Complex expression dynamics and robustness in C. elegans insulin networks

Ashlyn D. Ritter; Yuan Shen; Juan Fuxman Bass; Sankarganesh Jeyaraj; Bart Deplancke; Arnab Mukhopadhyay; Jian Xu; Monica Driscoll; Heidi A. Tissenbaum; Albertha J.M. Walhout

doi:10.1101/gr.150466.112

Complex expression dynamics and robustness in C. elegans insulin networks

¹Program in Systems Biology, University of Massachusetts Medical School, Worcester, Massachusetts 01605, USA;
²Program in Gene Function and Expression, University of Massachusetts Medical School, Worcester, Massachusetts 01605, USA;
³Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, Massachusetts 01605, USA;
⁴Department of Molecular Biology and Biochemistry, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08855, USA

↵Present addresses: ⁵Division of Endocrinology, Children's Hospital Boston, Harvard Medical School, Boston, MA 02115, USA;
↵6 Institut für Tropenmedizin, University of Tübingen, 72074 Tübingen, Germany;
↵7 Laboratory of Systems Biology and Genetics, Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland;
↵8 Molecular Aging Laboratory, National Institute of Immunology, New Delhi 110067, India.

Abstract

Gene families expand by gene duplication, and resulting paralogs diverge through mutation. Functional diversification can include neofunctionalization as well as subfunctionalization of ancestral functions. In addition, redundancy in which multiple genes fulfill overlapping functions is often maintained. Here, we use the family of 40 Caenorhabditis elegans insulins to gain insight into the balance between specificity and redundancy. The insulin/insulin-like growth factor (IIS) pathway comprises a single receptor, DAF-2. To date, no single insulin-like peptide recapitulates all DAF-2-associated phenotypes, likely due to redundancy between insulin-like genes. To provide a first-level annotation of potential patterns of redundancy, we comprehensively delineate the spatiotemporal and conditional expression of all 40 insulins in living animals. We observe extensive dynamics in expression that can explain the lack of simple patterns of pairwise redundancy. We propose a model in which gene families evolve to attain differential alliances in different tissues and in response to a range of environmental stresses.

Footnotes

↵9 Corresponding authors

E-mail heidi.tissenbaum{at}umassmed.edu

E-mail marian.walhout{at}umassmed.edu
[Supplemental material is available for this article.]
Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.150466.112.

Received October 9, 2012.
Accepted March 22, 2013.

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