Genome-wide SNP analysis of Siamese cobra (Naja kaouthia) reveals the molecular basis of transitions between Z and W sex chromosomes and supports the presence of an ancestral super-sex chromosome in amniotes

Laopichienpong, Nararat; Kraichak, Ekaphan; Singchat, Worapong; Sillapaprayoon, Siwapech; Muangmai, Narongrit; Suntrarachun, Sunutcha; Baicharoen, Sudarath; Peyachoknagul, Surin; Chanhome, Lawan; Ezaz, Tariq; Srikulnath, Kornsorn

doi:10.1016/j.ygeno.2020.09.058

Cited by 17 publications

(47 citation statements)

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“…Although transposable elements can be dispersed on many chromosomes or even throughout the entire genome, large amplification of the elements are often found on sex chromosomes in many organisms ( Ahmad et al, 2020 ; Koomgun et al, 2020 ; Laopichienpong et al, 2020 ; Yoshido et al, 2020 ). The presence of accumulated TEs leads to the establishment of heterochromatin, and possibly also to TE recombination between non-homologous copies.…”

Section: Discussionmentioning

confidence: 99%

“…This suggests that the XX/XY sex determination system might co-exist with ZZ/ZW system in the same individuals of C. gariepinus. Genomic convergence has been detected by comparative cytogenetics studies in which unrelated sex chromosomes share sex chromosomal linkage homologies across distantly related species (Srikulnath et al, 2014(Srikulnath et al, , 2015Ahmad et al, 2020;Koomgun et al, 2020;Laopichienpong et al, 2020;Singchat et al, 2020a,b). We found that a male-linked locus under the 70:30 criterion shared partial homology with ADD3 which is localized on GGA6, which is further orthologous to sex chromosomes of sand lizard (Lacerta agilis).…”

Section: Discussionmentioning

confidence: 99%

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An Investigation of ZZ/ZW and XX/XY Sex Determination Systems in North African Catfish (Clarias gariepinus, Burchell, 1822)

et al. 2021

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An investigation of sex-specific loci may provide important insights into fish sex determination strategies. This may be useful for biotechnological purposes, for example, to produce all-male or all-female fish for commercial breeding. The North African catfish species, Clarias gariepinus, has been widely adopted for aquaculture because its superior growth and disease resistance render the species suitable for hybridization with other catfish to improve the productivity and quality of fish meat. This species has either a ZZ/ZW or XX/XY sex determination system. Here, we investigate and characterize these systems using high-throughput genome complexity reduction sequencing as Diversity Arrays Technology. This approach was effective in identifying moderately sex-linked loci with both single-nucleotide polymorphisms (SNPs) and restriction fragment presence/absence (PA) markers in 30 perfectly sexed individuals of C. gariepinus. However, SNPs based markers were not found in this study. In total, 41 loci met the criteria for being moderately male-linked (with male vs. female ratios 80:20 and 70:30), while 25 loci were found to be moderately linked to female sex. No strictly male- or female-linked loci were detected. Seven moderately male-linked loci were partially homologous to some classes of transposable elements and three moderately male-linked loci were partially homologous to functional genes. Our data showed that the male heterogametic XX/XY sex determination system should co-exist with the ZZ/ZW system in C. gariepinus. Our finding of the co-existence of XX/XY and ZZ/ZW systems can be applied to benefit commercial breeding of this species in Thailand. This approach using moderately sex-linked loci provides a solid baseline for revealing sex determination mechanisms and identify potential sex determination regions in catfish, allowing further investigation of genetic improvements in breeding programs.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

An Investigation of ZZ/ZW and XX/XY Sex Determination Systems in North African Catfish (Clarias gariepinus, Burchell, 1822)

et al. 2021

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“…During the time, chromosome rearrangements fragmented the ancestral "super-sex chromosome", but some of the emerged chromosomes still maintain the role as sex chromosomes in extant, phylogenetically distant lineages of amniotes. The major support for this hypothesis originates from the partial similarity of the sex chromosome gene content between birds, monotremes and the gecko Gekko hokouensis [8][9][10][11][12][13][14], as well as between viviparous mammals and lacertid lizards [12]. The hypothesis of the ancestral GSD expects that ESD evolved multiple times within amniotes and that ESD can be phylogenetically nested within a paraphyletic group whose members share homologous GSD.…”

Section: Introductionmentioning

confidence: 99%

Independent Evolution of Sex Chromosomes in Eublepharid Geckos, A Lineage with Environmental and Genotypic Sex Determination

