Pervasive male-biased expression throughout the germline-specific regions of the sea lamprey genome supports key roles in sex differentiation and spermatogenesis

Abstract

Sea lamprey undergo programmed genome rearrangement (PGR) in which ∼20% of the genome is jettisoned from somatic cells during embryogenesis. Although the role of PGR in embryonic development has been studied, the role of the germline-specific region (GSR) in gonad development is unknown. We analysed RNA-sequence data from 28 sea lamprey gonads sampled across life-history stages, generated a genome-guided de novo superTranscriptome with annotations, and identified germline-specific genes (GSGs). Overall, we identified 638 GSGs that are enriched for reproductive processes and exhibit 36x greater odds of being expressed in testes than ovaries. Next, while 55% of the GSGs have putative somatic paralogs, the somatic paralogs are not differentially expressed between sexes. Further, putative orthologs of some the male-biased GSGs have known functions in sex determination or differentiation in other vertebrates. We conclude that the GSR of sea lamprey plays an important role in testicular differentiation and potentially sex determination.

Novel selectively amplified DNA sequences in the germline genome of the Japanese hagfish, Eptatretus burgeri

“…Studies of nematodes revealed that the eliminated genome contains at least 685 predicted genes, and one of them (named rpS19G ) encodes a homologue to the 40S ribosomal protein S19 of eukaryotes 21 , 22 . Similar results were reported in sea lamprey and zebra finch, in which protein-coding genes are also eliminated during early embryogenesis , 3 , 6 , 23 . Hence, these studies suggest that the biological functions of PGR include its’ ability to remove functional protein-coding genes and provide a mechanism by which irreversibly gene silencing can occur to avoid potentially misexpression in somatic lineage.…”

“…The elimination of specific chromosomal fragments or entire chromosomes from germ cells called chromosomal elimination and chromatin diminution respectively occurs in several species of nematodes, insects, crustaceans, and vertebrates, and is collectively referred to as programmed genome rearrangement (PGR) 2 . While the eliminated chromosomes (E-chromosomes) are typically composed of constitutive heterochromatin and highly repetitive DNA sequences, there are protein coding genes that could be involved in early stages of embryogenesis or gonadogenesis, as reported in songbird and sea lamprey 3 – 6 .…”

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

“…Embargoes on the use of this improved lamprey genome assembly are lifted upon publication of this study. We are aware that another manuscript 42 reports genome-wide predictions of germline-specific scaffolds and chromosomes, as well as the impacts of our improved assembly on the annotation of germline-specific genes. That work was published despite the presence of fair-use embargo agreements.…”

Extensive DNA methylome rearrangement during early lamprey embryogenesis

“…In our study, we found that WGBS read coverage at eliminated sequences in the egg was comparable to that of somatic tissues, suggestive of some degree of DNA elimination. Previously, RNA-seq analyses of male and female lamprey gonad development have shown that eliminated genes are 36X more likely to be expressed in testes than in ovaries and that strikingly, ~70% of those genes were not expressed in differentiated ovarian samples 43 . This indeed suggests that the complement of eliminated genes might differ between the male and female germline and that programmed DNA loss from mature oocytes is indeed a possibility.…”