Repeated translocation of a supergene underlying rapid sex chromosome turnover in
            <i>Takifugu</i>
            pufferfish

Ahammad, Kabir; Ieda, Risa; Fujikawa, Daigaku; Atsumi, K.; Tajima, S.; Nozawa, Akiko; Koyama, Takashi; Hirase, Shotaro; Nakamura, Osamu; Kadota, Mitsutaka; Nishimura, Osamu; Kuraku, Shigehiro; Nakamura, Yasukazu; Kobayashi, Hisato; Toyoda, Atsushi; Tasumi, Satoshi; Kikuchi, Kiyoshi

doi:10.1073/pnas.2121469119

Cited by 27 publications

(10 citation statements)

References 81 publications

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“…Initially, the paralogs of S ‐locus genes were likely distributed among different chromosomes, and subsequently, through independent duplications, they were inserted into the same genomic location. Notably, the contribution of TEs to duplication and translocation events in animals and plants has been well‐established (S. Yang et al ., 2008; Kabir et al ., 2022; Kim et al ., 2022). The accumulation of TEs in the S ‐locus region of N. indica supports our hypothesis that TEs likely facilitated the movement and insertion of genes during this process.…”

Section: Discussionmentioning

confidence: 99%

Haplotype‐resolved genome assembly provides insights into the evolution of S‐locus supergene in distylous Nymphoides indica

Yang,

Xue,

et al. 2023

New Phytologist

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Summary Distyly has evolved independently in numerous animal‐pollinated angiosperm lineages. Understanding of its molecular basis has been restricted to a few species, primarily Primula. Here, we investigate the genetic architecture of the single diallelic locus (S‐locus) supergene, a linkage group of functionally associated genes, and explore how it may have evolved in distylous Nymphoides indica, a lineage of flowering plants not previously investigated. We assembled haplotype‐resolved genomes, used read‐coverage‐based genome‐wide association study (rb‐GWAS) to locate the S‐locus supergene, co‐expression network analysis to explore gene networks underpinning the development of distyly, and comparative genomic analyses to investigate the origins of the S‐locus supergene. We identified three linked candidate S‐locus genes – NinBAS1, NinKHZ2, and NinS1 – that were only evident in the short‐styled morph and were hemizygous. Co‐expression network analysis suggested that brassinosteroids contribute to dimorphic sex organs in the short‐styled morph. Comparative genomic analyses indicated that the S‐locus supergene likely evolved via stepwise duplications and has been affected by transposable element activities. Our study provides novel insight into the structure, regulation, and evolution of the supergene governing distyly in N. indica. It also provides high‐quality genomic resources for future research on the molecular mechanisms underlying the striking evolutionary convergence in form and function across heterostylous taxa.

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Section: Discussionmentioning

confidence: 99%

Haplotype‐resolved genome assembly provides insights into the evolution of S‐locus supergene in distylous Nymphoides indica

Yang,

Xue,

et al. 2023

New Phytologist

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“…Sex chromosome turnovers are classified into homogametic (XY to XY, or ZW to ZW) and heterogametic transitions (XY to ZW, or ZW to XY) (Bull, 1983; Saunders et al, 2018), and (van Doorn and Kirkpatrick, 2010) introduced the categories of nonhomologous transitions (the sex-linked region is on a different chromosome, and the old sex chromosome or linkage group becomes an autosome) versus homologous transitions (with no major change in location of the sex determining region); predictions for these two types of changes were reviewed by (Bull, 1983). A change to a different region within the same chromosome is also possible (Ieda et al, 2018; Kabir et al, 2022). The Salicaceae display all these types (Yang et al, 2021; Li et al, 2022; Wang et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

Gap-free X and Y chromosomes ofSalix arbutifoliareveal an evolutionary change from male to female heterogamety in willows, without a change in the sex-determining region

