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Odd vertebrate gets rid of hundreds of genes early in development

Enlarge/ There's no jaw on the front of that face, and ..

Enlarge/ There's no jaw on the front of that face, and all the tissues you see have deleted hundreds of key developmental genes.Michael Heck, Oregon Fish and Wildlife

Sea lampreys are parasites native to the northern and western Atlantic Ocean that suck blood and other vital fluids from their fellow fish. They have the distinction of possibly being the first destructive invasive species in North America; they entered the Great Lakes in the 1830s through the Welland Canal and have been killing trout there ever since.

They also have the distinction of having split off from the rest of the vertebrate lineage very early on, about 550 million years ago, before the evolution of jaws. This makes lampreys useful as a model organism for shedding light on the evolution of various vertebrate traits. But our studies have also revealed some strange features of the lamprey, including the fact that they get rid of hundreds of genes early in development.

Sea lampreys have several traits that other (jawed) vertebrates do not, suggesting that these traits either (a) were present in our last shared ancestor and lost by us or (b) arose since lampreys diverged from the jawed vertebrate lineage. One of these traits is a real oddity: programmed genome rearrangement. During this process, sea lampreys jettison about 20 percent of their genome during embryonic development. A few cells don't undergo this process, and these go on to pass on the otherwise missing DNA to another generation.

Once this genome rearrangement was discovered in 2009, scientists speculated that the deleted genetic sequences must be important for germ cells and/or early on in embryo development, but deleterious to more mature cells. But sea lampreys have a highly repetitive genome, comprised of 99 chromosome pairs in the germline, so sequencing data confirming this speculation was difficult to generate. The post-deletion genome was completed in 2013, but the full germline genome took until this week to complete.

Comparing the two genomes revealed that hundreds of genes are eliminated in programmed genome rearrangement. The human versions of these genes are involved in processes including cell division, migration, and adhesion, as well as commitment to a specialized state. These are biological functions that are, in fact, vital during embryogenesis but very problematic for somatic cells, where they could promote aggressive cancers.

Moreover, the mouse versions of these genes are shut down in embryonic stem cells and are presumably released from this silencing later on if these cells eventually differentiate into germline cells. So all vertebrates must somehow deactivate these growth-promoting genes when maturing out of an early embryonic state.

Sea lampreys do it by physically eliminating the genes, while mice (and probably humans) do it by silencing them. There may be advantages and drawbacks to both approaches, so the topic is worth looking at further. And it would be interesting to find out how lampreys target specific genes for deletion, since that could be a useful tool to have in our genetic arsenal.

Nature Genetics, 2018. DOI: 10.1038/s41588-017-0036-1 (About DOIs).

Original Article

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