New work from a team of researchers led by Stanford University, including Arthur Grossman and Carnegie’s Tingting Xiang, unveils a long-standing mystery about the relationship between form and function in the genetic material of a diverse group algae called dinoflagellates.
Their findings, published in Genetics of nature, have implications for the understanding of the principles of genomic organization of all organisms.
Dinoflagellates include more than 2,000 species of marine and freshwater plankton, many of which are photosynthetic, and some of which also ingest other organisms for food. They play a wide variety of roles in various ecosystems, including extreme environments, and are known primarily to humans as the cause of toxic “red tides” and as the source of most of the bioluminescence in the oceans.
Some photosynthetic dinoflagellates are also essential for healthy coral reefs. These algae are taken up by individual coral cells and form mutually beneficial relationships through which nutrients are exchanged. Warming oceans and pollution can lead to the breakdown of this relationship between algae and animal, resulting in “bleached” ghostly white corals that risk starving to death, which could lead to the death of reef ecosystems.
“Like animals and plants, dinoflagellates are complex eukaryotic organisms and are evolutionarily interesting because their genetic material is uniquely conditioned among organisms with complex cell architecture,” said senior author Georgi Marinov of Stanford University.
A defining characteristic of eukaryotes is that their DNA is housed inside a nucleus in each cell and is organized into separate units called chromosomes. Additionally, in most eukaryotes, segments of DNA are wrapped around a coil-shaped complex of proteins called a nucleosome. This organization is believed to predate the common ancestor of all eukaryotes. It helps condense genetic material into a small space and control access to DNA and how the genes encoded in it are activated to direct the physiological functions of the cell.
“In contrast, even though dinoflagellates are eukaryotes, their genome is not conditioned as nucleosomes, but rather appears to be permanently condensed and exist in a liquid crystal state,” explained Grossman. “We still have a lot to learn about how genome architecture influences genome function in all eukaryotes; thus, the exceptional “tight” conditioning of dinoflagellate DNA may help us understand the similarities and differences in organizational principles between eukaryotic genomes.
To explore this question further, the research team – which also included Stanford’s Alexandro E. Trevino, Anshul Kundaje, and William J. Greenleaf – used sophisticated technology to map the 3D spatial relationships of genetic material from the dinoflagellate Breviolum minutum.
“Our work has revealed topological features in the Breviolum genome that differ from the various organizational patterns of the dinoflagellate genome that have been predicted since the 1960s,” Xiang said.
They found evidence of large self-interacting regions of DNA in the dinoflagellate genome called “topologically associated domains”. The work suggests that this genomic architecture is induced by the process by which genes are transcribed into RNA; this RNA is then translated into proteins which carry out the various activities of the cell.
In fact, when transcription was inhibited, the architecture “relaxed” indicating that the rigorously preserved topographic features are, indeed, a function of gene activity.
“There are many more questions raised by these findings, which represent a big step forward in unraveling the mysteries of the dinoflagellate genome. They also offer a new perspective on the structure-function relationships inherent in chromosomes,” Grossman concluded. .
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