Holometabolous Insects Research Articles

Endophytic ancestors of modern leaf miners may have evolved in the Late Carboniferous.

Endophytic feeding behaviors, including stem borings and galling, have been observed in the fossil record from as early as the Devonian and involve the consumption of a variety of plant (and fungal) tissues. Historically, the exploitation of internal stem tissues through galling has been well documented as emerging during the Pennsylvanian (c. 323-299 million years ago (Ma)), replaced during the Permian by galling of foliar tissues. However, leaf mining, a foliar endophytic behavior that today is exhibited exclusively by members of the four hyperdiverse holometabolous insect orders, has been more sparsely documented, with confirmed examples dating back only to the Early Triassic (c. 252-250 Ma). Here, we describe a trace fossil on seed-fern foliage from the Rhode Island Formation of Massachusetts, USA, representing the earliest indication of a general, endophytic type of feeding damage and dating from the Middle Pennsylvanian (c. 312 Ma). Although lacking the full features of Mesozoic leaf mines, this specimen provides evidence of how endophytic mining behavior may have originated. It sheds light on the evolutionary transition to true foliar endophagy, contributes to our understanding of the behaviors of early holometabolous insects, and enhances our knowledge of macroevolutionary patterns of plant-insect interactions.

Day-flying lepidoptera larvae have a poorer ability to thermoregulate than adults.

Changes to ambient temperatures under climate change may detrimentally impact small ectotherms that rely on their environment for thermoregulation; however, there is currently a limited understanding of insect larval thermoregulation. As holometabolous insects, Lepidoptera differ in morphology, ecology and behaviour across the life cycle, and so it is likely that adults and larvae differ in their capacity to thermoregulate. In this study, we investigated the thermoregulatory capacity (buffering ability) of 14 species of day-flying Lepidoptera, whether this is influenced by body length or gregariousness, and whether it differs between adult and larval life stages. We also investigated what thermoregulation mechanisms are used: microclimate selection (choosing locations with a particular temperature) or behavioural thermoregulation (controlling temperature through other means, such as basking). We found that Lepidoptera larvae differ in their buffering ability between species and body lengths, but gregariousness did not influence buffering ability. Larvae are worse at buffering themselves against changes in air temperature than adults. Therefore Lepidoptera may be more vulnerable to adverse temperature conditions during their larval life stage. Adults and larvae rely on different thermoregulatory mechanisms; adults primarily use behavioural thermoregulation, whereas larvae use microclimate selection. This implies that larvae are highly dependent on the area around their foodplant for effective thermoregulation. These findings have implications for the management of land and species, for example, highlighting the importance of creating and preserving microclimates and vegetation complexity surrounding Lepidoptera foodplants for larval thermoregulation under future climate change.

Matrix metalloproteinase 2 contributes to adult eclosion and immune response in the small hive beetle, Aethina tumida.

During the pupal-adult eclosion process of holometabolous insects, the old cuticle is shed and replaced by a completely different new cuticle that requires tanning and expansion, along with extensive extracellular matrix (ECM) remodeling. In vertebrates, matrix metalloproteinases (MMPs), a class of zinc-dependent endopeptidases, play key roles in regulating the ECM that surrounds cells. However, little is known about these extracellular proteinases available in insects. The small hive beetle (SHB), Aethina tumida, is a widespread invasive parasite of honey bees. In this study, 6 MMP homologs were identified in the SHB genome. RNA interference experiments showed that all 6 AtMmps are not required for the larval-pupal transition, only AtMmp2 was essential for pupal-adult eclosion in SHB. Knockdown of AtMmp2 resulted in eclosion defects and wing expansion failure, as well as mortality within 3d of adult eclosion. Transcriptomic analysis revealed that knockdown of AtMmp2 significantly increased expression of the Toll and Imd pathways, chitin metabolism, and cross-linking (such as the pro-phenoloxidase activating cascade pathway and the tyrosine-mediated cuticle sclerotization and pigmentation pathway). These data revealed evolutionarily conserved functions of Mmp2 in controlling adult eclosion and wing expansion, also provided a preliminary exploration of the novel function of regulating Toll and Imd pathways, as well as new insights into how MMPs regulate insect development and defense barriers.

