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When every photon counts

April 17, 2009

The eyes of nocturnal mammals have very large numbers of highly-sensitive rod photoreceptors (the cell type responsible for night vision). They have to perceive light which is less than a millionth of the intensity of daylight. An international team headed by LMU researchers Dr. Boris Joffe, Dr. Irina Solovei and Professor Thomas Cremer has now succeeded in demonstrating that a nocturnal lifestyle and the challenges posed by it have a dramatic effect on the organisation of the nuclei of rod cells. The scientists observed a unique distribution of densely packed inactive and less densely packed active regions of DNA in the rods of nocturnal mammals. This organization differs from the nuclear architecture in all cells of almost all other eukaryotic organisms -- including rod cells of diurnal mammals. "There is an explanation for this difference,"� notes Joffe. "With this inverted arrangement, the cell nuclei of nocturnal mammals function as collecting lenses which strongly reduce scatter of the incident light. Computer simulations show that stacks of many such cell nuclei channel the light very effectively into the light-sensitive outer segment of the rods. The modified organization of the rod cell nuclei thus enhances these animals' nocturnal vision -- and offers new insights into the evolution of the mammalian retina and for our understanding of the spatial organisation of the nucleus."�

The art of nuclear packing: The DNA molecule in diploid mammals is two metres long, but has to fit into a cell nucleus just a few micrometres in size. The DNA molecule is tightly packed and covered by proteins. Some regions of this so-called chromatin contain genes, that is information about proteins, and are known as euchromatin. They are typically found in the interior of the nucleus. The major part of the heterochromatin, formed by non-coding DNA, is located at the periphery of the nucleus. This organization of the nucleus has been retained over the course of the last 500 million years in multicellular organisms almost without exception.

"This arrangement is so universal that it can be described as the 'conventional architecture' of the nucleus,"� explains Dr. Boris Joffe of the BioCenter at LMU Munich. "The discovery that there are substantial differences in the nuclear architecture and that this depends on the lifestyle of the animal is then all the more surprising."� An interdisciplinary team of researchers from LMU, the Max Planck Institute for Brain Research in Frankfurt and the Cavendish Laboratory in Cambridge was able to demonstrate that the arrangement of chromatin in the rod cells of nocturnal mammals is inverted compared to the conventional one. The tightly packed heterochromatin is located in the interior of the nucleus, whilst the more loosely packed euchromatin containing the active areas of DNA is located at the periphery.

The explanation for this unusual nuclear architecture is to be found in the biology of vision. In humans and all other vertebrates, light must pass the retina before reaching the light-sensitive outer segment of the photoreceptors. This presents nocturnal animals with a dilemma. They need a very large number of rods to detect low light levels, which results in a thicker retina and consequently greater light loss through scattering before the light can reach the outer segment of the photoreceptors. To solve problem, evolution has exploited an unusual physical characteristic of the tightly packed heterochromatin.

As a result of its increased packing density, heterochromatin refracts light more strongly than euchromatin but it does not reduce scatter of light if it is located in the periphery of the nucleus. If, however, it is concentrated in the center, the whole nucleus functions as a tiny converging lens. A number of these micro-lenses are stacked on top of each other, because the rod cell nuclei are arranged in columns. Computer simulations clearly demonstrate the benefit of this unique cellular arrangement: Light is channelled through the retina with almost no loss from scattering and focused onto the light-sensitive outer segments of the photoreceptors.

This specific architecture of the rod cell nuclei must have arisen more than one hundred million years ago and thus provides new insights into early mammalian evolution. At this time, the ancestors of today's mammals adapted to a nocturnal lifestyle in order to escape carniovorous reptiles, the dominant predators of that period. All nocturnal mammals, including recent species, retained the inverted rod cell nuclear architecture. However, mammals which became diurnal -- such as man -- reacquired a conventional organization of the chromatin in their rod cells.

"This emphasizes the functional advantage of the conventional architecture,"� notes Joffe. "The inversion of nuclear organisation obviously entails some unknown disadvantages. One possible explanation could be that the conventional architecture makes it easier to share nuclear machinery between the active areas of the chromatin. But the advantages of enhanced night vision outweigh this benefit in nocturnal mammals."� (suwe)

LMU Munich