Transcriptomic and gene-family dynamic analyses reveal gene expression pattern and evolution in toxin-producing tissues of Asiatic toad (Bufo gargarizans)
Comprising a major clade of Anura, toads produce and secrete numerous toxins from both the parotoid glands behind their eyes and their dorsal skin. These toxins, made of various proteins and compounds, possess pharmacological potential to be repurposed to benefit human health. However, the detailed...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-07-01
|
| Series: | Frontiers in Ecology and Evolution |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fevo.2022.924248/full |
| _version_ | 1818041428586004480 |
|---|---|
| author | Yunyun Lv Yanping Li Zhengyong Wen Qiong Shi Qiong Shi |
| author_facet | Yunyun Lv Yanping Li Zhengyong Wen Qiong Shi Qiong Shi |
| author_sort | Yunyun Lv |
| collection | DOAJ |
| description | Comprising a major clade of Anura, toads produce and secrete numerous toxins from both the parotoid glands behind their eyes and their dorsal skin. These toxins, made of various proteins and compounds, possess pharmacological potential to be repurposed to benefit human health. However, the detailed genetic regulation of toad toxin production is still poorly understood. A recent publication uncovering the genome of the representative Asiatic toad (Bufo gargarizans) provides a good reference to resolve this issue. In the present study, we sequenced the transcriptomes of parotoid gland, dorsal skin and liver from the Asiatic toad. Combining our data with 35 previously published transcriptomes across eight different tissues from the same species but from different locations, we constructed a comprehensive gene co-expression network of the Asiatic toad with the assistance of the reference genome assembly. We identified 2,701 co-expressed genes in the toxin-producing tissues (including parotoid gland and dorsal skin). By comparative genomic analysis, we identified 599 expanded gene families with 2,720 genes. Through overlapping these co-expressed genes in the toad toxin-producing tissues, we observed that three cytochrome P450 (Cyp) family members (Cyp27a1, Cyp2c29, and Cyp2c39) were significantly enriched in pathways related to cholesterol metabolism. Cholesterol is a critical precursor to steroids, and the known main steroidal toxins of bufadienolides are considered as the major bioactive components in the parotoid glands of Asiatic toad. We found 3-hydroxy-methylglutaryl CoA reductase (hmgcr), encoding the major rate-limiting enzyme for cholesterol biosynthesis, appears with multiple copies in both Asiatic toad and common toad, possibly originating from a tandem duplication event. The five copies of hmgcr genes consistently displayed higher transcription levels in the parotoid gland when compared with the abdominal skin, suggesting it as a vital candidate gene in the involvement of toad toxin production. Taken together, our current study uncovers transcriptomic and gene-family dynamic evidence to reveal the vital role of both expanded gene copies and gene expression changes for production of toad toxins. |
| first_indexed | 2024-12-10T08:30:16Z |
| format | Article |
| id | doaj.art-9a4113e8f0164f109a2e7085fc8ab2e8 |
| institution | Directory Open Access Journal |
| issn | 2296-701X |
| language | English |
| last_indexed | 2024-12-10T08:30:16Z |
| publishDate | 2022-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Ecology and Evolution |
| spelling | doaj.art-9a4113e8f0164f109a2e7085fc8ab2e82022-12-22T01:56:07ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2022-07-011010.3389/fevo.2022.924248924248Transcriptomic and gene-family dynamic analyses reveal gene expression pattern and evolution in toxin-producing tissues of Asiatic toad (Bufo gargarizans)Yunyun Lv0Yanping Li1Zhengyong Wen2Qiong Shi3Qiong Shi4Key Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, College of Life Sciences, Neijiang Normal University, Neijiang, ChinaKey Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, College of Life Sciences, Neijiang Normal University, Neijiang, ChinaKey Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, College of Life Sciences, Neijiang Normal University, Neijiang, ChinaKey Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, College of Life Sciences, Neijiang Normal University, Neijiang, ChinaShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen, ChinaComprising a major clade of Anura, toads produce and secrete numerous