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

Abstract

Insect metamorphosis generates reproductive adults and is commonly accompanied by 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 adult 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 obvious effect on E93 transcription, while treatment on male prepupae resulted in decreased E93 transcripts. In this study, we emphasize the importance of examining cases of atypical 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.\n\nGraphical abstract\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=91 SRC=\"FIGDIR/small/283556v1_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (21K):\norg.highwire.dtl.DTLVardef@1dca37corg.highwire.dtl.DTLVardef@7142a5org.highwire.dtl.DTLVardef@1ce7675org.highwire.dtl.DTLVardef@1c30267_HPS_FORMAT_FIGEXP M_FIG C_FIG Highlights- Neotenic female Planococcus kraunhiae (Japanese mealybug) develops with low E93 expression.\n- E93 expression pattern during male development is typical to other insects.\n- Juvenile hormone mimic treatment on male prepupae results in decreased E93 transcripts.\n- Juvenile hormone mimic treatment on female nymphs does not have obvious effects on E93 transcription.\n- Female mealybugs have low sensitivity to juvenile hormone mimic treatments compared to males and other insects.