Inheritance of associative memories and acquired cellular changes in C. elegans

Noa Deshe, Yifat Eliezer, Lihi Hoch, Eyal Itskovits, Eduard Bokman, Shachaf Ben-Ezra and Alon Zaslaver ()
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Noa Deshe: Edmond J. Safra Campus, The Hebrew University of Jerusalem
Yifat Eliezer: Edmond J. Safra Campus, The Hebrew University of Jerusalem
Lihi Hoch: Edmond J. Safra Campus, The Hebrew University of Jerusalem
Eyal Itskovits: Edmond J. Safra Campus, The Hebrew University of Jerusalem
Eduard Bokman: Edmond J. Safra Campus, The Hebrew University of Jerusalem
Shachaf Ben-Ezra: Edmond J. Safra Campus, The Hebrew University of Jerusalem
Alon Zaslaver: Edmond J. Safra Campus, The Hebrew University of Jerusalem

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract Experiences have been shown to modulate behavior and physiology of future generations in some contexts, but there is limited evidence for inheritance of associative memory in different species. Here, we trained C. elegans nematodes to associate an attractive odorant with stressful starvation conditions and revealed that this associative memory was transmitted to the F1 progeny who showed odor-evoked avoidance behavior. Moreover, the F1 and the F2 descendants of trained animals exhibited odor-evoked cellular stress responses, manifested by the translocation of DAF-16/FOXO to cells’ nuclei. Sperm, but not oocytes, transmitted these odor-evoked cellular stress responses which involved H3K9 and H3K36 methylations, the small RNA pathway machinery, and intact neuropeptide secretion. Activation of a single chemosensory neuron sufficed to induce a serotonin-mediated systemic stress response in both the parental trained generation and in its progeny. Moreover, inheritance of the cellular stress responses increased survival chances of the progeny as exposure to the training odorant allowed the animals to prepare in advance for an impending adversity. These findings suggest that in C. elegans associative memories and cellular changes may be transferred across generations.

Date: 2023
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DOI: 10.1038/s41467-023-39804-8

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