Three amphioxus reference genomes reveal gene and chromosome evolution of chordates

Huang, Zhen; Xu, Luohao; Cai, Changqing; Zhou, Yitao; Liu, Jing; Zhu, Zexian; Kang, Wen; Chen, Duo; Pei, Surui; Xue, Ting; Wan, Chengsong; Shi, Chenggang; Wu, Xiaotong; Huang, Yongji; Xu, Chaohua; Yan, Yanan; Yang, Ying; He, Wenjing; Hu, Xuefeng; Zhang, Yanding; Chen, Youqiang; Bi, Changwei; He, Chunpeng; Xue, Lingzhan; Xiao, Shijun; Yue, Zhicao; Jiang, Yu; Yu, Jr-Kai; Jarvis, Erich D.; Li, Guang; Lin, Gang; Zhang, Qiujin; Zhou, Qi

doi:10.1101/2022.01.04.475009

Cited by 6 publications

(20 citation statements)

References 128 publications

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“…That is, none of the B. belcheri scaffolds map to both chromosomes 9 and 11 of B.floridae or to both chromosomes 15 and 19 of B. lanceolatum . These results match recent evidence on B. belcheri and B.floridae karyotype reconstruction, pointing towards a chromosomal fusion in the B. floridae branch with respect to B. belcheri [11]. Here, we show that this chromosomal fusion is B. floridae specific (is not shared with B. lanceolatum ) and that there is an additional chromosomal fusion in B. lanceolatum .…”

Section: Resultssupporting

confidence: 92%

“…While there is also an enrichment in orthogroups which are single-copy in both lineages (1.09 times more than expected), it is less strong than the enrichment of parallel small-scale duplication. These results are robust to the inclusion of lineage-specific genes in the analysis (Figure S3, Table S2) and are consistent with recent observations in other amphioxus species [11]. Moreover, duplicated orthogroups with a low number of gene copies (<=2.5 mean number of genes) in amphioxus tend to have a low number of copies in vertebrates (Spearman’s ᵨ = 0.28; Table S3, contingency table chi-squared test p-value < 0.0001).…”

Section: Resultssupporting

confidence: 90%

“…While one-to-one orthologs show an overall conservation of synteny between the two species, there are also two important chromosomal rearrangements (Figure 6). belcheri [11]. Here, we show that this chromosomal fusion is B. floridae speci c (is not shared with B. lanceolatum) and that there is an additional chromosomal fusion in B. lanceolatum.…”

Section: Amphioxus Gene Syntenymentioning

confidence: 59%

“…The density of the distribution of this di erence in expression between B. lanceolatum and D. rerio is shown for four di erent types of orthologous genes: genes that are single-copy in both species ( rst row); zebra sh ohnolog genes that are orthologs to B. lanceolatum single-copy genes (second row); zebra sh small-scale duplicates that are orthologs to single-copy B. lanceolatum genes (third row); and zebra sh single-copy genes that are orthologs to small-scale duplicates B. lanceolatum genes (fourth row). Black arrows highlight the direction of the skewness (when present) of the one-to-one gene comparisons belcheri [11]. Here, we show that this chromosomal fusion is B. floridae speci c (is not shared with B. lanceolatum) and that there is an additional chromosomal fusion in B. lanceolatum.…”

Section: Expression and Evolution Of Duplicate Genesmentioning

confidence: 66%

“…When building a genome assembly, duplicated sequences must neither be collapsed into a single region nor placed as alternative haplotypes [27,28]. Thus, assembling the genome with long-read and long-distance data, as well as using haplotype collapsing methods, is critical to the study of gene duplications in amphioxus [11].…”

Section: Introductionmentioning

confidence: 99%

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Parallel evolution of amphioxus and vertebrate small-scale gene duplications

