Ancient homomorphy of molluscan sex chromosomes sustained by reversible sex-biased genes and sex determiner translocation

Han, Wentao; Liu, Liangjie; Wang, Jing; He, Wei; Li, Yuli; Zhang, Lijing; Guo, Zhenyi; Li, Yajuan; Liu, Tian; Zeng, Qifan; Xing, Qiang; Shu, Ya; Wang, Tong; Yang, Yaxin; Zhang, Meiwei; Li, Ruojiao; Yu, Jiangyong; Pu, Zhongqi; Lv, Jia; Lian, Shanshan; Hu, Jiang; Hu, Xiaoli; Bao, Zhenmin; Bao, Lisui; Zhang, Lingling; Wang, Shi

doi:10.1038/s41559-022-01898-6

Cited by 38 publications

(17 citation statements)

References 134 publications

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“…In general, high degrees of synteny have been observed across much of Pteriomorphia, including between scallop species (Han et al 2022), between scallop and ark clam genomes (Bao et al 2021), and scallop versus Mytilidae comparisons (Yang et al 2021). The most extensive genome rearrangements in Pteriomorphia are in the oysters, which have notably fewer chromosomes (e.g., Gundappa et al 2022) than groups such as scallops.…”

Section: Resultsmentioning

confidence: 99%

Chromosome-level genome assembly of the disco clam,Ctenoides ales, a first for the bivalve order Limida

McElroy,

Masonbrink,

Chudalayandi

et al. 2024

Preprint

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The bivalve subclass Pteriomorphia, which includes the economically important scallops, oysters, mussels, and ark clams, exhibits extreme ecological, morphological, and behavioral diversity. Among this diversity are five morphologically distinct eye types, making Pteriomorphia an excellent setting to explore the molecular basis for the evolution of novel traits. Of pteriomorphian bivalves, Limida is the only order lacking genomic resources, greatly limiting the potential phylogenomic analyses related to eyes and phototransduction. Here, we present the first limid genome assembly, the disco clam,Ctenoides ales, which is characterized by invaginated eyes, exceptionally long tentacles, and a flashing light display. This genome assembly was constructed with PacBio long reads and Dovetail Omni-CTMproximity-ligation sequencing. The final assembly is ~2.3Gb and over 99% of the total length is contained in 18 pseudomolecule scaffolds. We annotated 41,064 protein coding genes and report a BUSCO completeness of 91.9% for metazoa_obd10. Additionally, we report the completely annotated mitochondrial genome, also a first for Limida. The ~20Kb mitogenome has 12 protein coding genes, 22 tRNAs, 2 rRNA genes, and a 1,589 bp duplicated sequence containing the origin of replication. TheC. alesnuclear genome size is substantially larger than other pteriomorphian genomes, mainly accounted for by transposable element sequences. We inventoried the genome for opsins, the signaling proteins that initiate phototransduction, and found that, unlike its closest eyed-relatives, the scallops,C. aleslacks duplication of the rhabdomeric Gq-coupled opsin that is typically used for invertebrate vision. In fact,C. aleshas uncharacteristically few opsins relative to the other pteriomorphian families, all of which have unique expansions of xenopsins, a recently discovered opsin subfamily. This chromosome-level assembly, along with the mitogenome, will be valuable resources for comparative genomics and phylogenetics in bivalves and particularly for the understudied but charismatic limids.

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Section: Resultsmentioning

confidence: 99%

Chromosome-level genome assembly of the disco clam,Ctenoides ales, a first for the bivalve order Limida

McElroy,

Masonbrink,

Chudalayandi

et al. 2024

Preprint

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“…Indeed, Foxl2 also behaves in a dose-dependent manner in some turtle species where its overexpression at the embryonic stage can induce male-to-female sex reversal in ZZ soft-shelled turtles ( Pelodiscus sinensis ) and female differentiation in male-temperature-incubated red-eared sliders ( Trachemys scripta ) (Jin et al 2022; Ma et al 2022). Importantly, Dmrt1 has been recruited to act as a primary sex determining gene in multiple taxa (Matson and Zarkower, 2012), while Foxl2 has remained mysteriously absent from this list—with the singular putative exception being recently described in some species of bivalve mollusks (Han et al 2022). Thus, the identification of both Foxl2 and a duplicated Foxl2 copy in the W-limited region of the Shinisaurus genome supports the expanded list of the “usual suspects” that might act as the PSD in vertebrates.…”

Section: Discussionmentioning

confidence: 99%

It’s a Trap?! Escape from an ancient, ancestral sex chromosome system and implication ofFoxl2as the putative primary sex determining gene in a lizard (Anguimorpha; Shinisauridae)

