Identification of the silkworm quail gene reveals a crucial role of a receptor guanylyl cyclase in larval pigmentation
Diverse color patterns on the integument of lepidopteran larvae play important roles in their survival through camouflage, mimicry, sexual signaling, and aposematism. In the silkworm Bombyx mori, many color pattern variations have been preserved in inbred strains making them a good model for elucida...
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Veröffentlicht in: | Insect biochemistry and molecular biology 2016-01, Vol.68, p.33-40 |
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creator | Yuasa, Masashi Kiuchi, Takashi Banno, Yutaka Katsuma, Susumu Shimada, Toru |
description | Diverse color patterns on the integument of lepidopteran larvae play important roles in their survival through camouflage, mimicry, sexual signaling, and aposematism. In the silkworm Bombyx mori, many color pattern variations have been preserved in inbred strains making them a good model for elucidating the molecular mechanisms that underlie color pattern formation. In this study, we focused on the silkworm quail (q) mutant, which exhibits abnormalities in multiple pigment biosynthesis pathways. Positional cloning of the q gene revealed that disruption of a guanylyl cyclase gene, BmGC-I, is responsible for its abnormal pigmentation. In q mutants, we identified a 16-bp deletion in the BmGC-I transcript, resulting in the production of a premature stop codon. Knockout of the BmGC-I gene resulted in the q-like abnormal pigmentation, thereby demonstrating that the BmGC-I gene is involved in the pigment biosynthesis pathway in the integument. Moreover, quantitative reverse transcription polymerase chain reaction showed that BmGC-I was strongly expressed in the fourth instar on day 2. Our results suggest that BmGC-I deficiency affects the pigment biosynthesis pathway, which supports the involvement of guanylyl cyclase in larval coloration.
[Display omitted]
•The silkworm quail mutant shows extra black spots and pinkish color on larval skin.•Positional cloning identified a gene responsible for quail.•The responsible gene encodes a guanylyl cyclase protein, BmGC-I.•Knockout of BmGC-I causes the quail-like pigmentation pattern. |
doi_str_mv | 10.1016/j.ibmb.2015.10.016 |
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[Display omitted]
•The silkworm quail mutant shows extra black spots and pinkish color on larval skin.•Positional cloning identified a gene responsible for quail.•The responsible gene encodes a guanylyl cyclase protein, BmGC-I.•Knockout of BmGC-I causes the quail-like pigmentation pattern.</description><identifier>ISSN: 0965-1748</identifier><identifier>EISSN: 1879-0240</identifier><identifier>DOI: 10.1016/j.ibmb.2015.10.016</identifier><identifier>PMID: 26561270</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Animals ; Base Sequence ; Bombyx - genetics ; Bombyx - growth & development ; Bombyx - metabolism ; Bombyx - physiology ; Bombyx mori ; Cloning, Molecular ; DNA ; Female ; Gene Knockout Techniques ; Genes, Insect ; Guanylyl cyclase ; Integument ; Larva - physiology ; Lepidoptera ; Male ; Melanin ; Molecular Sequence Data ; Phenotype ; Pigmentation ; Pigmentation - genetics ; Quail ; Receptors, Guanylate Cyclase-Coupled - physiology ; Transcriptome</subject><ispartof>Insect biochemistry and molecular biology, 2016-01, Vol.68, p.33-40</ispartof><rights>2015 Elsevier Ltd</rights><rights>Copyright © 2015 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c455t-5f984b9f5de49c5df151d41db19c19f959e4bdb138cfbf65427a7861aa6a65d53</citedby><cites>FETCH-LOGICAL-c455t-5f984b9f5de49c5df151d41db19c19f959e4bdb138cfbf65427a7861aa6a65d53</cites><orcidid>0000-0002-5791-0000</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ibmb.2015.10.016$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>315,781,785,3551,27928,27929,45999</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26561270$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yuasa, Masashi</creatorcontrib><creatorcontrib>Kiuchi, Takashi</creatorcontrib><creatorcontrib>Banno, Yutaka</creatorcontrib><creatorcontrib>Katsuma, Susumu</creatorcontrib><creatorcontrib>Shimada, Toru</creatorcontrib><title>Identification