toxins from both the parotoid glands behind their eyes and their dorsal skin. These toxins, made of various proteins and compounds, possess pharmacological potential to be repurposed to benefit human health. However, the detailed genetic regulation of toad toxin production is still poorly understood. A recent publication uncovering the genome of the representative Asiatic toad (Bufo gargarizans) provides a good reference to resolve this issue. In the present study, we sequenced the transcriptomes of parotoid gland, dorsal skin and liver from the Asiatic toad. Combining our data with 35 previously published transcriptomes across eight different tissues from the same species but from different locations, we constructed a comprehensive gene co-expression network of the Asiatic toad with the assistance of the reference genome assembly. We identified 2,701 co-expressed genes in the toxin-producing tissues (including parotoid gland and dorsal skin). By comparative genomic analysis, we identified 599 expanded gene families with 2,720 genes. Through overlapping these co-expressed genes in the toad toxin-producing tissues, we observed that three cytochrome P450 (Cyp) family members (Cyp27a1, Cyp2c29, and Cyp2c39) were significantly enriched in pathways related to cholesterol metabolism. Cholesterol is a critical precursor to steroids, and the known main steroidal toxins of bufadienolides are considered as the major bioactive components in the parotoid glands of Asiatic toad. We found 3-hydroxy-methylglutaryl CoA reductase (hmgcr), encoding the major rate-limiting enzyme for cholesterol biosynthesis, appears with multiple copies in both Asiatic toad and common toad, possibly originating from a tandem duplication event. The five copies of hmgcr genes consistently displayed higher transcription levels in the parotoid gland when compared with the abdominal skin, suggesting it as a vital candidate gene in the involvement of toad toxin production. Taken together, our current study uncovers transcriptomic and gene-family dynamic evidence to reveal the vital role of both expanded gene copies and gene expression changes for production of toad toxins.https://www.frontiersin.org/articles/10.3389/fevo.2022.924248/fulltoxintranscriptomeCyphmgcrgene family |
| spellingShingle | Yunyun Lv Yanping Li Zhengyong Wen Qiong Shi Qiong Shi Transcriptomic and gene-family dynamic analyses reveal gene expression pattern and evolution in toxin-producing tissues of Asiatic toad (Bufo gargarizans) Frontiers in Ecology and Evolution toxin transcriptome Cyp hmgcr gene family |
| title | Transcriptomic and gene-family dynamic analyses reveal gene expression pattern and evolution in toxin-producing tissues of Asiatic toad (Bufo gargarizans) |
| title_full | Transcriptomic and gene-family dynamic analyses reveal gene expression pattern and evolution in toxin-producing tissues of Asiatic toad (Bufo gargarizans) |
| title_fullStr | Transcriptomic and gene-family dynamic analyses reveal gene expression pattern and evolution in toxin-producing tissues of Asiatic toad (Bufo gargarizans) |
| title_full_unstemmed | Transcriptomic and gene-family dynamic analyses reveal gene expression pattern and evolution in toxin-producing tissues of Asiatic toad (Bufo gargarizans) |
| title_short | Transcriptomic and gene-family dynamic analyses reveal gene expression pattern and evolution in toxin-producing tissues of Asiatic toad (Bufo gargarizans) |
| title_sort | transcriptomic and gene family dynamic analyses reveal gene expression pattern and evolution in toxin producing tissues of asiatic toad bufo gargarizans |
| topic | toxin transcriptome Cyp hmgcr gene family |
| url | https://www.frontiersin.org/articles/10.3389/fevo.2022.924248/full |
| work_keys_str_mv | AT yunyunlv transcriptomicandgenefamilydynamicanalysesrevealgeneexpressionpatternandevolutionintoxinproducingtissuesofasiatictoadbufogargarizans AT yanpingli transcriptomicandgenefamilydynamicanalysesrevealgeneexpressionpatternandevolutionintoxinproducingtissuesofasiatictoadbufogargarizans AT zhengyongwen transcriptomicandgenefamilydynamicanalysesrevealgeneexpressionpatternandevolutionintoxinproducingtissuesofasiatictoadbufogargarizans AT qiongshi transcriptomicandgenefamilydynamicanalysesrevealgeneexpressionpatternandevolutionintoxinproducingtissuesofasiatictoadbufogargarizans AT qiongshi transcriptomicandgenefamilydynamicanalysesrevealgeneexpressionpatternandevolutionintoxinproducingtissuesofasiatictoadbufogargarizans |