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.
Highlights
Fireflies are among the most charismatic insects for their spectacular bioluminescence, but the origin and evolution of bioluminescence remain elusive
Among the assembled genomes of six phylogenetically related luminous beetles including four previously reported[12,13] and two fireflies sequenced in this study (Fig. 2a,b), L. yunnana genome has the largest size (1053 Mb) and the highest percentage of repetitive elements (66.62%), while those of A. terminalis (501 Mb; 36.54%) are similar to those of American firefly Photinus pyralis (471 Mb; 47.70%) (Table 1; Supplementary Tables S8–S9)
Comparative analyses of whole genomes among five fireflies indicate that genome size variation mainly results from the relative abundance of transposable elements (TEs), especially DNA transposons and long interspersed nuclear elements (LINEs), which are two most abundant types of TEs among the genomes of all luminous beetles previously reported[12,13] and sequenced in this study, and correlate in abundance with their host genome size (Table 1, Fig. 2c; Supplementary Table S9, Fig. S11)
Summary
Fireflies are among the most charismatic insects for their spectacular bioluminescence, but the origin and evolution of bioluminescence remain elusive. 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. 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. The origin and evolution of luciferase genes and how bioluminescent light signal pattern (glow, flash) evolve in luminous beetles remain elusive. A thorough investigation integrating multilevel data (including comparative genomics, proteomics and transcriptomics of luminous organs and their three-dimension reconstruction, functional verification of genes in vitro experiments, and CRISPR/Cas[9] gene editing) provides new perspectives on luciferin biosynthesis, the origin and evolution of bioluminescence and light pattern
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