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Genomic and transcriptomic insights into molecular basis of sexually dimorphic nuptial spines in Leptobrachium leishanense.

ABSTRACT: Sexually dimorphic (SD) traits are important in sexual selection and species survival, yet the molecular basis remains elusive, especially in amphibians where SD traits have evolved repeatedly. We focus on the Leishan moustache toad (Leptobrachium leishanense), in which males develop nuptial spines on their maxillary skin. Here we report a 3.5?Gb genome assembly with a contig N50 of 1.93?Mb. We find a specific expansion of the intermediate filament gene family including numerous keratin genes. Within these genes, a cluster of duplicated hair keratin genes exhibits male-biased and maxillary skin-specific expression, suggesting a role in developing nuptial spines. We identify a module of coexpressed genes significantly associated with spine formation. In addition, we find several hormones likely to be involved in regulating spine development. This study not only presents a high-quality anuran genome but also provides a reference for studying skin-derived SD traits in amphibians.

SUBMITTER: Li J

PROVIDER: S-EPMC6895153 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Genomic and transcriptomic insights into molecular basis of sexually dimorphic nuptial spines in Leptobrachium leishanense.

Li Jun J Yu Haiyan H Wang Wenxia W Fu Chao C Zhang Wei W Han Fengming F Wu Hua H

Nature communications 20191205 1

Sexually dimorphic (SD) traits are important in sexual selection and species survival, yet the molecular basis remains elusive, especially in amphibians where SD traits have evolved repeatedly. We focus on the Leishan moustache toad (Leptobrachium leishanense), in which males develop nuptial spines on their maxillary skin. Here we report a 3.5 Gb genome assembly with a contig N50 of 1.93 Mb. We find a specific expansion of the intermediate filament gene family including numerous keratin genes. W ...[more]

PMID: 31804492

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Project description:BACKGROUND:The expression of sexually selected traits often varies with populations' breeding cycles in many animals. The elucidation of mechanisms underlying the expression of such traits is a research topic in evolutionary biology; however, the genetic basis of the seasonal development of their expression remains unknown. Male Leptobrachium boringii develop keratinized nuptial spines on their upper jaw during the breeding season that fall off when the breeding season ends. To illuminate the genetic basis for the expression of this trait and its seasonal development, we assessed the de novo transcriptome for L. boringii using brain, testis and upper jaw skin and compared gene expression profiles of these tissues between two critical periods of the spine growth cycle. RESULTS:We identified 94,900 unigenes in our transcriptome. Among them, 2,131 genes were differentially expressed between the breeding period when the spines developed and the post-breeding period when the spines were sloughed. An increased number of differentially expressed genes (DEGs) were identified in the upper jaw skin compared with the testis and brain. In the upper jaw skin, DEGs were mainly enriched in cytosolic part, peptidase inhibitor activity and peptidase regulator activity based on GO enrichment analysis and in glycolysis/gluconeogenesis, ribosome biogenesis in eukaryotes and retinol metabolism based on KEGG enrichment analysis. In the other two tissues, DEGs were primarily involved in the cell cycle, DNA replication and melatonin production. Specifically, insulin/insulin-like growth factor and sex steroid hormone-related DEGs were identified in the upper jaw skin, indicating . The expression variation of IGF2 and estrogen-related genes may be the main factors regulating the seasonal development of the spines. CONCLUSIONS:Our study provides a list of potential genes involved in the regulation of seasonal development of nuptial spines in L. boringii. This is the first transcriptome survey of seasonally developed sexually selected traits for non-model amphibian species, and candidate genes provided here may provide valuable information for further studies of L. boringii.

Project description:BACKGROUND: Our knowledge on zebrafish reproduction is very limited. We generated a gonad-derived cDNA microarray from zebrafish and used it to analyze large-scale gene expression profiles in adult gonads and other organs. METHODOLOGY/PRINCIPAL FINDINGS: We have identified 116638 gonad-derived zebrafish expressed sequence tags (ESTs), 21% of which were isolated in our lab. Following in silico normalization, we constructed a gonad-derived microarray comprising 6370 unique, full-length cDNAs from differentiating and adult gonads. Labeled targets from adult gonad, brain, kidney and 'rest-of-body' from both sexes were hybridized onto the microarray. Our analyses revealed 1366, 881 and 656 differentially expressed transcripts (34.7% novel) that showed highest expression in ovary, testis and both gonads respectively. Hierarchical clustering showed correlation of the two gonadal transcriptomes and their similarities to those of the brains. In addition, we have identified 276 genes showing sexually dimorphic expression both between the brains and between the gonads. By in situ hybridization, we showed that the gonadal transcripts with the strongest array signal intensities were germline-expressed. We found that five members of the GTP-binding septin gene family, from which only one member (septin 4) has previously been implicated in reproduction in mice, were all strongly expressed in the gonads. CONCLUSIONS/SIGNIFICANCE: We have generated a gonad-derived zebrafish cDNA microarray and demonstrated its usefulness in identifying genes with sexually dimorphic co-expression in both the gonads and the brains. We have also provided the first evidence of large-scale differential gene expression between female and male brains of a teleost. Our microarray would be useful for studying gonad development, differentiation and function not only in zebrafish but also in related teleosts via cross-species hybridizations. Since several genes have been shown to play similar roles in gonadogenesis in zebrafish and other vertebrates, our array may even provide information on genetic disorders affecting gonadal phenotypes and fertility in mammals.

Dataset Information

Genomic and transcriptomic insights into molecular basis of sexually dimorphic nuptial spines in Leptobrachium leishanense.

Publications

Genomic and transcriptomic insights into molecular basis of sexually dimorphic nuptial spines in Leptobrachium leishanense.

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