Evolutionary history and functional characterization of Lj-TICAM-a and Lj-TICAM-b formed via lineage-specific tandem duplication in lamprey (Lampetra japonica).

Toll/interleukin-1 receptor domain-containing adaptor molecule (TICAM) genes respond to infections. We identified TICAM-a and TICAM-b in Lampetra japonica and investigated their evolutionary history and potential function via comparative genomics and molecular evolution analyses. They are arranged in tandem and evolved from a multi-exon to a single-exon structure. Lj-TICAM-a and Lj-TICAM-b might be the ancestral gene of the vertebrate TICAM genes. Lj-TICAM-b arose via a lamprey-specific tandem duplication event. Both genes are expressed in many tissues during an immune response, and exhibit different responses to peptidoglycan, indicating their functional divergence. Simultaneous overexpression of both proteins activated nuclear factor κB expression and co-immunoprecipitation assays indicated that they might form a complex for signal transduction. However, unlike in mammals, the TICAM-dependent signaling pathway in lamprey might rely on TRAF3 rather than on TRAF6. These results suggest that both Lj-TICAM-a and Lj-TICAM-b play a role in host defenses.

Chromosome-level genome assembly of Lethenteron reissneri provides insights into lamprey evolution.

The reissner lamprey Lethenteron reissneri, belonging to the class Cyclostomata, serves as a bridge between invertebrates and jawed vertebrates, and is considered the sister group of jawed vertebrates. However, despite this evolutionary significance, the genetic mechanisms underlying the adaptive evolution of the lamprey lineage remain unclear. Here, we assembled a 1.06 Gb chromosome-level draft genome of L. reissneri, with 72 chromosomes (ranging in length from 4.5 Mb to 25.9 Mb) and a scaffold N50 length of 13.23 Mb. Genome quality comparisons revealed that the reissner lamprey genome has higher completeness and contiguity than the previously published sea lamprey and Japanese lamprey genomes. Moreover, reissner lamprey, sea lamprey, and Japanese lamprey species share similar transposable element profiles and Hox gene cluster compositions, suggesting that a burst of transposable element activity and whole genome duplication occurred before their divergence. Additionally, the Lip gene copy numbers, which have been studied for their functions in the host defence system, were found to be expanded uniquely in lamprey lineages, suggesting key roles for these genes in lamprey evolution and adaptation. We also identified two neural-related genes, Nrn1 and Unc13a, with copy number expansions in jawed vertebrates, which may be functionally relevant to the origin of lamprey brains. Hence, this study not only provides the first chromosome-level reference genome for Cyclostomata, but also highlights features of the unique biology and adaptive evolution of the lamprey lineage.