Seadragon genome analysis provides insights into its phenotype and sex determination locus

Qu, Meng; Liu, Yali; Zhang, Yanhong; Wan, Shiming; Ravi, Vydianathan; Qin, Geng; Jiang, Han; Wang, Xin; Zhang, Huixian; Zhang, Bo; Gao, Zexia; Huysseune, Ann; Zhang, Zhixin; Zhang, Hao; Chen, Zelin; Yu, Haiyan; Wu, Yongli; Tang, Lu; Li, Chunyan; Zhong, Jia; Ma, Liming; Wang, Fengling; Zheng, Hongkun; Yin, Jingdong; Witten, P. Eckhard; Meyer, Axel; Venkatesh, Byrappa; Lin, Qiang

doi:10.1126/sciadv.abg5196

Cited by 46 publications

(56 citation statements)

References 68 publications

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“…mossambicus . These results are in sharp contrast to the sex determining systems shared among several closely related species in other fish lineages, for example, the male-specific amhy in 11 Esociformes species ( Pan et al, 2021a ) and amhr2y in two seadragons ( Qu et al, 2021 ). A rapid turnover of sex chromosomes and sex-determining genes may have contributed to the adaptative radiation in tilapia and other cichlids ( Ser et al, 2010 ; Ronco et al, 2021 ).…”

Section: Discussioncontrasting

confidence: 82%

A Chromosome-Level Genome Assembly of Mozambique Tilapia (Oreochromis mossambicus) Reveals the Structure of Sex Determining Regions

et al. 2021

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The Mozambique tilapia (Oreochromis mossambicus) is a fascinating taxon for evolutionary and ecological research. It is an important food fish and one of the most widely distributed tilapias. Because males grow faster than females, genetically male tilapia are preferred in aquaculture. However, studies of sex determination and sex control in O. mossambicus have been hindered by the limited characterization of the genome. To address this gap, we assembled a high-quality genome of O. mossambicus, using a combination of high coverage of Illumina and Nanopore reads, coupled with Hi-C and RNA-Seq data. Our genome assembly spans 1,007 Mb with a scaffold N50 of 11.38 Mb. We successfully anchored and oriented 98.6% of the genome on 22 linkage groups (LGs). Based on re-sequencing data for male and female fishes from three families, O. mossambicus segregates both an XY system on LG14 and a ZW system on LG3. The sex-patterned SNPs shared by two XY families narrowed the sex determining regions to ∼3 Mb on LG14. The shared sex-patterned SNPs included two deleterious missense mutations in ahnak and rhbdd1, indicating the possible roles of these two genes in sex determination. This annotated chromosome-level genome assembly and identification of sex determining regions represents a valuable resource to help understand the evolution of genetic sex determination in tilapias.

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Section: Discussioncontrasting

confidence: 82%

A Chromosome-Level Genome Assembly of Mozambique Tilapia (Oreochromis mossambicus) Reveals the Structure of Sex Determining Regions

et al. 2021

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“…With these genome models and rich accompanying data, we add to the existing collection of high-quality genomic tools and insights for several syngnathid groups, including genera Syngnathus ( 8 , 9 ), Hippocampus ( 10 , 11 ), Microphis ( 12 ), and most recently (published as of the writing of this paper) Phyllopteryx and Syngnathoides ( 13 ). Such tools are useful in illuminating the evolution and development of puzzling syngnathid novelties such as male pregnancy and leaf-like appendages.…”

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confidence: 99%

Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes

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et al. 2022

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

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Seadragons are a remarkable lineage of teleost fishes in the family Syngnathidae, renowned for having evolved male pregnancy. Comprising three known species, seadragons are widely recognized and admired for their fantastical body forms and coloration, and their specific habitat requirements have made them flagship representatives for marine conservation and natural history interests. Until recently, a gap has been the lack of significant genomic resources for seadragons. We have produced gene-annotated, chromosome-scale genome models for the leafy and weedy seadragon to advance investigations of evolutionary innovation and elaboration of morphological traits in seadragons as well as their pipefish and seahorse relatives. We identified several interesting features specific to seadragon genomes, including divergent noncoding regions near a developmental gene important for integumentary outgrowth, a high genome-wide density of repetitive DNA, and recent expansions of transposable elements and a vesicular trafficking gene family. Surprisingly, comparative analyses leveraging the seadragon genomes and additional syngnathid and outgroup genomes revealed striking, syngnathid-specific losses in the family of fibroblast growth factors (FGFs), which likely involve reorganization of highly conserved gene regulatory networks in ways that have not previously been documented in natural populations. The resources presented here serve as important tools for future evolutionary studies of developmental processes in syngnathids and hold value for conservation of the extravagant seadragons and their relatives.

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“…Gene duplication/insertion is one of the most important mechanisms for the origin of new SD genes, which could suppress recombination more readily than allelic diversification [49,50]. Male-specific duplication of amhr2 has been identified in four species of teleosts, namely yellow perch [35], ayu [36], common seadragon and alligator pipefish [37]. Our present study provided a new example of an amhr2 duplication event.…”

Section: Discussionmentioning

confidence: 71%

Identification of sex chromosome and sex-determining gene of southern catfish ( Silurus meridionalis ) based on XX, XY and YY genome sequencing

et al. 2022

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Teleosts are important models to study sex chromosomes and sex-determining (SD) genes because they present a variety of sex determination systems. Here, we used Nanopore and Hi-C technologies to generate a high-contiguity chromosome-level genome assembly of a YY southern catfish ( Silurus meridionalis ). The assembly is 750.0 Mb long, with contig N50 of 15.96 Mb and scaffold N50 of 27.22 Mb. We also sequenced and assembled an XY male genome with a size of 727.2 Mb and contig N50 of 13.69 Mb. We identified a candidate SD gene through comparisons to our previous assembly of an XX individual. By resequencing male and female pools, we characterized a 2.38 Mb sex-determining region (SDR) on Chr24. Analysis of read coverage and comparison of the X and Y chromosome sequences showed a Y specific insertion (approx. 500 kb) in the SDR which contained a male-specific duplicate of amhr2 (named amhr2y ). amhr2y and amhr2 shared high-nucleotide identity (81.0%) in the coding region but extremely low identity in the promotor and intron regions. The exclusive expression in the male gonadal primordium and loss-of-function inducing male to female sex reversal confirmed the role of amhr2y in male sex determination. Our study provides a new example of amhr2 as the SD gene in fish and sheds light on the convergent evolution of the duplication of AMH/AMHR2 pathway members underlying the evolution of sex determination in different fish lineages.

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Seadragon genome analysis provides insights into its phenotype and sex determination locus

Cited by 46 publications

References 68 publications

A Chromosome-Level Genome Assembly of Mozambique Tilapia (Oreochromis mossambicus) Reveals the Structure of Sex Determining Regions

A Chromosome-Level Genome Assembly of Mozambique Tilapia (Oreochromis mossambicus) Reveals the Structure of Sex Determining Regions

Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes

Identification of sex chromosome and sex-determining gene of southern catfish ( Silurus meridionalis ) based on XX, XY and YY genome sequencing

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