Wang,

Gong,

Zhang

et al. 2023

Preprint

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In theVetrixclade ofSalix, a genus of woody flowering plants, sex determination involves chromosome 15, but an XY system has changed to a ZW system. We used genome sequencing (with chromosome conformation capture (Hi-C) and PacBio HiFi high-fidelity reads) to study the evolutionary history of the sex-linked regions before and after the transition. We assembled chromosome level gap-free X and Y chromosomes ofSalix arbutifolia, and distinguished the haplotypes in the 15X- and 15Y-linked regions. This revealed “micro-heteromorphism” differentiating the haplotypes of the Y- and X-linked regions, including insertions, deletions and duplications. Unusually, the X-linked region is considerably larger than the corresponding Y region, and we show that this primarily reflects extensive accumulation of repetitive sequences and gene duplications. The phylogenies of single-copy orthogroups within the sex-linked regions ofS. arbutifolia(X and Y) andS. purpurea(Z and W) indicate that they possess a common ancestral sex-linked region that is physically small and located in a repeat-rich region near the chromosome 15 centromere. During the change in heterogamety, the W-linked region was derived from the X-linked one and the Z from the Y. The W may subsequently have evolved a region in which recombination became suppressed. We also detected accumulation of genes with opposite sex-biases in the sex-linked regions.

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“…in Ty3/Gypsy elements in papaya 56 ), and even temporarily increase the size of the heterogametic chromosome at the early stage of differentiation 57 . The presence of TEs in the sex-determining region may also facilitate translocation of the sex-determining factor either via transposition or via ectopic recombination, potentially leading to the rise of a new sex chromosome pair 58 , 59 , or influence the expression of neighbouring genes. For instance, TE-induced methylation of a transcription factor realizes sex determination in melon 60 .…”

Section: Discussionmentioning

confidence: 99%

Accumulation of retrotransposons contributes to W chromosome differentiation in the willow beauty Peribatodes rhomboidaria (Lepidoptera: Geometridae)

Hejníčková

Dalíková

Zrzavá

et al. 2023

Sci Rep

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The W chromosome of Lepidoptera is typically gene-poor, repeat-rich and composed of heterochromatin. Pioneering studies investigating this chromosome reported an abundance of mobile elements. However, the actual composition of the W chromosome varies greatly between species, as repeatedly demonstrated by comparative genomic hybridization (CGH) or fluorescence in situ hybridization (FISH). Here we present an analysis of repeats on the W chromosome in the willow beauty, Peribatodesrhomboidaria (Geometridae), a species in which CGH predicted an abundance of W-enriched or W-specific sequences. Indeed, comparative analysis of male and female genomes using RepeatExplorer identified ten putative W chromosome-enriched repeats, most of which are LTR or LINE mobile elements. We analysed the two most abundant: PRW LINE-like and PRW Bel-Pao. The results of FISH mapping and bioinformatic analysis confirmed their enrichment on the W chromosome, supporting the hypothesis that mobile elements are the driving force of W chromosome differentiation in Lepidoptera. As the W chromosome is highly underrepresented in chromosome-level genome assemblies of Lepidoptera, this recently introduced approach, combining bioinformatic comparative genome analysis with molecular cytogenetics, provides an elegant tool for studying this elusive and rapidly evolving part of the genome.

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Repeated translocation of a supergene underlying rapid sex chromosome turnover in Takifugu pufferfish

Cited by 27 publications

References 81 publications

Haplotype‐resolved genome assembly provides insights into the evolution of S‐locus supergene in distylous Nymphoides indica

Haplotype‐resolved genome assembly provides insights into the evolution of S‐locus supergene in distylous Nymphoides indica

Gap-free X and Y chromosomes ofSalix arbutifoliareveal an evolutionary change from male to female heterogamety in willows, without a change in the sex-determining region

Accumulation of retrotransposons contributes to W chromosome differentiation in the willow beauty Peribatodes rhomboidaria (Lepidoptera: Geometridae)

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