The sea lamprey germline genome — providing insights into programmed genome rearrangement and vertebrate evolution

Sea lamprey (Petromyzon marinus) is a member of an ancient lineage that diverged from the vertebrate (animal with a backbone or spinal column) stem ~550 million years ago, give or take a few months. Accordingly, the lamprey has served as an important model for understanding evolution of several conserved features that are relevant to many fields of biology and medicine. Lampreys have been used to provide evolutionary perspectives –– on developmental pathways that define vertebrate embryogenesis, vertebrate nervous and neuroendocrine systems, genome structure, immunity, clotting, and other features. These studies show aspects of vertebrate biology that have been conserved over long spans of evolutionary time and identify evolutionary modifications that gave rise to novel features that emerged within the gnathostomes (any vertebrate having a mouth with jaws).

Lampreys also possess several features that are not observed in gnathostomes –– which might represent either aspects of ancestral vertebrate biology that have not been conserved in gnathostomes, or features that arose since divergence of the ancestral lineages that gave rise to lampreys and gnathostomes. These features include the ability to achieve full functional recovery after complete spinal cord transection, deployment of evolutionarily independent yet functionally equivalent adaptive immune receptors, and physical restructuring of the genome during development –– known as programmed genome rearrangement (PGR).

PGR results in the physical elimination of ~0.5 Gb of DNA (gigabase = billion bases, so 0.5 Gb = 500 Mb or 500 million bases) from the organism’s ~2.3-Gb genome..!! The elimination events that mediate PGR –– are initiated at the 7th embryonic cell division –– and are essentially complete by 3 days post-fertilization. As a result, lampreys are effectively chimeric (cells having distinct genotypes within the same organism), with germ cells possessing a full complement of genes and all other cell types possessing a smaller reproducible fraction of the germline genome. Our understanding of the mechanisms and consequences of PGR remains incomplete, because only the smaller, reproducible fraction of the genome (i.e. that which lacks the 0.5 Gb specific to the germline) has been sequenced to date.

Authors [see attached article] thus assembled both the chromosomal and whole-genome duplications that have played significant roles in evolution of ancestral vertebrate and lamprey genomes –– including chromosomes that carry the six lamprey homeobox (HOX) clusters. The assembly also contains several hundred genes that are always eliminated from somatic cells during early development in lamprey. Comparative analyses show that gnathostome (e.g. mouse) homologs of these genes are frequently marked by polycomb repressive complexes (PRCs) in embryonic stem cells. These data suggest overlaps in the regulatory logic of somatic DNA elimination and bivalent states that are regulated by early embryonic PRCs. This new assembly should now help studies that are relevant to lampreys’ unique biology and evolutionary/comparative perspective.

Nature Genet Feb 2o18; 50: 270–277

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