Brasó-Vives

Marlétaz

Echchiki

et al. 2022

Preprint

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Background: Amphioxus are non-vertebrate chordates characterized by a slow morphological and molecular evolution. They share the basic chordate body-plan and genome organization with vertebrates but lack their '2R' whole-genome duplications and their developmental complexity. For these reasons, amphioxus are frequently used as an outgroup to study vertebrate genome evolution and Evo-Devo. Aside from whole-genome duplications, genes continuously duplicate on a smaller scale. Small-scale duplicated genes can be found in both amphioxus and vertebrate genomes, while only the vertebrate genome has duplicated genes product of their 2R whole-genome duplications. Here, we explore the history of small-scale gene duplications in the amphioxus lineage and compare it to small- and large-scale gene duplication history in vertebrates. Results: We present a study of the European amphioxus (Branchiostoma lanceolatum) gene duplications thanks to a new, high-quality genome reference. We find that, despite its overall slow molecular evolution, the amphioxus lineage has had a history of small-scale duplications similar to the one observed in vertebrates. We find parallel gene duplication profiles between amphioxus and vertebrates, and conserved functional constraints in gene duplication. Moreover, amphioxus gene duplicates show levels of expression and patterns of functional specialization similar to the ones observed in vertebrate duplicated genes. We also find strong conservation of gene synteny between two distant amphioxus species, B. lanceolatum and B. floridae, with two major chromosomal rearrangements. Conclusions: In contrast to their slower molecular and morphological evolution, amphioxus small-scale gene duplication history resembles that of the vertebrate lineage both in quantitative and in functional terms.

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Section: Resultssupporting

confidence: 92%

Section: Resultssupporting

confidence: 90%

Section: Amphioxus Gene Syntenymentioning

confidence: 59%

Section: Expression and Evolution Of Duplicate Genesmentioning

confidence: 66%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Parallel evolution of amphioxus and vertebrate small-scale gene duplications

Brasó-Vives

Marlétaz

Echchiki

et al. 2022

Preprint

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Three amphioxus reference genomes reveal gene and chromosome evolution of chordates

Huang

Cai

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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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.

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Evolutionary analysis of a complete chicken genome

Huang

Bai

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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Microchromosomes are prevalent in nonmammalian vertebrates [P. D. Waters et al. , Proc. Natl. Acad. Sci. U.S.A. 118 (2021)], but a few of them are missing in bird genome assemblies. Here, we present a new chicken reference genome containing all autosomes, a Z and a W chromosome, with all gaps closed except for the W. We identified ten small microchromosomes (termed dot chromosomes) with distinct sequence and epigenetic features, among which six were newly assembled. Those dot chromosomes exhibit extremely high GC content and a high level of DNA methylation and are enriched for housekeeping genes. The pericentromeric heterochromatin of dot chromosomes is disproportionately large and continues to expand with the proliferation of satellite DNA and testis-expressed genes. Our analyses revealed that the 41-bp CNM repeat frequently forms higher-order repeats (HORs) at the centromeres of acrocentric chromosomes. The centromere core regions where the kinetochore attaches often encompass telomeric sequence (TTAGGG)n, and in a one of the dot chromosomes, the centromere core recruits an endogenous retrovirus (ERV). We further demonstrate that the W chromosome shares some common features with dot chromosomes, having large arrays of hypermethylated tandem repeats. Finally, using the complete chicken chromosome models, we reconstructed a fine picture of chordate karyotype evolution, revealing frequent chromosomal fusions before and after vertebrate whole-genome duplications. Our sequence and epigenetic characterization of chicken chromosomes shed insights into the understanding of vertebrate genome evolution and chromosome biology.

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Three amphioxus reference genomes reveal gene and chromosome evolution of chordates

Cited by 6 publications

References 128 publications

Parallel evolution of amphioxus and vertebrate small-scale gene duplications

Parallel evolution of amphioxus and vertebrate small-scale gene duplications

Three amphioxus reference genomes reveal gene and chromosome evolution of chordates

Evolutionary analysis of a complete chicken genome

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