Journal of Cell Science, Vol 111, Issue 18 2753-2761, Copyright © 1998 by Company of Biologists

JOURNAL ARTICLES

Dynamics of the sub-nuclear distribution of Modulo and the regulation of position-effect variegation by nucleolus in Drosophila

L Perrin, O Demakova, L Fanti, S Kallenbach, S Saingery, NI Mal'ceva, S Pimpinelli, I Zhimulev and J Pradel
Laboratoire de Genetique et de Physiologie du Developpement, Institut de Biologie du Developpement de Marseille, CNRS/INSERM/Universite de la Mediterranee/AP de Marseille, Campus de Luminy Case 907. 13288 Marseille cedex 9, France.

modulo belongs to the class of Drosophila genes named 'suppressor of position-effect variegation', suggesting the involvement of the encoded protein in chromatin compaction/relaxation processes. Using complementary procedures of cell fractionation, immunolocalisation on mitotic and polytene chromosomes and cross-linking/immunoprecipitation of genomic DNA targets, we have analysed the sub-nuclear distribution of Modulo. While actually associated to condensed chromatin and heterochromatin sites, the protein is also abundantly found at nucleolus. From a comparison of Modulo pattern on chromosomes of different cell types and mutant lines, we propose a model in which the nucleolus balances the Modulo protein available for chromatin compaction and PEV modification. At a molecular level, repetitive elements instead of rDNA constitute Modulo DNA targets, indicating that the protein directly contacts DNA in heterochromatin but not at the nucleolus. Consistent with a role for Modulo in nucleolus activity and protein synthesis capacity, somatic clones homozygous for a null mutation express a cell-autonomous phenotype consisting of growth alteration and short slender bristles, characteristic traits of Minute mutations, which are known to affect ribosome biogenesis. The results provide evidence suggesting that Modulo participates in distinct molecular networks in the nucleolus and heterochromatin and has distinct functions in the two compartments.