Genome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthus
Abstract Background Insect body coloration often functions as camouflage to survive from predators or mate selection. Transportation of pigment precursors or related metabolites from cytoplasm to subcellular pigment granules is one of the key steps in insect pigmentation and usually executed via suc...
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| Format: | Article |
| Language: | English |
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BMC
2021-02-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-021-07400-z |
| _version_ | 1818878286896300032 |
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| author | Guichun Liu Wei Liu Ruoping Zhao Jinwu He Zhiwei Dong Lei Chen Wenting Wan Zhou Chang Wen Wang Xueyan Li |
| author_facet | Guichun Liu Wei Liu Ruoping Zhao Jinwu He Zhiwei Dong Lei Chen Wenting Wan Zhou Chang Wen Wang Xueyan Li |
| author_sort | Guichun Liu |
| collection | DOAJ |
| description | Abstract Background Insect body coloration often functions as camouflage to survive from predators or mate selection. Transportation of pigment precursors or related metabolites from cytoplasm to subcellular pigment granules is one of the key steps in insect pigmentation and usually executed via such transporter proteins as the ATP-binding cassette (ABC) transmembrane transporters and small G-proteins (e.g. Rab protein). However, little is known about the copy numbers of pigment transporter genes in the butterfly genomes and about the roles of pigment transporters in the development of swallowtail butterflies. Results Here, we have identified 56 ABC transporters and 58 Rab members in the genome of swallowtail butterfly Papilio xuthus. This is the first case of genome-wide gene copy number identification of ABC transporters in swallowtail butterflies and Rab family in lepidopteran insects. Aiming to investigate the contribution of the five genes which are orthologous to well-studied pigment transporters (ABCG: white, scarlet, brown and ok; Rab: lightoid) of fruit fly or silkworm during the development of swallowtail butterflies, we performed CRISPR/Cas9 gene-editing of these genes using P. xuthus as a model and sequenced the transcriptomes of their morphological mutants. Our results indicate that the disruption of each gene produced mutated phenotypes in the colors of larvae (cuticle, testis) and/or adult eyes in G0 individuals but have no effect on wing color. The transcriptomic data demonstrated that mutations induced by CRISPR/Cas9 can lead to the accumulation of abnormal transcripts and the decrease or dosage compensation of normal transcripts at gene expression level. Comparative transcriptomes revealed 606 ~ 772 differentially expressed genes (DEGs) in the mutants of four ABCG transporters and 1443 DEGs in the mutants of lightoid. GO and KEGG enrichment analysis showed that DEGs in ABCG transporter mutants enriched to the oxidoreductase activity, heme binding, iron ion binding process possibly related to the color display, and DEGs in lightoid mutants are enriched in glycoprotein binding and protein kinases. Conclusions Our data indicated these transporter proteins play an important role in body color of P. xuthus. Our study provides new insights into the function of ABC transporters and small G-proteins in the morphological development of butterflies. |
| first_indexed | 2024-12-19T14:11:46Z |
| format | Article |
| id | doaj.art-b1428f44d7624ab9a3cb649912b66efd |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-19T14:11:46Z |
| publishDate | 2021-02-01 |
| publisher | BMC |
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| series | BMC Genomics |
| spelling | doaj.art-b1428f44d7624ab9a3cb649912b66efd2022-12-21T20:18:07ZengBMCBMC Genomics1471-21642021-02-0122111810.1186/s12864-021-07400-zGenome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthusGuichun Liu0Wei Liu1Ruoping Zhao2Jinwu He3Zhiwei Dong4Lei Chen5Wenting Wan6Zhou Chang7Wen Wang8Xueyan Li9School of Ecology and Environment, Northwestern Polytechnical UniversityState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of SciencesSchool of Ecology and Environment, Northwestern Polytechnical UniversityState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of SciencesSchool of Ecology and Environment, Northwestern Polytechnical UniversitySchool of Ecology and Environment, Northwestern Polytechnical UniversityState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of SciencesSchool of Ecology and Environment, Northwestern Polytechnical UniversityState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of SciencesAbstract Background Insect body coloration often functions as camouflage to survive from predators or mate selection. Transportation of pigment precursors or related metabolites from cytoplasm to subcellular pigment granules is one of the key steps in insect pigmentation and usually executed via such transporter proteins as the ATP-binding cassette (ABC) transmembrane transporters and small G-proteins (e.g. Rab protein). However, little is known about the copy numbers of pigment transporter genes in the butterfly genomes and about the roles of pigment transporters in the development of swallowtail butterflies. Results Here, we have identified 56 ABC transporters and 58 Rab members in the genome of swallowtail butterfly Papilio xuthus. This is the first case of genome-wide gene copy number identification of ABC transporters in swallowtail butterflies and Rab family in lepidopteran insects. Aiming to investigate the contribution of the five genes which are orthologous to well-studied pigment transporters (ABCG: white, scarlet, brown and ok; Rab: lightoid) of fruit fly or silkworm during the development of swallowtail butterflies, we performed CRISPR/Cas9 gene-editing of these genes using P. xuthus as a model and sequenced the transcriptomes of their morphological mutants. Our results indicate that the disruption of each gene produced mutated phenotypes in the colors of larvae (cuticle, testis) and/or adult eyes in G0 individuals but have no effect on wing color. The transcriptomic data demonstrated that mutations induced by CRISPR/Cas9 can lead to the accumulation of abnormal transcripts and the decrease or dosage compensation of normal transcripts at gene expression level. Comparative transcriptomes revealed 606 ~ 772 differentially expressed genes (DEGs) in the mutants of four ABCG transporters and 1443 DEGs in the mutants of lightoid. GO and KEGG enrichment analysis showed that DEGs in ABCG transporter mutants enriched to the oxidoreductase activity, heme binding, iron ion binding process possibly related to the color display, and DEGs in lightoid mutants are enriched in glycoprotein binding and protein kinases. Conclusions Our data indicated these transporter proteins play an important role in body color of P. xuthus. Our study provides new insights into the function of ABC transporters and small G-proteins in the morphological development of butterflies.https://doi.org/10.1186/s12864-021-07400-zATP-binding cassette (ABC) transportersRab transportersPapilio xuthusCRISPR/Cas9Transcriptome |
| spellingShingle | Guichun Liu Wei Liu Ruoping Zhao Jinwu He Zhiwei Dong Lei Chen Wenting Wan Zhou Chang Wen Wang Xueyan Li Genome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthus BMC Genomics ATP-binding cassette (ABC) transporters Rab transporters Papilio xuthus CRISPR/Cas9 Transcriptome |
| title | Genome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthus |
| title_full | Genome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthus |
| title_fullStr | Genome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthus |
| title_full_unstemmed | Genome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthus |
| title_short | Genome-wide identification and gene-editing of pigment transporter genes in the swallowtail butterfly Papilio xuthus |
| title_sort | genome wide identification and gene editing of pigment transporter genes in the swallowtail butterfly papilio xuthus |
| topic | ATP-binding cassette (ABC) transporters Rab transporters Papilio xuthus CRISPR/Cas9 Transcriptome |
| url | https://doi.org/10.1186/s12864-021-07400-z |
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