An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes
Nataliya Timoshevskaya,
Kaan İ. Eşkut,
Vladimir A. Timoshevskiy,
Sofia M.C. Robb,
Carson Holt,
Jon E. Hess,
Hugo J. Parker,
Cindy F. Baker,
Allison K. Miller,
Cody Saraceno,
Mark Yandell,
Robb Krumlauf,
Shawn R. Narum,
Ralph T. Lampman,
Neil J. Gemmell,
Jacquelyn Mountcastle,
Bettina Haase,
Jennifer R. Balacco,
Giulio Formenti,
Sarah Pelan,
Ying Sims,
Kerstin Howe,
Olivier Fedrigo,
Erich D. Jarvis,
Jeramiah J. Smith
Affiliations
Nataliya Timoshevskaya
Department of Biology, University of Kentucky, Lexington, KY 40506, USA
Kaan İ. Eşkut
Department of Biology, University of Kentucky, Lexington, KY 40506, USA
Vladimir A. Timoshevskiy
Department of Biology, University of Kentucky, Lexington, KY 40506, USA
Sofia M.C. Robb
Stowers Institute for Medical Research, Kansas City, MO 64110, USA
Carson Holt
Department of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA
Jon E. Hess
Columbia River Inter-Tribal Fish Commission, Portland, OR 97232, USA
Hugo J. Parker
Stowers Institute for Medical Research, Kansas City, MO 64110, USA
Cindy F. Baker
National Institute of Water and Atmospheric Research Limited (NIWA), Hamilton, Waikato 3261, New Zealand
Allison K. Miller
Department of Anatomy, School of Biomedical Sciences, University of Otago, Dunedin, Otago 9054, New Zealand
Cody Saraceno
Department of Biology, University of Kentucky, Lexington, KY 40506, USA
Mark Yandell
Department of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA
Robb Krumlauf
Stowers Institute for Medical Research, Kansas City, MO 64110, USA; Department of Anatomy & Cell Biology, The University of Kansas School of Medicine, Kansas City, KS 66160, USA
Shawn R. Narum
Columbia River Inter-Tribal Fish Commission, Hagerman, ID 83332, USA
Ralph T. Lampman
Yakama Nation Fisheries Resource Management Program, Pacific Lamprey Project, Toppenish, WA 98948, USA
Neil J. Gemmell
Department of Anatomy, School of Biomedical Sciences, University of Otago, Dunedin, Otago 9054, New Zealand
Jacquelyn Mountcastle
Vertebrate Genome Lab, The Rockefeller University, New York, NY 10065, USA
Bettina Haase
Vertebrate Genome Lab, The Rockefeller University, New York, NY 10065, USA
Jennifer R. Balacco
Vertebrate Genome Lab, The Rockefeller University, New York, NY 10065, USA
Giulio Formenti
Vertebrate Genome Lab, The Rockefeller University, New York, NY 10065, USA; Laboratory of Neurogenetics of Language, The Rockefeller University, New York, NY 10065, USA
Sarah Pelan
Tree of Life, Wellcome Sanger Institute, Cambridge CB10 1SA, UK
Ying Sims
Tree of Life, Wellcome Sanger Institute, Cambridge CB10 1SA, UK
Kerstin Howe
Tree of Life, Wellcome Sanger Institute, Cambridge CB10 1SA, UK
Olivier Fedrigo
Vertebrate Genome Lab, The Rockefeller University, New York, NY 10065, USA
Erich D. Jarvis
Vertebrate Genome Lab, The Rockefeller University, New York, NY 10065, USA; Laboratory of Neurogenetics of Language, The Rockefeller University, New York, NY 10065, USA; Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA
Jeramiah J. Smith
Department of Biology, University of Kentucky, Lexington, KY 40506, USA; Corresponding author
Summary: Programmed DNA loss is a gene silencing mechanism that is employed by several vertebrate and nonvertebrate lineages, including all living jawless vertebrates and songbirds. Reconstructing the evolution of somatically eliminated (germline-specific) sequences in these species has proven challenging due to a high content of repeats and gene duplications in eliminated sequences and a corresponding lack of highly accurate and contiguous assemblies for these regions. Here, we present an improved assembly of the sea lamprey (Petromyzon marinus) genome that was generated using recently standardized methods that increase the contiguity and accuracy of vertebrate genome assemblies. This assembly resolves highly contiguous, somatically retained chromosomes and at least one germline-specific chromosome, permitting new analyses that reconstruct the timing, mode, and repercussions of recruitment of genes to the germline-specific fraction. These analyses reveal major roles of interchromosomal segmental duplication, intrachromosomal duplication, and positive selection for germline functions in the long-term evolution of germline-specific chromosomes.