Genomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies
Abstract Fireflies are among the most charismatic insects for their spectacular bioluminescence, but the origin and evolution of bioluminescence remain elusive. Especially, the genic basis of luciferin (d-luciferin) biosynthesis and light patterns is largely unknown. Here, we present the high-qualit...
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2020
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oai:doaj.org-article:7c29eb56a0e643bbae6b33d3e724fe232021-12-02T18:51:13ZGenomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies10.1038/s41598-020-72900-z2045-2322https://doaj.org/article/7c29eb56a0e643bbae6b33d3e724fe232020-09-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-72900-zhttps://doaj.org/toc/2045-2322Abstract Fireflies are among the most charismatic insects for their spectacular bioluminescence, but the origin and evolution of bioluminescence remain elusive. Especially, the genic basis of luciferin (d-luciferin) biosynthesis and light patterns is largely unknown. Here, we present the high-quality reference genomes of two fireflies Lamprigera yunnana (1053 Mb) and Abscondita terminalis (501 Mb) with great differences in both morphology and luminous behavior. We sequenced the transcriptomes and proteomes of luminous organs of two species. We created the CRISPR/Cas9-induced mutants of Abdominal B gene without luminous organs in the larvae of A. terminalis and sequenced the transcriptomes of mutants and wild-types. Combining gene expression analyses with comparative genomics, we propose a more complete luciferin synthesis pathway, and confirm the convergent evolution of bioluminescence in insects. Using experiments, the function of the firefly acyl-CoA thioesterase (ACOT1) to convert l-luciferin to d-luciferin was validated for the first time. Comparisons of three-dimension reconstruction of luminous organs and their differentially expressed genes among two species suggest that two positive genes in the calcium signaling pathway and structural difference of luminous organs may play an important role in the evolution of flash pattern. Altogether, our results provide important resources for further exploring bioluminescence in insects.Ru ZhangJinwu HeZhiwei DongGuichun LiuYuan YinXinying ZhangQi LiYandong RenYongzhi YangWei LiuXianqing ChenWenhao XiaKang DuanFei HaoZeshan LinJie YangZhou ChangRuoping ZhaoWenting WanSihan LuYanqiong PengSiqin GeWen WangXueyan LiNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 10, Iss 1, Pp 1-19 (2020) |
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Medicine R Science Q Ru Zhang Jinwu He Zhiwei Dong Guichun Liu Yuan Yin Xinying Zhang Qi Li Yandong Ren Yongzhi Yang Wei Liu Xianqing Chen Wenhao Xia Kang Duan Fei Hao Zeshan Lin Jie Yang Zhou Chang Ruoping Zhao Wenting Wan Sihan Lu Yanqiong Peng Siqin Ge Wen Wang Xueyan Li Genomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies |
description |
Abstract Fireflies are among the most charismatic insects for their spectacular bioluminescence, but the origin and evolution of bioluminescence remain elusive. Especially, the genic basis of luciferin (d-luciferin) biosynthesis and light patterns is largely unknown. Here, we present the high-quality reference genomes of two fireflies Lamprigera yunnana (1053 Mb) and Abscondita terminalis (501 Mb) with great differences in both morphology and luminous behavior. We sequenced the transcriptomes and proteomes of luminous organs of two species. We created the CRISPR/Cas9-induced mutants of Abdominal B gene without luminous organs in the larvae of A. terminalis and sequenced the transcriptomes of mutants and wild-types. Combining gene expression analyses with comparative genomics, we propose a more complete luciferin synthesis pathway, and confirm the convergent evolution of bioluminescence in insects. Using experiments, the function of the firefly acyl-CoA thioesterase (ACOT1) to convert l-luciferin to d-luciferin was validated for the first time. Comparisons of three-dimension reconstruction of luminous organs and their differentially expressed genes among two species suggest that two positive genes in the calcium signaling pathway and structural difference of luminous organs may play an important role in the evolution of flash pattern. Altogether, our results provide important resources for further exploring bioluminescence in insects. |
format |
article |
author |
Ru Zhang Jinwu He Zhiwei Dong Guichun Liu Yuan Yin Xinying Zhang Qi Li Yandong Ren Yongzhi Yang Wei Liu Xianqing Chen Wenhao Xia Kang Duan Fei Hao Zeshan Lin Jie Yang Zhou Chang Ruoping Zhao Wenting Wan Sihan Lu Yanqiong Peng Siqin Ge Wen Wang Xueyan Li |
author_facet |
Ru Zhang Jinwu He Zhiwei Dong Guichun Liu Yuan Yin Xinying Zhang Qi Li Yandong Ren Yongzhi Yang Wei Liu Xianqing Chen Wenhao Xia Kang Duan Fei Hao Zeshan Lin Jie Yang Zhou Chang Ruoping Zhao Wenting Wan Sihan Lu Yanqiong Peng Siqin Ge Wen Wang Xueyan Li |
author_sort |
Ru Zhang |
title |
Genomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies |
title_short |
Genomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies |
title_full |
Genomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies |
title_fullStr |
Genomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies |
title_full_unstemmed |
Genomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies |
title_sort |
genomic and experimental data provide new insights into luciferin biosynthesis and bioluminescence evolution in fireflies |
publisher |
Nature Portfolio |
publishDate |
2020 |
url |
https://doaj.org/article/7c29eb56a0e643bbae6b33d3e724fe23 |
work_keys_str_mv |
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