Increase in heat tolerance following a period of heat stress in a naturally occurring insect species.

Climate warming is the defining environmental crisis of the 21st century. Elucidating whether organisms can adapt to rapidly changing thermal environments is therefore a crucial research priority. We investigated warming effects on a native Hemipteran insect (Murgantia histrionica) that feeds on an endemic plant species (Isomeris arborea) of the California coastal sage scrub. Experiments conducted in 2009 quantified the temperature responses of juvenile maturation rates and stage-specific and cumulative survivorship. The intervening decade has seen some of the hottest years ever recorded, with increasing mean temperatures accompanied by an increase in the frequency of hot extremes. Experiments repeated in 2021 show a striking change in the bugs' temperature responses. In 2009, no eggs developed past the second nymphal stage at 33°C. In 2021, eggs developed into reproductive adults at 33°C. Upper thermal limits for maturation and survivorship have increased, along with a decrease in mortality risk with increasing age and temperature, and a decrease in the temperature sensitivity of mortality with increasing age. While we cannot exclude the possibility that other environmental factors occurring in concert could have affected our findings, the fact that all observed trait changes are in the direction of greater heat tolerance suggests that consistent exposure to extreme heat stress may at least be partially responsible for these changes. Harlequin bugs belong to the suborder Heteroptera, which contains a number of economically important pests, biological control agents and disease carriers. Their differential success in withstanding warming compared to beneficial holometabolous insects such as pollinators may exacerbate the decline of beneficial insects due to other causes (e.g. pollution and pesticides) with potentially serious consequences on both biodiversity and ecosystem functioning.

Gut bacterial population and community dynamics following adult emergence in pest tephritid fruit flies

Gut microbiota are important contributors to insect success. Host-microbe interactions are dynamic and can change as hosts age and/or encounter different environments. A turning point in these relationships the transition from immature to adult life stages, particularly for holometabolous insects where there is radical restructuring of the gut. Improved knowledge of population and community dynamics of gut microbiomes upon adult emergence inform drivers of community assembly and physiological aspects of host-microbe interactions. Here, we evaluated the bacterial communities of the pest tephritid species melon fly (Zeugodacus cucurbitae) and Medditeranean fruit fly (medfly, Ceratitis capitata) associated with the pupae life stage and timepoints immediately following adult eclosion. We used a combination of culturing to determine cultivatable bacterial titers, qPCR to determine 16S-rRNA SSU copy numbers, and 16S V4 sequencing to determine changes in communities. Both culturing and qPCR revealed that fly bacterial populations declined upon adult emergence by 10 to 100-fold followed by recovery within 24 h following eclosion. Titers reached ~ 107 CFUs (~ 108 16S rRNA copies) within a week post-emergence. We also observed concurrent changes in amplicon sequence variance (ASVs), where the ASV composition differed overtime for both melon fly and medfly adults at different timepoints. Medfly, in particular, had different microbiome compositions at each timepoint, indicating greater levels of variation before stabilization. These results demonstrate that tephritid microbiomes experience a period of flux following adult emergence, where both biomass and the makeup of the community undergoes dramatic shifts. The host-microbe dynamics we document suggest plasticity in the community and that there may be specific periods where the tephritid gut microbiome may be pliable to introduce and establish new microbial strains in the host.

The Intricate Role of Ecdysis Triggering Hormone Signaling in Insect Development and Reproductive Regulation.

