期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：9
DOI：10.1073/pnas.2114773119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
As caterpillars metamorphose to butterflies, insects change their appearance dramatically through metamorphosis. Some insects have an immobile pupal stage for morphological remodeling (homometaboly). Other insects, such as cockroaches, have no pupal stage, and the juveniles and adults are morphologically similar (hemimetaboly). Notably, among the most-ancestral hemimetabolous insects, dragonflies drastically alter their appearance from aquatic nymphs to aerial adults. In dragonflies, we showed that transcription factors
Kr-h1 and
E93 are essential for regulating metamorphosis as in other insects, while
broad, the master gene for pupation in holometabolous insects, regulates a number of both nymph-specific genes and adult-specific genes, providing insight into what evolutionary trajectory the key transcription factor
broad has experienced before ending up with governing pupation and holometaboly.
Insects comprise over half of the described species, and the acquisition of metamorphosis must have contributed to their diversity and prosperity. The order Odonata (dragonflies and damselflies) is among the most-ancestral insects with drastic morphological changes upon metamorphosis, in which understanding of the molecular mechanisms will provide insight into the evolution of incomplete and complete metamorphosis in insects. In order to identify metamorphosis-related genes in Odonata, we performed comprehensive RNA-sequencing of the blue-tailed damselfly
Ischnura senegalensis at different developmental stages. Comparative RNA-sequencing analyses between nymphs and adults identified eight nymph-specific and seven adult-specific transcripts. RNA interference (RNAi) of these candidate genes demonstrated that three transcription factors,
Krüppel homolog 1 (
Kr-h1),
broad, and
E93 play important roles in metamorphosis of both
I. senegalensis and a phylogenetically distant dragonfly,
Pseudothemis zonata.
E93 is essential for adult morphogenesis, and RNAi of
Kr-h1 induced precocious metamorphosis in epidermis via up-regulation of
E93. Precocious metamorphosis was also induced by RNAi of the juvenile hormone receptor
Methoprene-tolerant (
Met), confirming that the regulation of metamorphosis by the MEKRE93 (Met-Kr-h1-E93) pathway is conserved across diverse insects including the basal insect lineage Odonata. Notably, RNAi of
broad produced unique grayish pigmentation on the nymphal abdominal epidermis. Survey of downstream genes for
Kr-h1,
broad, and
E93 uncovered that unlike other insects,
broad regulates a substantial number of nymph-specific and adult-specific genes independently of
Kr-h1 and
E93. These findings highlight the importance of functional changes and rewiring of the transcription factors
Kr-h1,
broad, and
E93 in the evolution of insect metamorphosis.
