B1–2, and Chriz/CHRO protein.
Banding pattern in the region 10A–B (DAPI) (A), immunostaining of Chriz/CHRO and FISH of the DNA probe (A), immunostaining of Chriz/CHRO, FISH of the DNA probe and DAPI (C). Bar represents 5 µm.
Figure 6
Figure 6. Relation of genetic map, and band/interband pattern in the region 9F13 – 10B3.
A - predicted bands B - FlyBase genes C – 30 chromatin states in BG3 and S2 cells D - DNase I hypersensitivity sites (DHS) in S2, BG3 and Kc cells E - ORC-binding sites in S2, BG3 and Kc cells F – Nucleosome Density (modENCODE, Henikoff group) G - active chromatin specific and - interbands specific proteins. Predicted interbands (dotted vertical lines are according to peaks in distribution of corresponding elements, solid lines reflect the edges of distributions of different characteristics).
Figure 7
Figure 7. Comparison of extents of band/interbands in polytene chromosomes according to Flybase r5.25 (A, B) and to the data of this study (C).
Physical DNA map is situated between 10792800 and 11220400 positions of the map of Flybase.
See this image and copyright information in PMC

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