Insect growth is interrupted by molts, during which the insect develops a new exoskeleton. The exoskeleton confers protection and undergoes shedding between each developmental stage through an evolutionarily conserved and ordered sequence of behaviors, collectively referred to as ecdysis. Ecdysis is triggered by Ecdysis triggering hormone (ETH) synthesized and secreted from peripheral Inka cells on the tracheal surface and plays a vital role in the orchestration of ecdysis in insects and possibly in other arthropod species. ETH synthesized by Inka cells then binds to ETH receptor (ETHR) present on the peptidergic neurons in the central nervous system (CNS) to facilitate synthesis of various other neuropeptides involved in ecdysis. The mechanism of ETH function on ecdysis has been well investigated in holometabolous insects such as moths Manduca sexta and Bombyx mori, fruit fly Drosophila melanogaster, the yellow fever mosquito Aedes aegypti and beetle Tribolium castaneum etc. In contrast, very little information is available about the role of ETH in sequential and gradual growth and developmental changes associated with ecdysis in hemimetabolous insects. Recent studies have identified ETH precursors and characterized functional and biochemical features of ETH and ETHR in a hemimetabolous insect, desert locust, Schistocerca gregaria. Recently, the role of ETH in Juvenile hormone (JH) mediated courtship short-term memory (STM) retention and long-term courtship memory regulation and retention have also been investigated in adult male Drosophila. Our review provides a novel synthesis of ETH signaling cascades and responses in various insects triggering diverse functions in adults and juvenile insects including their development and reproductive regulation and might allow researchers to develop sustainable pest management strategies by identifying novel compounds and targets.

Functional Divergence of the Tribolium castaneum engrailed and invected Paralogs.

Engrailed (en) and invected (inv) encode paralogous transcription factors found as a closely linked tandem duplication within holometabolous insects. Drosophila en mutants segment normally, then fail to maintain their segments. Loss of Drosophila inv is viable, while loss of both genes results in asegmental larvae. Surprisingly, the knockdown of Oncopeltus inv can result in the loss or fusion of the entire abdomen and en knockdowns in Tribolium show variable degrees of segmental loss. The consequence of losing or knocking down both paralogs on embryogenesis has not been studied beyond Drosophila. To further investigate the relative functions of each paralog and the mechanism behind the segmental loss, Tribolium double and single knockdowns of en and inv were analyzed. The most common cuticular phenotype of the double knockdowns was small, limbless, and open dorsally, with all but a single, segmentally iterated row of bristles. Less severe knockdowns had fused segments and reduced appendages. The Tribolium paralogs appear to act synergistically: the knockdown of either Tribolium gene alone was typically less severe, with all limbs present, whereas the most extreme single knockdowns mimic the most severe double knockdown phenotype. Morphological abnormalities unique to either single gene knockdown were not found. inv expression was not affected in the Tribolium en knockdowns, but hh expression was unexpectedly increased midway through development. Thus, while the segmental expression of en/inv is broadly conserved within insects, the functions of en and inv are evolving independently in different lineages.

State dependency of behavioural traits is a function of the life stage in a holometabolous insect

State dependency of behavioural traits is a function of the life stage in a holometabolous insect

Identification of ecdysone receptor target genes in the worker honey bee brains during foraging behavior

Ecdysone signaling plays central roles in morphogenesis and female ovarian development in holometabolous insects. In the European honey bee (Apis mellifera L.), however, ecdysone receptor (EcR) is expressed in the brains of adult workers, which have already undergone metamorphosis and are sterile with shrunken ovaries, during foraging behavior. Aiming at unveiling the significance of EcR signaling in the worker brain, we performed chromatin-immunoprecipitation sequencing of EcR to search for its target genes using the brains of nurse bees and foragers. The majority of the EcR targets were common between the nurse bee and forager brains and some of them were known ecdysone signaling-related genes. RNA-sequencing analysis revealed that some EcR target genes were upregulated in forager brains during foraging behavior and some were implicated in the repression of metabolic processes. Single-cell RNA-sequencing analysis revealed that EcR and its target genes were expressed mostly in neurons and partly in glial cells in the optic lobes of the forager brain. These findings suggest that in addition to its role during development, EcR transcriptionally represses metabolic processes during foraging behavior in the adult worker honey bee brain.

A STIM dependent dopamine-neuropeptide axis maintains the larval drive to feed and grow in Drosophila.