Pinto,

Nielsen,

Sullivan

et al. 2023

Preprint

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Although sex determination is ubiquitous in vertebrates, mechanisms of sex determination vary from environmentally- to genetically-influenced. Genetic sex determination is typically accomplished with sex chromosomes via the presence/absence of a specific allele at a genetic locus, which initiates the sex determination signaling network. In vertebrates, well-studied groups like mammals and birds maintain conserved sex chromosome systems (XY and ZW, respectively), while sex chromosomes in many other clades may not be conserved across long evolutionary timeframes. Among squamate reptiles, for example, some groups are relatively stable, like iguanids (Pleurodonta), caenophidian snakes (Caenophidia), and lacertids (Lacertidae) while others are highly variable in their modes of sex determination, such as geckos (Gekkota) and the clade containing chameleons and dragon lizards (Acrodonta). One group inferred to have an evolutionarily stable mode of sex determination is the Anguimorpha, a clade of charismatic taxa, including monitor lizards (Varanus), beaded lizards (Heloderma), glass lizards (Ophisaurus), and the crocodile lizard (Shinisaurus crocodilurus). The most recent common ancestor to extant anguimorphs possessed a ZW system that has been retained across the clade. However, determination of sex chromosomes in some anguimorph species has remained elusive including in the endangered, monotypic family of crocodile lizards (Shinisauridae). Here, we use a combination of whole genome re-sequencing and RADseq to demonstrate that S. crocodilurus has replaced the ancestral anguimorph ZW system on their LG7 chromosome with a novel ZW system on LG3. The syntenic region that corresponds with this linkage group in chicken is chromosome 9, and this is the first documented use of this syntenic block as a sex chromosome in amniotes. Additionally, this ~1Mb region harbors approximately 10 genes, including a duplication of the well-characterized transcription factor, Foxl2, a critical locus for the maintenance of sexual differentiation in vertebrates, and thus a putative primary sex determining gene for S. crocodilurus.

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“…For example, in Phylum Mollusca, Class Bivalvia, there are gonochoric species with genetic sex determination in the absence of heteromorphic chromosomes and hermaphroditic species in which male and female gonadal material are present in the same individual, either simultaneously (e.g., bay scallop, Argopecten irradians ) or sequentially (Breton et al, 2018; Wei et al, 2021). A recent comparative phylogenomic survey of sex in the family Pectinidae suggests that sex chromosome homomorphy in gonochoric scallop species evolved as early as 350 million years ago via repetitive element‐driven chromosomal rearrangement and has been maintained through regulatory flexibility of sex‐related genes during gonadal development (Han et al, 2022). Among bivalve hermaphrodites, sequential hermaphrodites can be female first (protogynous; e.g., Asian clam, Corbicula fluminalis ), male first (protandrous; e.g., pearl oyster, Pinctada margaritifera ), or capable of alternating between sexes within a single reproductive season such as the European flat oyster, Ostrea edulis (Joyce et al, 2013; Morton, 1982; Teaniniuraitemoana et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

Sex‐specific gene expression in eastern oyster, Crassostrea virginica, gonad and mantle tissues

Proestou,

Delomas,

Sullivan

et al. 2024

Invertebrate Biology

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The eastern oyster (Crassostrea virginica) is a protandrous hermaphrodite of commercial importance. As with many marine invertebrates, little is known about sex determination and differentiation systems in this species. Such knowledge has important implications not only for understanding the evolution of sex but also for applied questions in aquaculture. In order to examine mechanistic differences in reproductive development between the sexes, we compared the transcriptomes of gonad and mantle tissues from six male and six female oysters. A total of 7675 transcripts were differentially expressed between male and female gonads (3936 and 3739 were upregulated in males and females, respectively). Transcripts identified include those associated with sex in other invertebrate and vertebrate species such as Dmrt1, Sox‐30, Bindin, Dpy‐30, and Histone H4 in males and Foxl2, Vitellogenin, and Bystin in females. GO terms associated with transcripts upregulated in male gonads include protein modification, reproductive process, and cell projection organization, whereas RNA metabolic process and amino acid metabolic process were associated with transcripts upregulated in females. Far fewer transcripts were differentially expressed between male and female mantle tissues, with 87 transcripts upregulated in females and 16 upregulated in males. However, 41% of transcripts identified as differentially expressed between mantle tissues were also differentially expressed between male and female gonads including Histone H4 and Bystin. This study represents the first characterization of eastern oyster male and female gonad transcriptomes. We further identify differing expression profiles between male and female mantle tissues, which provides evidence for sex‐specific functions of the mantle and suggests that this tissue could harbor biomarkers for identifying oyster sex non‐destructively.

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Ancient homomorphy of molluscan sex chromosomes sustained by reversible sex-biased genes and sex determiner translocation

Cited by 38 publications

References 134 publications

Chromosome-level genome assembly of the disco clam,Ctenoides ales, a first for the bivalve order Limida

Chromosome-level genome assembly of the disco clam,Ctenoides ales, a first for the bivalve order Limida

It’s a Trap?! Escape from an ancient, ancestral sex chromosome system and implication ofFoxl2as the putative primary sex determining gene in a lizard (Anguimorpha; Shinisauridae)

Sex‐specific gene expression in eastern oyster, Crassostrea virginica, gonad and mantle tissues

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