Uterus-specific transcriptional regulation underlies eggshell pigment production in Japanese quail.
The precursor of heme, protoporphyrin IX (PPIX), accumulates abundantly in the uteri of birds, such as Japanese quail, Coturnix japonica, which has brown-speckled eggshells; however, the molecular basis of PPIX production in the uterus remains largely unknown. Here, we investigated the cause of low...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0265008 |
| _version_ | 1828858438896058368 |
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| author | Satoshi Ishishita Shumpei Kitahara Mayuko Takahashi Sakura Iwasaki Shoji Tatsumoto Izumi Hara Yoshiki Kaneko Keiji Kinoshita Katsushi Yamaguchi Akihito Harada Yasushige Ohmori Yasuyuki Ohkawa Yasuhiro Go Shuji Shigenobu Yoichi Matsuda Takayuki Suzuki |
| author_facet | Satoshi Ishishita Shumpei Kitahara Mayuko Takahashi Sakura Iwasaki Shoji Tatsumoto Izumi Hara Yoshiki Kaneko Keiji Kinoshita Katsushi Yamaguchi Akihito Harada Yasushige Ohmori Yasuyuki Ohkawa Yasuhiro Go Shuji Shigenobu Yoichi Matsuda Takayuki Suzuki |
| author_sort | Satoshi Ishishita |
| collection | DOAJ |
| description | The precursor of heme, protoporphyrin IX (PPIX), accumulates abundantly in the uteri of birds, such as Japanese quail, Coturnix japonica, which has brown-speckled eggshells; however, the molecular basis of PPIX production in the uterus remains largely unknown. Here, we investigated the cause of low PPIX production in a classical Japanese quail mutant exhibiting white eggshells by comparing its gene expression in the uterus with that of the wild type using transcriptome analysis. We also performed genetic linkage analysis to identify the causative genomic region of the white eggshell phenotype. We found that 11 genes, including 5'-aminolevulinate synthase 1 (ALAS1) and hephaestin-like 1 (HEPHL1), were specifically upregulated in the wild-type uterus and downregulated in the mutant. We mapped the 172 kb candidate genomic region on chromosome 6, which contains several genes, including a part of the paired-like homeodomain 3 (PITX3), which encodes a transcription factor. ALAS1, HEPHL1, and PITX3 were expressed in the apical cells of the luminal epithelium and lamina propria cells of the uterine mucosa of the wild-type quail, while their expression levels were downregulated in the cells of the mutant quail. Biochemical analysis using uterine homogenates indicated that the restricted availability of 5'-aminolevulinic acid is the main cause of low PPIX production. These results suggest that uterus-specific transcriptional regulation of heme-biosynthesis-related genes is an evolutionarily acquired mechanism of eggshell pigment production in Japanese quail. Based on these findings, we discussed the molecular basis of PPIX production in the uteri of Japanese quails. |
| first_indexed | 2024-12-13T01:56:33Z |
| format | Article |
| id | doaj.art-89aadf0c469a42109fbcfb57e5d1f44e |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-13T01:56:33Z |
| publishDate | 2022-01-01 |
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| series | PLoS ONE |
| spelling | doaj.art-89aadf0c469a42109fbcfb57e5d1f44e2022-12-22T00:03:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-01173e026500810.1371/journal.pone.0265008Uterus-specific transcriptional regulation underlies eggshell pigment production in Japanese quail.Satoshi IshishitaShumpei KitaharaMayuko TakahashiSakura IwasakiShoji TatsumotoIzumi HaraYoshiki KanekoKeiji KinoshitaKatsushi YamaguchiAkihito HaradaYasushige OhmoriYasuyuki OhkawaYasuhiro GoShuji ShigenobuYoichi MatsudaTakayuki SuzukiThe precursor of heme, protoporphyrin IX (PPIX), accumulates abundantly in the uteri of birds, such as Japanese quail, Coturnix japonica, which has brown-speckled eggshells; however, the molecular basis of PPIX production in the uterus remains largely unknown. Here, we investigated the cause of low PPIX production in a classical Japanese quail mutant exhibiting white eggshells by comparing its gene expression in the uterus with that of the wild type using transcriptome analysis. We also performed genetic linkage analysis to identify the causative genomic region of the white eggshell phenotype. We found that 11 genes, including 5'-aminolevulinate synthase 1 (ALAS1) and hephaestin-like 1 (HEPHL1), were specifically upregulated in the wild-type uterus and downregulated in the mutant. We mapped the 172 kb candidate genomic region on chromosome 6, which contains several genes, including a part of the paired-like homeodomain 3 (PITX3), which encodes a transcription factor. ALAS1, HEPHL1, and PITX3 were expressed in the apical cells of the luminal epithelium and lamina propria cells of the uterine mucosa of the wild-type quail, while their expression levels were downregulated in the cells of the mutant quail. Biochemical analysis using uterine homogenates indicated that the restricted availability of 5'-aminolevulinic acid is the main cause of low PPIX production. These results suggest that uterus-specific transcriptional regulation of heme-biosynthesis-related genes is an evolutionarily acquired mechanism of eggshell pigment production in Japanese quail. Based on these findings, we discussed the molecular basis of PPIX production in the uteri of Japanese quails.https://doi.org/10.1371/journal.pone.0265008 |
| spellingShingle | Satoshi Ishishita Shumpei Kitahara Mayuko Takahashi Sakura Iwasaki Shoji Tatsumoto Izumi Hara Yoshiki Kaneko Keiji Kinoshita Katsushi Yamaguchi Akihito Harada Yasushige Ohmori Yasuyuki Ohkawa Yasuhiro Go Shuji Shigenobu Yoichi Matsuda Takayuki Suzuki Uterus-specific transcriptional regulation underlies eggshell pigment production in Japanese quail. PLoS ONE |
| title | Uterus-specific transcriptional regulation underlies eggshell pigment production in Japanese quail. |
| title_full | Uterus-specific transcriptional regulation underlies eggshell pigment production in Japanese quail. |
| title_fullStr | Uterus-specific transcriptional regulation underlies eggshell pigment production in Japanese quail. |
| title_full_unstemmed | Uterus-specific transcriptional regulation underlies eggshell pigment production in Japanese quail. |
| title_short | Uterus-specific transcriptional regulation underlies eggshell pigment production in Japanese quail. |
| title_sort | uterus specific transcriptional regulation underlies eggshell pigment production in japanese quail |
| url | https://doi.org/10.1371/journal.pone.0265008 |
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