Three amphioxus reference genomes reveal gene and chromosome evolution of chordates

Abstract

The slow-evolving invertebrate amphioxus has an irreplaceable role in advancing our understanding of the vertebrate origin and innovations. Here we resolve the nearly complete chromosomal genomes of three amphioxus species, one of which best recapitulates the 17 chordate ancestor linkage groups. We reconstruct the fusions, retention, or rearrangements between descendants of whole-genome duplications, which gave rise to the extant microchromosomes likely existed in the vertebrate ancestor. Similar to vertebrates, the amphioxus genome gradually establishes its three-dimensional chromatin architecture at the onset of zygotic activation and forms two topologically associated domains at the Hox gene cluster. We find that all three amphioxus species have ZW sex chromosomes with little sequence differentiation, and their putative sex-determining regions are nonhomologous to each other. Our results illuminate the unappreciated interspecific diversity and developmental dynamics of amphioxus genomes and provide high-quality references for understanding the mechanisms of chordate functional genome evolution.

Evolution of the gene regulatory network of body axis by enhancer hijacking in amphioxus

“…Positions of Lefty , Gdf1/3-like , Bmp2/4 , and Gdf1/3 genes in the genomes of B. floridae , B. belcheri , B. japonicum , and B. lanceolatum were determined according to two recent studies ( Brasó-Vives et al, 2022 ; Huang et al, 2023 ), while positions of these genes in sea urchin ( S. purpuratus ) were retrieved directly from Echinobase, in other species including zebrafish ( D. rerio ), elephant shark ( C. milii ), vase tunicate ( C. intestinalis ), acorn worm ( S. kowalevskii ), polychaete worm ( C. teleta ), and fruit fly ( D. melanogaster ) were retrieved directly from Ensembl database.…”

Amphioxus as a model to study the evolution of development in chordates

“…Finally, high-throughput sequencing techniques have made it possible to obtain the complete chromosome-level genome assembly of four amphioxus species, B. floridae, B. lanceolatum, B. belcheri and B. japonicum ( Putnam et al, 2008 ; Marlétaz et al, 2018 ; Brasó-Vives et al, 2022 ; Huang et al, 2023 ; Huang et al, 2014 ), thus opening the door to functional and comparative genomics studies. The use of new sequencing techniques at the level of single cells has been producing significant amount of information in recent years in various animal models.…”

“…Amphioxus genomic data also helped reconstructing the chordate ancestral karyotype, and the evolution of gene families in this clade. Finally, recent epigenomic analyses showed that chromatin conformation evolution ( Acemel et al, 2016 ; Huang et al, 2023 ) and complexification of developmental gene regulation ( Marlétaz et al, 2018 ) and of the interconnectivity between signalling pathways ( Gil-Gálvez et al, 2022 ) might have participated to the emergence of vertebrate specific traits.…”

“…Moreover, the regulation of gene expression is much simpler than in vertebrates ( Gil-Gálvez et al, 2022 ). And although it is still a point of debate, the amphioxus three-dimensional chromatin structure also seems to be less complicated than the vertebrate’s one ( Acemel et al, 2016 ; Huang et al, 2023 ). Altogether, the crucial phylogenetic position, conserved morphological traits and genome organization make amphioxus a useful organism for answering fundamental questions in biology, particularly with respect to vertebrate evolution.…”

Gene Novelties in Amphioxus Illuminate the Early Evolution of Deuterostomes

“…Therefore, amphioxus is considered an irreplaceable model organism for evolutionary studies. With the advent of high-throughput sequencing, genome-based investigation has revolutionized the study of amphioxus evolution and greatly expanded our knowledge of the origin and evolution of vertebrates (Holland et al 2008; Putnam et al 2008; Huang et al 2014; Acemel et al 2016; Marlétaz et al 2018; Simakov et al 2020; Brasó-Vives et al 2022; Huang et al 2023). Whole-genome comparison of the three chordate groups provided evidence supporting the 2R hypothesis, which posits that two rounds of whole-genome duplication occurred in the early vertebrate lineage (Holland et al 2008; Putnam et al 2008).…”