Juvenile hormone signaling in short germ-band hemimetabolan embryos

Abstract

The role of juvenile hormone (JH) in insect embryos is far from understood, especially in short germ-band hemimetabolan species. To shed light on this issue, we depleted the mRNA levels of Krüppel homolog 1, Methoprene-tolerant and JH acid -methyltransferase, key elements of JH signaling, in embryos of the short germ-band hemimetabolan species This precluded the formation of the germ-band anlage in a group of embryos. Hatchability was also reduced, which might have been caused by premature upregulation of laccase 2, a promoter of cuticle tanning. In other cases, development was interrupted in mid embryogenesis, involving defects related to dorsal closure and appendage formation. These phenotypes possibly result from the low levels of Broad-complex (BR-C) produced under JH-depleted conditions. This contrasts with holometabolan species, in which JH does not promote expression, which remains low during embryo development. Possibly, the stimulatory role of JH on expression and the morphogenetic functions of BR-C in hemimetabolan embryos were lost in holometabolan species. If so, this might have been a key driver for the evolution of holometabolan metamorphosis.

Comparative Transcriptomics in Two Extreme Neopterans Reveals General Trends in the Evolution of Modern Insects

“…Moreover, the high expression of JH genes in early embryogenesis observed in B. germanica may be typical of the hemimetabolan species. Indeed, JH genes have been shown to have important functions in early embryogenesis of B. germanica ( Fernandez-Nicolas and Belles, 2017 ), which does not appear to be the case in the holometabolan silkworm, Bombyx mori ( Daimon et al., 2015 ).…”

“…Many of them appear to be specific, but some observed in JH and 20E transducers could be representative of the type of embryogenesis and/or metamorphosis. For example, transcripts of JH transducers that are present at significant amounts in very early embryo stages of B. germanica , but not in D. melanogaster , may reflect a different regulation of the blastoderm formation related to the germband type, short ( B. germanica ) or long ( D. melanogaster ) (see Fernandez-Nicolas and Belles, 2017 , for functional studies). It is plausible that loss of these JH transducers in the very early embryo has been one of the drivers of evolution from short to long germband.…”

“…It is plausible that loss of these JH transducers in the very early embryo has been one of the drivers of evolution from short to long germband. Another difference relates to the expression of these hormonal transducers in the mid and late embryo, which is quantitatively and functionally important in hemimetabolan species ( Fernandez-Nicolas and Belles, 2017 , Piulachs et al., 2010 ) but not in holometabolans ( Daimon et al., 2015 ). Thus, the declining influence of JH in the embryo may have been another factor driving the morphological divergence of juvenile stages in the holometabolan last common ancestor and the evolution of metamorphosis toward holometaboly.…”

“…(2013) , a fundamental innovation in postembryonic development in holometabolans has been an expansion of BR-C functions, from one specialized in wing development to a larger array of morphogenetic functions that culminated with the pupal specifier role. Conversely, in hemimetabolans, BR-C would have important morphogenetic roles in embryo development, and its loss may have been an important factor in the evolution of holometaboly from hemimetaboly (see also Fernandez-Nicolas and Belles, 2017 ).…”

DNA methylation in cockroaches is essential in early embryo development and reduces gene expression noise

“…Maternal RNAi assays have been described previously (Fernandez-Nicolas and Belles 2017). DNMT1 and DNMT3 sequences were amplified by PCR and then cloned into pSTBlue-1 vector.…”