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. 2023 Mar 28;42(3):112263.
doi: 10.1016/j.celrep.2023.112263. Epub 2023 Mar 15.

An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes

Nataliya Timoshevskaya  1 , Kaan I Eşkut  1 , Vladimir A Timoshevskiy  1 , Sofia M C Robb  2 , Carson Holt  3 , Jon E Hess  4 , Hugo J Parker  2 , Cindy F Baker  5 , Allison K Miller  6 , Cody Saraceno  1 , Mark Yandell  3 , Robb Krumlauf  7 , Shawn R Narum  8 , Ralph T Lampman  9 , Neil J Gemmell  6 , Jacquelyn Mountcastle  10 , Bettina Haase  10 , Jennifer R Balacco  10 , Giulio Formenti  11 , Sarah Pelan  12 , Ying Sims  12 , Kerstin Howe  12 , Olivier Fedrigo  10 , Erich D Jarvis  13 , Jeramiah J Smith  14
Affiliations

An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes

Nataliya Timoshevskaya et al. Cell Rep. .

Abstract

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.

Keywords: CP: Molecular biology; assembly; chromatin diminution; chromosome; evolution; genome; germline; lamprey; programmed DNA loss.

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Conflict of interest statement

Declaration of interests The authors declare no competing interests.

Figures

Figure 1.
Figure 1.. Assembly quality metrics for the VGP lamprey genome and other lamprey genomes
(A) Percent of short-read k-mers found in the assembly. This statistic reflects the degree to which the assembly incorporates sequences that are sampled from the organism. Analyses were performed using germline (blue) and somatic (red) reads. (B) Estimated error rate reflects the degree to which the assembly bases are consistent with large samples of reads. This statistic can be impacted by intraspecific polymorphism when assembly and evaluation read sets are generated from different tissues or individuals: the blue plus (+) symbol shows the value for this estimate when short-read data are from the same animal used for the assembly. (C) Percentage of predicted conserved metazoan orthologs detected. (D) Percentage of predicted conserved vertebrate orthologs detected. *, somatic reads not available; **, germline reads not available; P.m, P. marinus; E.t, E. tridentatus; L.c, L. camtschaticum; L.r, L. reissneri. Datasets and detailed numbers provided in Table S1.
Figure 2.
Figure 2.. Annotation and analysis of the germline-specific chromosome G1
A browser view showing a 600 kb subregion of ChrG1. This region shows strong segmental homology to at least seven somatically retained chromosomes (highlighted by coloration of the corresponding segments) and contains 13 gene models, including 6 paralogs of HYKK. Segments homologous to somatic chromosomes vary with respect to their length and the degree of sequence identity between ChrG1 and the corresponding somatic chromosome across nonrepetitive intervals. Browser view is from SIMRbase (https://simrbase.stowers.org) and displays a subset of tracks that are most informative to assessing DNA elimination and the evolution of the sequence content of this chromosome. A view of the entire chromosome is shown in Figure S3.
Figure 3.
Figure 3.. Example gene trees for germline-specific genes with well-defined somatic homologs in sea lamprey
A complete set of trees is shown in Figure S4. Germline-specific genes are highlighted in red. Lamprey somatic lineages are highlighted in orange (sea lamprey), green (Pacific lamprey), and purple (kanakana/piharau/pouched lamprey). Gnathostome lineages are highlighted in gray. Divergence dates are relative to three major divergence events within the lamprey lineage. **, gene trees with germline-specific clades with dN/dS >1 and higher than somatically retained clades; *, dN/dS not determined due to a high frequency of gap characters in amino acid alignments. Scale bars: 0.02 substitutions per amino acid site.
Figure 4.
Figure 4.. Expression of germline-specific genes and their somatic homologs during early embryogenesis and spermatogenesis
Groups of paralogs are separated based on the predicted timing of divergence for somatic- (S) vs. germline-specific copies. Expression is presented relative to FKPM (fragments per kilobase per million reads) to aid in comparisons between homologs of varying length. Colors depicting varying levels of gene expression are scaled relative to the log10(FKPM) to permit visualization of expression metrics spanning several orders of magnitude (inset scale).
See this image and copyright information in PMC

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