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Transgenerational Epigenetic Inheritance in Drosophila

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Environmental Epigenomics in Health and Disease

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Abstract

Transgenerational epigenetic inheritance involves the inheritance of a phenotype across at least one generation that does not involve any changes in the DNA sequence. The primary mark of transgenerational epigenetic inheritance is thought to be DNA methylation, such as in imprinting in mammals and in the inheritance of coat color in agouti viable yellow (Avy) mice. However, while most studies of Drosophila melanogaster indicate that there is no DNA cytosine methylation, nevertheless several systems of transgenerational epigenetic inheritance have been demonstrated in this organism. In this chapter, we review several Drosophila transgenerational epigenetic systems, including a system that we developed in our laboratory that involves the transgenerational epigenetic inheritance of an ectopic large bristle outgrowth (ELBO) in the eyes of D. melanogaster that can be passed from generation to generation for hundreds of generations. Understanding transgenerational epigenetic inheritance mechanisms in Drosophila can have a profound impact in understanding similar processes in humans in which environmental exposures can affect the health of future generations.

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Abbreviations

Avy :

Agouti viable yellow

DCC:

Dosage compensation complex

DMR:

Differentially methylated region

dsRNA:

Double-stranded RNA

ELBO:

Ectopic large bristle outgrowth

E(var):

Enhancer of variegation

E(z):

Enhancer of zeste

FISH:

Fluorescent in situ hybridization

H3K9:

Histone 3 lysine 9

H3K27:

Histone 3 lysine 27

H4K20:

Histone 4 lysine 20

HAT:

Histone acetyltransferase

HDAC:

Histone deacetylase

HMT:

Histone methyltransferases

HP1:

Heterochromatin protein 1

Hsp90:

Heat shock protein 90

IGF2:

Insulin growth factor 2

IAP:

Intracisternal A particle

JAK:

Janus kinase

KrIf-1:

Kruppel Irregular-facets 1

LacZ:

Beta galactosidase

miRNA:

microRNA

nm:

Nanometer

PcG:

Polycomb group

PEV:

Position-effect variegation

PGC:

Primordial germ cells

PRE:

Polycomb response elements

PSTVd:

Potato spindle tuber viroid

PTGS:

Posttranscriptional gene silencing

rasiRNA:

Repeat-associated small interfering RNA

RdDM:

RNA-directed DNA methylation

RISC:

RNA induced silencing complex

RNAi:

RNA interference

siRNA:

Small interfering RNA

Su(var):

Suppressor of variegation

TGS:

Transcriptional gene silencing

TRE:

Trithorax response elements

TrxG:

Trithorax group

Ubx:

Ultrabithorax

Wg:

Wingless

Xic:

X inactivation center

Xist:

X inactive-specific transcript

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Acknowledgments

This work was supported by a Michigan Core Technology grant from the State of Michigan’s 21st Century Fund Program to the Wayne State University Applied Genomics Technology Center. This work was also supported by the Environmental Health Sciences Center in Molecular and Cellular Toxicology with Human Applications Grant P30 ES06639 at Wayne State University, NIH R01 grants (ES012933) to D.M.R., and DK071073 to X.L.

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Correspondence to Douglas M. Ruden .

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Wang, L., Lu, X., Ruden, D.M. (2013). Transgenerational Epigenetic Inheritance in Drosophila. In: Jirtle, R., Tyson, F. (eds) Environmental Epigenomics in Health and Disease. Epigenetics and Human Health. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-23380-7_10

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