Stressed worms use epigenetic inheritance to produce more sexually attractive offspring

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Sexual reproduction allows organisms to mix their genes and develop new adaptations to survive in a harsh and constantly changing environment. Under nutrient-rich conditions, the worm C.elegans is usually asexual, but after enduring several generations of stress, the worms begin to reproduce sexually and release pheromones to appear more sexually attractive to male worms. In the magazine Development Cell February 7andthe researchers determined how sexual attraction is transmitted and that it does not occur through the modification of the worm’s DNA, but rather through the transfer of small RNAs.

“For more than a decade, we have been studying a highly controversial question: Can parental responses to environmental challenges be passed down from generation to generation?” says Oded Rechavi (@OdedRechavi), lead author of the study and a professor studying RNA memory inheritance at Tel Aviv University. “We know it can’t happen via DNA sequence changes, but surprisingly our work and the work of many others show it can happen, at least in simple organisms (notably C.elegans nematodes), via inheritance of small RNA molecules.”

Small RNAs can influence an organism’s gene expression through a phenomenon known as gene silencing. “Unlike DNA, small RNAs are synthesized in response to certain environmental conditions, resulting in gene expression changes that persist through generations to offspring that have not been exposed to the stressful environment” , says co-author Yael Mor (@YaelMor3) and MD -Doctoral student at the Rechavi laboratory.

The researchers simulated mildly stressful conditions in the lab by growing the worms at 25°C, which is hot for worms, but within the standard temperature range for lab cultures. Normally, hermaphroditic worms would wait until the end of their life cycle when they stop producing sperm to start secreting pheromones that attract males, but these stressful conditions caused the worms to become prematurely attractive to males.

“Another exciting aspect of our study is that sperm and sperm small RNAs can serve as a stress sensor (or rheostat),” says Rechavi. His team found that high temperatures induced defects in the worm’s sperm, and this is what triggers increased sexual attraction under environmental stress.

To identify the pathway by which worms regulate sexual attraction, the researchers examined worms with different small RNA species deactivated and tested whether they were more attractive than normal worms. “We have developed a unique system that allows us to eliminate the Argonaute HRDE-1 protein that binds hereditary small RNAs,” says co-author Itamar Lev (@itamar_lev), a former PhD student at the Rechavi lab and now a postdoc at the University of Vienna. “We found that deleting HRDE-1 in offspring (depleting hereditary small RNAs) eliminates inheritance of attractiveness.”

“One result that surprised us at first was that hermaphrodites do not immediately secrete the male-attracting pheromone when grown at higher temperatures: they wait about ~10 generations (~4 weeks) before increasing their attractiveness”, explains the co-author. Itai Toker (@Toker_IA), former PhD student at Rechavi Lab and now postdoc at Columbia University. “In retrospect, this makes a lot of sense – the persistent experience of previous generations can provide organisms with a relatively robust ‘prediction’ that this environment might persist for longer.”

C.elegans has a unique dual-mode reproductive strategy, but Rechavi’s team hopes to determine whether similar hereditary effects occur in other organisms. “This work links short-term epigenetic inheritance to long-term hardwired genetic changes, and thus to the evolutionary process,” explains Yael Mor.

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