Table 4F(1). Induced transgenerational epigenetic changes

Stimulus or stress



Heat stress

Fission yeast (S. pombe)

(Seong, Li et al. 2011; Seong, Maekawa et al. 2012)

Heat and UV-B


(Lang-Mladek, Popova et al. 2010)

Heavy metals


(Rahavi, Migicovsky et al. 2011)

Heavy metals


(Ou, Zhang et al. 2012)

Bacterial infection


(Luna, Bruce et al. 2012)

Viral infection


(Dong 2004; Boyko, Kathiria et al. 2007)

Viral infection


(Kathiria, Sidler et al. 2010)

Chemicals and predation


(Verhoeven, Jansen et al. 2010; Verhoeven and van Gurp 2012)



(Rasmann, De Vos et al. 2012)

Drought exposure

Polygonum persicaria

(Herman, Sultan et al. 2012)

Multiple stressors


(Boyko and Kovalchuk 2010; Herman and Sultan 2011; Rasmann, De Vos et al. 2012)

RNA (induced RNAi or piRNA)

Nematode (C. elegans)

(Burton, Burkhart et al. 2011; Ashe, Sapetschnig et al. 2012)

Endocrine disruptors


(Bollati and Baccarelli 2010; Walker and Gore 2011; Manikkam, Tracey et al. 2013)

Maternal behavior


(Weaver, Cervoni et al. 2004; Szyf, Weaver et al. 2005)




Ashe, A., A. Sapetschnig, et al. (2012). "piRNAs Can Trigger a Multigenerational Epigenetic Memory in the Germline of C. elegans." Cell 150(1): 88-99.

Bollati, V. and A. Baccarelli (2010). "Environmental epigenetics." Heredity (Edinb) 105(1): 105-112.

Boyko, A., P. Kathiria, et al. (2007). "Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virus-induced plant genome instability)." Nucleic Acids Res 35(5): 1714-1725.

Boyko, A. and I. Kovalchuk (2010). "Transgenerational response to stress in Arabidopsis thaliana." Plant Signal Behav 5(8).

Burton, N. O., K. B. Burkhart, et al. (2011). "Nuclear RNAi maintains heritable gene silencing in Caenorhabditis elegans." Proc Natl Acad Sci U S A 108(49): 19683-19688.

Dong, X. (2004). "Pathogen-induced systemic DNA rearrangement in plants." Trends Plant Sci 9(2): 60-61.

Herman, J. J. and S. E. Sultan (2011). "Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations." Front Plant Sci 2: 102.

Herman, J. J., S. E. Sultan, et al. (2012). "Adaptive transgenerational plasticity in an annual plant: grandparental and parental drought stress enhance performance of seedlings in dry soil." Integr Comp Biol 52(1): 77-88.

Kathiria, P., C. Sidler, et al. (2010). "Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants." Plant Physiol 153(4): 1859-1870.

Lang-Mladek, C., O. Popova, et al. (2010). "Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis." Mol Plant 3(3): 594-602.

Luna, E., T. J. Bruce, et al. (2012). "Next-generation systemic acquired resistance." Plant Physiol 158(2): 844-853.

Manikkam, M., R. Tracey, et al. (2013). "Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations." PLoS One 8(1): e55387.

Ou, X., Y. Zhang, et al. (2012). "Transgenerational Inheritance of Modified DNA Methylation Patterns and Enhanced Tolerance Induced by Heavy Metal Stress in Rice (Oryza sativa L.)." PLoS One 7(9): e41143.

Rahavi, M. R., Z. Migicovsky, et al. (2011). "Transgenerational adaptation to heavy metal salts in Arabidopsis." Front Plant Sci 2: 91.

Rasmann, S., M. De Vos, et al. (2012). "Herbivory in the previous generation primes plants for enhanced insect resistance." Plant Physiol 158(2): 854-863.

Rasmann, S., M. De Vos, et al. (2012). "Ecological role of transgenerational resistance against biotic threats." Plant Signal Behav 7(4): 447-449.

Seong, K. H., D. Li, et al. (2011). "Inheritance of stress-induced, ATF-2-dependent epigenetic change." Cell 145(7): 1049-1061.

Seong, K. H., T. Maekawa, et al. (2012). "Inheritance and memory of stress-induced epigenome change: roles played by the ATF-2 family of transcription factors." Genes Cells 17(4): 249-263.

Szyf, M., I. C. Weaver, et al. (2005). "Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat." Front Neuroendocrinol 26(3-4): 139-162.

Verhoeven, K. J., J. J. Jansen, et al. (2010). "Stress-induced DNA methylation changes and their heritability in asexual dandelions." New Phytol 185(4): 1108-1118.

Verhoeven, K. J. and T. P. van Gurp (2012). "Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion." PLoS One 7(6): e38605.

Walker, D. M. and A. C. Gore (2011). "Transgenerational neuroendocrine disruption of reproduction." Nat Rev Endocrinol 7(4): 197-207.

Weaver, I. C., N. Cervoni, et al. (2004). "Epigenetic programming by maternal behavior." Nat Neurosci 7(8): 847-854.