Pensabene

Kratochvíl

Rovatsos

2020

Life

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Geckos demonstrate a remarkable variability in sex determination systems, but our limited knowledge prohibits accurate conclusions on the evolution of sex determination in this group. Eyelid geckos (Eublepharidae) are of particular interest, as they encompass species with both environmental and genotypic sex determination. We identified for the first time the X-specific gene content in the Yucatán banded gecko, Coleonyx elegans, possessing X1X1X2X2/X1X2Y multiple sex chromosomes by comparative genome coverage analysis between sexes. The X-specific gene content of Coleonyx elegans was revealed to be partially homologous to genomic regions linked to the chicken autosomes 1, 6 and 11. A qPCR-based test was applied to validate a subset of X-specific genes by comparing the difference in gene copy numbers between sexes, and to explore the homology of sex chromosomes across eleven eublepharid, two phyllodactylid and one sphaerodactylid species. Homologous sex chromosomes are shared between Coleonyx elegans and Coleonyx mitratus, two species diverged approximately 34 million years ago, but not with other tested species. As far as we know, the X-specific gene content of Coleonyx elegans / Coleonyx mitratus was never involved in the sex chromosomes of other gecko lineages, indicating that the sex chromosomes in this clade of eublepharid geckos evolved independently.

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“…This might involve genomic regions orthologous to squamate chromosome 2 (SR2) and snake W sex chromosomes (Matsubara et al, 2006(Matsubara et al, , 2012(Matsubara et al, , 2019Srikulnath et al, 2009aSrikulnath et al, ,b, 2013Srikulnath et al, , 2014Srikulnath et al, , 2015Alföldi et al, 2011;Pokorná et al, 2011;Uno et al, 2012;Matsuda et al, 2015;Ezaz et al, 2017;Singchat et al, 2018Singchat et al, , 2020a. Comparison of genomewide single-nucleotide polymorphisms (SNPs) between males and females of the Siamese cobra revealed female-specific loci that also show partial homology with a variety of amniote sex chromosomes, including the ACA X-linked region as GGA15 (Laopichienpong et al, 2020), supporting the hypothesis that the Siamese cobra W sex chromosome is derived from a larger ancestral amniote super-sex chromosome. Interestingly, the cohybridization signals of the same sex-chromosomal linkage homology are also observed for different chromosomes, as seen in cDNA and bacterial artificial chromosome (BAC) chromosomal maps (Matsuda et al, 2005;Matsubara et al, 2006Matsubara et al, , 2012Matsubara et al, , 2019Srikulnath et al, 2009aSrikulnath et al, ,b, 2013Srikulnath et al, , 2014Srikulnath et al, , 2015Uno et al, 2012;Singchat et al, 2018Singchat et al, , 2020a.…”

Section: Introductionmentioning

confidence: 99%

Genome Complexity Reduction High-Throughput Genome Sequencing of Green Iguana (Iguana iguana) Reveal a Paradigm Shift in Understanding Sex-Chromosomal Linkages on Homomorphic X and Y Sex Chromosomes

et al. 2020

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The majority of lizards classified in the superfamily Iguanoidea have an XX/XY sexdetermination system in which sex-chromosomal linkage shows homology with chicken (Gallus gallus) chromosome 15 (GGA15). However, the genomics of sex chromosomes remain largely unexplored owing to the presence of homomorphic sex chromosomes in majority of the species. Recent advances in high-throughput genome complexity reduction sequencing provide an effective approach to the identification of sexspecific loci with both single-nucleotide polymorphisms (SNPs) and restriction fragment presence/absence (PA), and a better understanding of sex chromosome dynamics in Iguanoidea. In this study, we applied Diversity Arrays Technology (DArTseq TM) in 29 phenotypic sex assignments (14 males and 15 females) of green iguana (Iguana iguana). We confirmed a male heterogametic (XX/XY) sex determination mode in this species, identifying 29 perfectly sex-linked SNP/PA loci and 164 moderately sex-linked SNP/PA loci, providing evidence probably indicative of XY recombination. Three loci from among the perfectly sex-linked SNP/PA loci showed partial homology with several amniote sex chromosomal linkages. The results support the hypothesis of an ancestral super-sex chromosome with overlaps of partial sex-chromosomal linkages. However, only one locus among the moderately sex-linked loci showed homology with GGA15, which suggests that the specific region homologous to GGA15 was located outside the non-recombination region but in close proximity to this region of the sex chromosome

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Genome-wide SNP analysis of Siamese cobra (Naja kaouthia) reveals the molecular basis of transitions between Z and W sex chromosomes and supports the presence of an ancestral super-sex chromosome in amniotes

Cited by 17 publications

References 99 publications

An Investigation of ZZ/ZW and XX/XY Sex Determination Systems in North African Catfish (Clarias gariepinus, Burchell, 1822)

An Investigation of ZZ/ZW and XX/XY Sex Determination Systems in North African Catfish (Clarias gariepinus, Burchell, 1822)

Independent Evolution of Sex Chromosomes in Eublepharid Geckos, A Lineage with Environmental and Genotypic Sex Determination

Genome Complexity Reduction High-Throughput Genome Sequencing of Green Iguana (Iguana iguana) Reveal a Paradigm Shift in Understanding Sex-Chromosomal Linkages on Homomorphic X and Y Sex Chromosomes

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