E93 expression and links to the juvenile hormone in hemipteran mealybugs with insights on female neoteny

Abstract

Insect metamorphosis produces reproductive adults and is commonly accompanied with the direct or indirect development of wings. In some winged insects, the imago is altered by life history changes. For instance, in scale insects and mealybugs, reproductive females retain juvenile features and are wingless. The transcription factor E93 triggers metamorphosis and plays in concert with the juvenile hormone pathway to guarantee the successful transition from juvenile to adult. We previously provided evidence of an atypical down-regulation of the juvenile hormone pathway during female development in the Japanese mealybug. Here, we further investigate how E93 is involved in the production of neotenic wingless females, by identifying its isoforms, assessing their expression patterns and evaluating the effect of exogenous juvenile hormone mimic treatment on E93. This study identifies three E93 isoforms on the 5' end, based on Japanese mealybug cDNA and shows that female development occurs with the near absence of E93 transcripts, as opposed to male metamorphosis. Additionally, while male development is typically affected by exogenous juvenile hormone mimic treatments, females seem to remain insensitive to the treatment, and up-regulation of the juvenile hormone signaling is not observed. Furthermore, juvenile hormone mimic treatment on female nymphs did not have an obvious effect on E93 transcription, while treatment on male prepupae resulted in depleted E93 transcripts. In this study, we emphasize the importance in examining atypical cases of metamorphosis as complementary systems to provide a better understanding on the molecular mechanisms underlying insect metamorphosis. For instance, the factors regulating the expression of E93 are largely unclear. Investigating the regulatory mechanism of E93 transcription could provide clues towards identifying the factors that induce or suppress E93 transcription, in turn triggering male adult development or female neoteny.

Keywords: E93; Hemimetaboly; Insect metamorphosis; Juvenile hormone; Mealybugs; Neoteny.