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Genomic imprinting is the process by which some genes are turned on or off depending on whether our parents inherited them. Burga Lab researchers discovered a new way to control genes, related to the silencing of selfish genes. This discovery in Nature could explain the beginnings of the evolution of imprinting.
Alejandro Burga and his IMBA team and the laboratory of Eyal Ben-David at the Hebrew University found the first origin effect in nematodes. This discovery, published in Nature on March 6, 2024, sheds light on how some genes are silenced depending on whether they come from the mother or the father. This process, called genomic imprinting, is based on DNA methylation, an epigenetic signal. Understanding these parental effects is crucial to unraveling how genomic imprinting evolved millions of years ago.
Thirty years ago, IMP researcher Denise Barlow hypothesized that imprinting could be related to defense systems against selfish genetic elements, such as parasitic DNA. This evolutionary struggle is between these components and their defenses.
Pinelopi Pliota made an exciting discovery while investigating selfish genetic elements in the nematode C. tropicalis. She discovered that when the mother carries a particular characteristic, she poisons her eggs, ensuring her inheritance. However, when the roles were reversed, the effect disappeared. This led the team to investigate how inheriting the element from the mother or father produces different results, delving into the molecular basis of this father-of-origin effect.
To understand the father-of-origin effect, Burga’s group studied the piRNA pathway, a defense mechanism against selfish genetic elements. They collaborated with Julius Brennecke’s laboratory and identified the piRNA molecules and proteins involved. However, more was needed to explain his observations. They realized that the maternal mRNA, loaded into the eggs, was missing.
They showed that the venom mRNA, expressed in the mother’s germ line and loaded into the egg, is transported by the TA in maternal inheritance. Burga’s group demonstrated that this mRNA identifies TA as “self,” preventing it from being silenced by the piRNA pathway. “Gene expression is determined by the balance of this process, known as epigenetic licensing, with the piRNA pathway.”
Burga explains, “By default, the piRNA pathway will silence the toxin gene unless there is a maternal mRNA that authorizes it by repressing the piRNA pathway. This inhibition of the inhibitor causes the toxin gene to be activated and the eggs become poisoned.”
The silencing effect of the Burga group persisted for several generations, even affecting great-granddaughters. This impact persists, unlike genomic imprinting, which resets with each generation. This discovery strengthens the evolutionary relationship between parental-specific gene expression and defense mechanisms.
It suggests that organisms lacking DNA methylation and canonical imprinting could have initiated this process. Although different in worms and mammals, this mechanism could be a first step towards more complex heritable silencing, which would eventually lead to the evolution of genomic imprinting.
In conclusion, the Burga Lab study provides crucial information about the evolutionary origin of genomic imprinting. By uncovering the mechanisms underlying parental effects in nematodes and tracing their evolutionary implications, the research contributes significantly to our understanding of this intriguing biological phenomenon.
Magazine reference:
- Pliota, P., Marvanova, H., Koreshova, A., et al. Egoistic conflict underlies RNA-mediated parent-of-origin effects. Nature. DOI: 10.1038/s41586-024-07155-z.