Highlights ► The JH–Methoprene-tolerant (Met)–cofactor complex regulates specific genes. ► JH regulates larval molting through Krüppel homolog. ► JH regulates metamorphosis by controlling ...ecdysone-induced Broad (Br) expression. ► JH stimulates Tribolium vitellogenesis indirectly via production of specific ILPs. ► Timing of Drosophila optic lobe development and female receptivity requires JH-Met.
Developmental, genetic and endocrine data from diverse taxa provide insight into the evolution of insect metamorphosis. We equate the larva-pupa-adult of the Holometabola to the pronymph-nymph-adult ...of hemimetabolous insects. The hemimetabolous pronymph is a cryptic embryonic stage with unique endocrinology and behavioural modifications that probably served as preadaptations for the larva. It develops in the absence of juvenile hormone (JH) as embryonic primordia undergo patterning and morphogenesis, the processes that were arrested for the evolution of the larva. Embryonic JH then drives tissue differentiation and nymph formation. Experimental treatment of pronymphs with JH terminates patterning and induces differentiation, mimicking the processes that occurred during the evolution of the larva. Unpatterned portions of primordia persist in the larva, becoming imaginal discs that form pupal and adult structures. Key transcription factors are associated with the holometabolous life stages: Krüppel-homolog 1 (Kr-h1) in the larva, broad in the pupa and E93 in the adult. Kr-h1 mediates JH action and is found whenever JH acts, while the other two genes direct the formation of their corresponding stages. In hemimetabolous forms, the pronymph has low Broad expression, followed by Broad expression through the nymphal moults, then a switch to E93 to form the adult. This article is part of the theme issue 'The evolution of complete metamorphosis'.
The molecular action of juvenile hormone (JH), a regulator of vital importance to insects, was until recently regarded as a mystery. The past few years have seen an explosion of studies of JH ...signaling, sparked by a finding that a JH-resistance gene, Methoprene-tolerant (Met), plays a critical role in insect metamorphosis. Here, we summarize the recently acquired knowledge on the capacity of Met to bind JH, which has been mapped to a particular ligand-binding domain, thus establishing this bHLH-PAS protein as a novel type of an intracellular hormone receptor. Next, we consider the significance of JH-dependent interactions of Met with other transcription factors and signaling pathways. We examine the regulation and biological roles of genes acting downstream of JH and Met in insect metamorphosis. Finally, we discuss the current gaps in our understanding of JH action and outline directions for future research.
This autobiographical article describes the research career of Lynn M. Riddiford from its early beginnings in a summer program for high school students at Jackson Laboratory to the present ..."retirement" at the Friday Harbor Laboratories. The emphasis is on her forays into many areas of insect endocrinology, supported by her graduate students and postdoctoral associates. The main theme is the hormonal regulation of metamorphosis, especially the roles of juvenile hormone (JH). The article describes the work of her laboratory first in the elucidation of the endocrinology of the tobacco hornworm,
, and later in the molecular aspects of the regulation of cuticular and pigment proteins and of the ecdysone-induced transcription factor cascade during molting and metamorphosis. Later studies utilized
to answer further questions about the actions of JH.
Background: The timely onset of metamorphosis in holometabolous insects depends on their reaching the appropriate size known as critical weight. Once critical weight is reached, juvenile hormone (JH) ...titers decline, resulting in the release of prothoracicotropic hormone (PTTH) at the next photoperiod gate and thereby inducing metamorphosis. How individuals determine when they have reached critical weight is unknown. We present evidence that in Drosophila, a component of the ring gland, the prothoracic gland (PG), assesses growth to determine when critical weight has been achieved.
