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Originally published as Genetics Published Articles Ahead of Print on December 6, 2006.

Genetics, Vol. 175, 609-620, February 2007, Copyright © 2007
doi:10.1534/genetics.106.062133

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The SU(VAR)3-9/HP1 Complex Differentially Regulates the Compaction State and Degree of Underreplication of X Chromosome Pericentric Heterochromatin in Drosophila melanogaster

Olga V. Demakova, Galina V. Pokholkova, Tatyana D. Kolesnikova, Sergey A. Demakov, Eugenia N. Andreyeva, Elena S. Belyaeva and Igor F. Zhimulev1

Laboratory of Molecular Cytogenetics, Institute of Cytology and Genetics, Russian Academy of Sciences, Novosibirsk 630090, Russia

1 Corresponding author: Institute of Cytology and Genetics, Russian Academy of Sciences, 10 Lavrentiev Ave., Novosibirsk 630090, Russia.
E-mail: zhimulev{at}bionet.nsc.ru

In polytene chromosomes of Drosophila melanogaster, regions of pericentric heterochromatin coalesce to form a compact chromocenter and are highly underreplicated. Focusing on study of X chromosome heterochromatin, we demonstrate that loss of either SU(VAR)3-9 histone methyltransferase activity or HP1 protein differentially affects the compaction of different pericentric regions. Using a set of inversions breaking X chromosome heterochromatin in the background of the Su(var)3-9 mutations, we show that distal heterochromatin (blocks h26–h29) is the only one within the chromocenter to form a big "puff"-like structure. The "puffed" heterochromatin has not only unique morphology but also very special protein composition as well: (i) it does not bind proteins specific for active chromatin and should therefore be referred to as a pseudopuff and (ii) it strongly associates with heterochromatin-specific proteins SU(VAR)3-7 and SUUR, despite the fact that HP1 and HP2 are depleted particularly from this polytene structure. The pseudopuff completes replication earlier than when it is compacted as heterochromatin, and underreplication of some DNA sequences within the pseudopuff is strongly suppressed. So, we show that pericentric heterochromatin is heterogeneous in its requirement for SU(VAR)3-9 with respect to the establishment of the condensed state, time of replication, and DNA polytenization.




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