Open Access Research

Caenorhabditis elegans Heterochromatin protein 1 (HPL-2) links developmental plasticity, longevity and lipid metabolism

Peter Meister12, Sonia Schott3, Cécile Bedet3, Yu Xiao3, Sabine Rohner1, Selena Bodennec3, Bruno Hudry4, Laurent Molin5, Florence Solari5, Susan M Gasser1 and Francesca Palladino3*

Author affiliations

1 Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland

2 Cell Fate and Nuclear Organization, Institute of Cell Biology, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland

3 Laboratory of Molecular and Cellular Biology, CNRS, Université de Lyon, Ecole Normale Supérieure, 69364 Lyon Cedex 07, France

4 Development Biology Institute of Marseille Luminy, UMR 6216, Case 907 - Parc Scientifique de Luminy, 13288 Marseille Cedex 9, France

5 Center of Molecular and Cellular Physiology and Genetics, Université Lyon 1, CNRS UMR 5534, 69622 Villeurbanne, France

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Citation and License

Genome Biology 2011, 12:R123  doi:10.1186/gb-2011-12-12-r123

Published: 20 December 2011

Abstract

Background

Heterochromatin protein 1 (HP1) family proteins have a well-characterized role in heterochromatin packaging and gene regulation. Their function in organismal development, however, is less well understood. Here we used genome-wide expression profiling to assess novel functions of the Caenorhabditis elegans HP1 homolog HPL-2 at specific developmental stages.

Results

We show that HPL-2 regulates the expression of germline genes, extracellular matrix components and genes involved in lipid metabolism. Comparison of our expression data with HPL-2 ChIP-on-chip profiles reveals that a significant number of genes up- and down-regulated in the absence of HPL-2 are bound by HPL-2. Germline genes are specifically up-regulated in hpl-2 mutants, consistent with the function of HPL-2 as a repressor of ectopic germ cell fate. In addition, microarray results and phenotypic analysis suggest that HPL-2 regulates the dauer developmental decision, a striking example of phenotypic plasticity in which environmental conditions determine developmental fate. HPL-2 acts in dauer at least partly through modulation of daf-2/IIS and TGF-β signaling pathways, major determinants of the dauer program. hpl-2 mutants also show increased longevity and altered lipid metabolism, hallmarks of the long-lived, stress resistant dauers.

Conclusions

Our results suggest that the worm HP1 homologue HPL-2 may coordinately regulate dauer diapause, longevity and lipid metabolism, three processes dependent on developmental input and environmental conditions. Our findings are of general interest as a paradigm of how chromatin factors can both stabilize development by buffering environmental variation, and guide the organism through remodeling events that require plasticity of cell fate regulation.