Results: We used the GAL4/UAS system to suppress or enhance growth by overexpressing PTEN or Dp110, respectively, in various components of the ring gland. Suppression of the growth of the PG and CA, but not of the CA alone, produced larger-than-normal larvae and adults. Suppression of only PG growth resulted in nonviable larvae, but larvae with enlarged PGs produced significantly smaller larvae and adults. Rearing larvae with enlarged PGs under constant light enhanced these effects, suggesting a role for photoperiod-gated PTTH secretion. These larvae are smaller, in part as a result of their repressed growth rates, a phenotype that could be rescued through nutritional supplementation (yeast paste). Most importantly, larvae with enlarged PGs overestimated size so that they initiated metamorphosis before surpassing the minimal viable weight necessary to survive pupation.
Conclusions: The PG acts as a size-assessing tissue by using insulin-dependent PG cell growth to determine when critical weight has been reached.
Abstract
During postembryonic life, hormones, including ecdysteroids, juvenile hormones, insulin-like peptides, and activin/TGFβ ligands act to transform the larval nervous system into an adult ...version, which is a fine-grained mosaic of recycled larval neurons and adult-specific neurons. Hormones provide both instructional signals that make cells competent to undergo developmental change and timing cues to evoke these changes across the nervous system. While touching on all the above hormones, our emphasis is on the ecdysteroids, ecdysone and 20-hydroxyecdysone (20E). These are the prime movers of insect molting and metamorphosis and are involved in all phases of nervous system development, including neurogenesis, pruning, arbor outgrowth, and cell death. Ecdysteroids appear as a series of steroid peaks that coordinate the larval molts and the different phases of metamorphosis. Each peak directs a stereotyped cascade of transcription factor expression. The cascade components then direct temporal programs of effector gene expression, but the latter vary markedly according to tissue and life stage. The neurons read the ecdysteroid titer through various isoforms of the ecdysone receptor, a nuclear hormone receptor. For example, at metamorphosis the pruning of larval neurons is mediated through the B isoforms, which have strong activation functions, whereas subsequent outgrowth is mediated through the A isoform through which ecdysteroids play a permissive role to allow local tissue interactions to direct outgrowth. The major circulating ecdysteroid can also change through development. During adult development ecdysone promotes early adult patterning and differentiation while its metabolite, 20E, later evokes terminal adult differentiation.
The molecular control of insect metamorphosis from larva to pupa to adult has long been a mystery. The Broad and E93 transcription factors, which can modify chromatin domains, are known to direct the ...production of the pupa and the adult, respectively. We now show that chinmo, a gene related to broad, is essential for the repression of these metamorphic genes. Chinmo is strongly expressed during the formation and growth of the larva and its removal results in the precocious expression of broad and E93 in the first stage larva, causing a shift from larval to premetamorphic functions. This trinity of Chinmo, Broad, and E93 regulatory factors is mutually inhibitory. The interaction of this network with regulatory hormones likely ensures the orderly progression through insect metamorphosis.
Juvenile hormone (JH) is a unique sesquiterpenoid hormone which regulates both insect metamorphosis and insect reproduction. It also may be utilized by some insects to mediate polyphenisms and other ...life history events that are environmentally regulated. This article details the history of the research on this versatile hormone that began with studies by V. B. Wigglesworth on the “kissing bug”
Rhodnius prolixus
in 1934, through the discovery of a natural source of JH in the abdomen of male
Hyalophora cecropia
moths by C. M. Williams that allowed its isolation (“golden oil”) and identification, to the recent research on its receptor, termed
Methoprene-tolerant
(
Met
). Our present knowledge of cellular actions of JH in metamorphosis springs primarily from studies on
Rhodnius
and the tobacco hornworm
Manduca sexta
, with recent studies on the flour beetle
Tribolium castaneum
, the silkworm
Bombyx mori
, and the fruit fly
Drosophila melanogaster
contributing to the molecular understanding of these actions. Many questions still need to be resolved including the molecular basis of competence to metamorphose, differential tissue responses to JH, and the interaction of nutrition and other environmental signals regulating JH synthesis and degradation.
Juvenile hormone (JH) is a key hormone in regulation of the insect's life history, both in maintaining the larval state during molts and in directing reproductive maturation. This short review ...highlights the recent papers of the past year that lend new insight into the role of this hormone in the larva and the mechanisms whereby it achieves this role.
PDF