of the silkworm quail gene reveals a crucial role of a receptor guanylyl cyclase in larval pigmentation</title><title>Insect biochemistry and molecular biology</title><addtitle>Insect Biochem Mol Biol</addtitle><description>Diverse color patterns on the integument of lepidopteran larvae play important roles in their survival through camouflage, mimicry, sexual signaling, and aposematism. In the silkworm Bombyx mori, many color pattern variations have been preserved in inbred strains making them a good model for elucidating the molecular mechanisms that underlie color pattern formation. In this study, we focused on the silkworm quail (q) mutant, which exhibits abnormalities in multiple pigment biosynthesis pathways. Positional cloning of the q gene revealed that disruption of a guanylyl cyclase gene, BmGC-I, is responsible for its abnormal pigmentation. In q mutants, we identified a 16-bp deletion in the BmGC-I transcript, resulting in the production of a premature stop codon. Knockout of the BmGC-I gene resulted in the q-like abnormal pigmentation, thereby demonstrating that the BmGC-I gene is involved in the pigment biosynthesis pathway in the integument. Moreover, quantitative reverse transcription polymerase chain reaction showed that BmGC-I was strongly expressed in the fourth instar on day 2. Our results suggest that BmGC-I deficiency affects the pigment biosynthesis pathway, which supports the involvement of guanylyl cyclase in larval coloration.
[Display omitted]
•The silkworm quail mutant shows extra black spots and pinkish color on larval skin.•Positional cloning identified a gene responsible for quail.•The responsible gene encodes a guanylyl cyclase protein, BmGC-I.•Knockout of BmGC-I causes the quail-like pigmentation pattern.</description><subject>Animals</subject><subject>Base Sequence</subject><subject>Bombyx - genetics</subject><subject>Bombyx - growth & development</subject><subject>Bombyx - metabolism</subject><subject>Bombyx - physiology</subject><subject>Bombyx mori</subject><subject>Cloning, Molecular</subject><subject>DNA</subject><subject>Female</subject><subject>Gene Knockout Techniques</subject><subject>Genes, Insect</subject><subject>Guanylyl cyclase</subject><subject>Integument</subject><subject>Larva - physiology</subject><subject>Lepidoptera</subject><subject>Male</subject><subject>Melanin</subject><subject>Molecular Sequence Data</subject><subject>Phenotype</subject><subject>Pigmentation</subject><subject>Pigmentation - genetics</subject><subject>Quail</subject><subject>Receptors, Guanylate Cyclase-Coupled - physiology</subject><subject>Transcriptome</subject><issn>0965-1748</issn><issn>1879-0240</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1u1DAUhS1URIfCC7CovOwmg53xTyx1U1UFKlViA2vLsa8HT514aieD5u1xmJZlxcryud85V7oHoU-UrCmh4vNuHfqhX7eE8iqsq_QGrWgnVUNaRs7QiijBGypZd47el7IjhDDG5Tt03gouaCvJCh3uHYxT8MGaKaQRJ4-nX4BLiI-_Ux7w02xCxFsYAWc4gIkFG2zzbIOJOKcIi8PUmYX9lDLezmY8xmPE9mijKYDDiKPJh0rvw3aou_7u-YDe-poFH5_fC_Tzy92P22_Nw_ev97c3D41lnE8N96pjvfLcAVOWO085dYy6nipLlVdcAevrb9NZ33vBWSuN7AQ1RhjBHd9coKtT7j6npxnKpIdQLMRoRkhz0VSKdiOJJOx_UNIpyoiqaHtCbU6lZPB6n8Ng8lFTopdq9E4v1eilmkWrUjVdPufP_QDun-WliwpcnwCoBzkEyLrYAKMFF-p5J-1SeC3_D4VPoS0</recordid><startdate>201601</startdate><enddate>201601</enddate><creator>Yuasa, Masashi</creator><creator>Kiuchi, Takashi</creator><creator>Banno, Yutaka</creator><creator>Katsuma, Susumu</creator><creator>Shimada, Toru</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7SS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><orcidid>https://orcid.org/0000-0002-5791-0000</orcidid></search><sort><creationdate>201601</creationdate><title>Identification of the silkworm quail gene reveals a crucial role of a receptor guanylyl cyclase in larval pigmentation</title><author>Yuasa, Masashi ; Kiuchi, Takashi ; Banno, Yutaka ; Katsuma, Susumu ; Shimada, Toru</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c455t-5f984b9f5de49c5df151d41db19c19f959e4bdb138cfbf65427a7861aa6a65d53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Base Sequence</topic><topic>Bombyx - genetics</topic><topic>Bombyx - growth & development</topic><topic>Bombyx - metabolism</topic><topic>Bombyx - physiology</topic><topic>Bombyx mori</topic><topic>Cloning, Molecular</topic><topic>DNA</topic><topic>Female</topic><topic>Gene Knockout Techniques</topic><topic>Genes, Insect</topic><topic>Guanylyl cyclase</topic><topic>Integument</topic><topic>Larva - physiology</topic><topic>Lepidoptera</topic><topic>Male</topic><topic>Melanin</topic><topic>Molecular Sequence Data</topic><topic>Phenotype</topic><topic>Pigmentation</topic><topic>Pigmentation - genetics</topic><topic>Quail</topic><topic>Receptors, Guanylate Cyclase-Coupled - physiology</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yuasa, Masashi</creatorcontrib><creatorcontrib>Kiuchi, Takashi</creatorcontrib><creatorcontrib>Banno, Yutaka</creatorcontrib><creatorcontrib>Katsuma, Susumu</creatorcontrib><creatorcontrib>Shimada, Toru</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Insect biochemistry and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yuasa, Masashi</au><au>Kiuchi, Takashi</au><au>Banno, Yutaka</au><au>Katsuma, Susumu</au><au>Shimada, Toru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of the silkworm quail gene reveals a crucial role of a receptor guanylyl cyclase in larval pigmentation</atitle><jtitle>Insect biochemistry and molecular biology</jtitle><addtitle>Insect Biochem Mol Biol</addtitle><date>2016-01</date><risdate>2016</risdate><volume>68</volume><spage>33</spage><epage>40</epage><pages>33-40</pages><issn>0965-1748</issn><eissn>1879-0240</eissn><abstract>Diverse color patterns on the integument of lepidopteran larvae play important roles in their survival through camouflage, mimicry, sexual signaling, and aposematism. In the silkworm Bombyx mori, many color pattern variations have been preserved in inbred strains making them a good model for elucidating the molecular mechanisms that underlie color pattern formation. In this study, we focused on the silkworm quail (q) mutant, which exhibits abnormalities in multiple pigment biosynthesis pathways. Positional cloning of the q gene revealed that disruption of a guanylyl cyclase gene, BmGC-I, is responsible for its abnormal pigmentation. In q mutants, we identified a 16-bp deletion in the BmGC-I transcript, resulting in the production of a premature stop codon. Knockout of the BmGC-I gene resulted in the q-like abnormal pigmentation, thereby demonstrating that the BmGC-I gene is involved in the pigment biosynthesis pathway in the integument. Moreover, quantitative reverse transcription polymerase chain reaction showed that BmGC-I was strongly expressed in the fourth instar on day 2. Our results suggest that BmGC-I deficiency affects the pigment biosynthesis pathway, which supports the involvement of guanylyl cyclase in larval coloration.
[Display omitted]
•The silkworm quail mutant shows extra black spots and pinkish color on larval skin.•Positional cloning identified a gene responsible for quail.•The responsible gene encodes a guanylyl cyclase protein, BmGC-I.•Knockout of BmGC-I causes the quail-like pigmentation pattern.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>26561270</pmid><doi>10.1016/j.ibmb.2015.10.016</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-5791-0000</orcidid></addata></record> |
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subjects | Animals Base Sequence Bombyx - genetics Bombyx - growth & development Bombyx - metabolism Bombyx - physiology Bombyx mori Cloning, Molecular DNA Female Gene Knockout Techniques Genes, Insect Guanylyl cyclase Integument Larva - physiology Lepidoptera Male Melanin Molecular Sequence Data Phenotype Pigmentation Pigmentation - genetics Quail Receptors, Guanylate Cyclase-Coupled - physiology Transcriptome |
title | Identification of the silkworm quail gene reveals a crucial role of a receptor guanylyl cyclase in larval pigmentation |
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