Organisms inherit their mitochondria – the cell’s “power plants” – from their mothers, but what happens to all the father’s mitochondria?

Why and how are paternal mitochondria prevented from getting passed on to their offspring after fertilization? Just the randomness of evolution or is there a reason the phenomenon has been conserved?

One hypothesis holds that it is an active process in which paternal mitochondria are selectively degraded by a “self-eating” system known as autophagy, in which vesicles called autophagosomes engulf the cell’s unwanted structures. But the autophagy study was conducted on worms (C. elegans) whose sperm are quite different from the long, flagellated “head” and “tail” structures of both mammalian and fruit-fly sperm. The tail comprises the mitochondria: a long tube attached to, or coiled around, the tail’s skeletal structure. How would the tiny autophagosome engulf such a large structure – about 2 mm long in the fruit fly?

A second hypothesis, based mainly on mouse models, states that the absence of paternal mitochondria is due to a passive process of dilution in the sea of maternal mitochondria. But that could not explain why certain genetic markers related to autophagy were still detected on the paternal mitochondria after fertilization. 

Working instead with female fruit flies, Dr. Eli Arama and a team in the Weizmann Institute’s Molecular Genetics Department have discovered special cellular vesicles that originate in the female egg - and these vesicles actively seek out and destroy the father’s mitochondria upon fertilization. 

The team found that as soon as the sperm enters the egg, the cellular vesicles – already present in the fruit fly egg – immediately attract to the sperm like a magnet. They then proceed to disintegrate the sperm’s outer membrane and separate the mitochondria from the tail section, which is subsequently cut into smaller pieces that are then “devoured” by conventional selective autophagy.

But what were these vesicles? Close observation revealed they did not resemble an autophagosome, but rather a different type of vesicle that is usually involved in a distinct pathway. Yet these vesicles carried autophagy markers. “We were not witnessing classic autophagy machinery; these structures were too large and morphologically distinct to be typical autophagosomes,” says Arama.

The team’s findings suggest that the egg’s special cellular vesicles represent a new type of system that is a unique combination of three separate biological processes whose pathways may have diverged from their classic functions.

These new discoveries, which the scientists believe hold true for other organisms with flagellated sperm, including humans, may lead, among other things, toward an understanding of why only a quarter of IVF pregnancies carry to term. It may be that this invasive procedure somehow abrogates the ability of the egg to destroy the paternal mitochondria. 

Published in Development Cell