Appropriate nutritional intake is essential for organismal survival. In holometabolous insects such as Drosophila melanogaster, the quality and quantity of food ingested as larvae determines adult size and fecundity. Here we have identified a subset of dopaminergic neurons (THD') that maintain the larval motivation to feed. Dopamine release from these neurons requires the ER Ca2+ sensor STIM. Larvae with loss of STIM stop feeding and growing, whereas expression of STIM in THD' neurons rescues feeding, growth and viability of STIM null mutants to a significant extent. Moreover STIM is essential for maintaining excitability and release of dopamine from THD' neurons. Optogenetic stimulation of THD' neurons activated neuropeptidergic cells, including median neuro secretory cells that secrete insulin-like peptides. Loss of STIM in THD' cells alters the developmental profile of specific insulin-like peptides including ilp3. Loss of ilp3 partially rescues STIM null mutants and inappropriate expression of ilp3 in larvae affects development and growth. In summary we have identified a novel STIM-dependent function of dopamine neurons that modulates developmental changes in larval feeding behaviour and growth.

Steroid hormone regulation of innate immunity in Drosophila melanogaster.

Endocrine signaling networks control diverse biological processes and life history traits across metazoans. In both invertebrate and vertebrate taxa, steroid hormones regulate immune system function in response to intrinsic and environmental stimuli, such as microbial infection. The mechanisms of this endocrine-immune regulation are complex and constitute an ongoing research endeavor facilitated by genetically tractable animal models. The 20-hydroxyecdysone (20E) is the major steroid hormone in arthropods, primarily studied for its essential role in mediating developmental transitions and metamorphosis; 20E also modulates innate immunity in a variety of insect taxa. This review provides an overview of our current understanding of 20E-mediated innate immune responses. The prevalence of correlations between 20E-driven developmental transitions and innate immune activation are summarized across a range of holometabolous insects. Subsequent discussion focuses on studies conducted using the extensive genetic resources available in Drosophila that have begun to reveal the mechanisms underlying 20E regulation of immunity in the contexts of both development and bacterial infection. Lastly, I propose directions for future research into 20E regulation of immunity that will advance our knowledge of how interactive endocrine networks coordinate animals' physiological responses to environmental microbes.

Discovery of the oldest known elmid larva (Coleoptera, Elmidae) from the Lower Eocene of Rajasthan (India, Palana Formation)

A single elmid larva is reported from a laminate maroon shale bed of Gurha opencast lignite mine (Palana Formation, early Eocene, Bikaner District, north-western Rajasthan, India). It is the first fossil larva that can be attributed to Elmidae with certainty. A generic assignation is not possible, because the larva is strongly compressed, and the most important characters are not visible or poorly preserved. The larva is described morphologically and illustrated by photographs and line drawings. A larva of a holometabolous insect from Baltic amber, which was published recently as a member of Elmidae by Zippel et al. (2022), possesses no structural characters that would clearly suggest placement in this family. A photograph of the hitherto unknown larva of the extant Grouvellinus rioloides from Kyrgyzstan is included for comparison.

20-hydroxyecdysone reprograms amino acid metabolism to support the metamorphic development of Helicoverpa armigera

Amino acid metabolism is regulated according to nutrient conditions; however, the mechanism is not fully understood. Using the holometabolous insect cotton bollworm (Helicoverpa armigera) as a model, we report that hemolymph metabolites are greatly changed from the feeding larvae to the wandering larvae and to pupae. Arginine, alpha-ketoglutarate (α-KG), and glutamate (Glu) are identified as marker metabolites of feeding larvae, wandering larvae, and pupae, respectively. Arginine level is decreased by 20-hydroxyecdysone (20E) regulation via repression of argininosuccinate synthetase (Ass) expression and upregulation of arginase (Arg) expression during metamorphosis. α-KG is transformed from Glu by glutamate dehydrogenase (GDH) inlarval midgut, which is repressed by 20E. The α-KG is then transformed to Glu by GDH-like in pupal fatbody, which is upregulated by 20E. Thus, 20E reprogrammed amino acid metabolism during metamorphosis by regulating gene expression in a stage- and tissue-specific manner to support insect metamorphic development.

