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Inheritance of associative memories in C. elegans nematodes

Noa Deshe, Yifat Eliezer, Lihi Hoch, Eyal Itskovits, Shachaf Ben-Ezra, View ORCID ProfileAlon Zaslaver
doi: https://doi.org/10.1101/2020.09.08.287318
Noa Deshe
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel
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Yifat Eliezer
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel
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Lihi Hoch
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel
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Eyal Itskovits
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel
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Shachaf Ben-Ezra
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel
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Alon Zaslaver
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel
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  • ORCID record for Alon Zaslaver
  • For correspondence: alonzas@mail.huji.ac.il
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Summary

The notion that associative memories may be transmitted across generations is intriguing, yet controversial. Here, we trained C. elegans nematodes to associate an odorant with stressful starvation conditions, and surprisingly, this associative memory was evident two generations down of the trained animals. The inherited memory endowed the progeny with a fitness advantage, as memory reactivation induced rapid protective stress responses that allowed the animals to prepare in advance for an impending adversity. Sperm, but not oocytes, transmitted the associative memory, and the inheritance required H3K9 and H3K36 methylations, the small RNA-binding Argonaute NRDE-3, and intact neuropeptide secretion. Remarkably, 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. These findings challenge long-held concepts by establishing that associative memories may indeed be transferred across generations.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted September 09, 2020.
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Inheritance of associative memories in C. elegans nematodes
Noa Deshe, Yifat Eliezer, Lihi Hoch, Eyal Itskovits, Shachaf Ben-Ezra, Alon Zaslaver
bioRxiv 2020.09.08.287318; doi: https://doi.org/10.1101/2020.09.08.287318
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Inheritance of associative memories in C. elegans nematodes
Noa Deshe, Yifat Eliezer, Lihi Hoch, Eyal Itskovits, Shachaf Ben-Ezra, Alon Zaslaver
bioRxiv 2020.09.08.287318; doi: https://doi.org/10.1101/2020.09.08.287318

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