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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Autores principales: 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
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Publicado: Nature Portfolio 2020
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spelling 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)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle 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
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