20-Hydroxyecdysone counteracts insulin to promote programmed cell death by modifying phosphoglycerate kinase 1

BackgroundThe regulation of glycolysis and autophagy during feeding and metamorphosis in holometabolous insects is a complex process that is not yet fully understood. Insulin regulates glycolysis during the larval feeding stage, allowing the insects to grow and live. However, during metamorphosis, 20-hydroxyecdysone (20E) takes over and regulates programmed cell death (PCD) in larval tissues, leading to degradation and ultimately enabling the insects to transform into adults. The precise mechanism through which these seemingly contradictory processes are coordinated remains unclear and requires further research. To understand the coordination of glycolysis and autophagy during development, we focused our investigation on the role of 20E and insulin in the regulation of phosphoglycerate kinase 1 (PGK1). We examined the glycolytic substrates and products, PGK1 glycolytic activity, and the posttranslational modification of PGK1 during the development of Helicoverpa armigera from feeding to metamorphosis.ResultsOur findings suggest that the coordination of glycolysis and autophagy during holometabolous insect development is regulated by a balance between 20E and insulin signaling pathways. Glycolysis and PGK1 expression levels were decreased during metamorphosis under the regulation of 20E. Insulin promoted glycolysis and cell proliferation via PGK1 phosphorylation, while 20E dephosphorylated PGK1 via phosphatase and tensin homolog (PTEN) to repress glycolysis. The phosphorylation of PGK1 at Y194 by insulin and its subsequent promotion of glycolysis and cell proliferation were important for tissue growth and differentiation during the feeding stage. However, during metamorphosis, the acetylation of PGK1 by 20E was key in initiating PCD. Knockdown of phosphorylated PGK1 by RNA interference (RNAi) at the feeding stage led to glycolysis suppression and small pupae. Insulin via histone deacetylase 3 (HDAC3) deacetylated PGK1, whereas 20E via acetyltransferase arrest-defective protein 1 (ARD1) induced PGK1 acetylation at K386 to stimulate PCD. Knockdown of acetylated-PGK1 by RNAi at the metamorphic stages led to PCD repression and delayed pupation.ConclusionsThe posttranslational modification of PGK1 determines its functions in cell proliferation and PCD. Insulin and 20E counteractively regulate PGK1 phosphorylation and acetylation to give it dual functions in cell proliferation and PCD.

Steroid hormone-dependent changes in trehalose physiology in the silkworm, Bombyx mori.

Holometabolous insects undergo metamorphosis to reconstruct their body to the adult form during pupal period. Since pupae cannot take any diets from the outside because of a hard pupal cuticle, those insects stock up on nutrients sufficient for successful metamorphosis during larval feeding period. Among those nutrients, carbohydrates are stored as glycogen or trehalose, which is the major blood sugar in insects. The hemolymph trehalose is constantly high during the feeding period but suddenly decreases at the beginning of the prepupal period. It is believed that trehalase, which is a trehalose-hydrolyzing enzyme, becomes highly active to reduce hemolymph trehalose level during prepupal period. This change in the hemolymph trehalose level has been interpreted as the physiological shift from storage to utilization of trehalose at that stage. Although this shift in trehalose physiology is indispensable for energy production required for successful metamorphosis, little is known on the regulatory mechanisms of trehalose metabolism in accordance with developmental progress. Here, we show that ecdysone, an insect steroid hormone, plays essential roles in the regulation of soluble trehalase activity and its distribution in the midgut of silkworm, Bombyx mori. In the end of larval period, soluble trehalase was highly activated in the midgut lumen. This activation was disappeared in the absence of ecdysone and also restored by ecdysone administration. Our present results suggest that ecdysone is essentially required for the changes in the function of the midgut on trehalose physiology as development progresses.

Metabolic changes during larval-pupal metamorphosis of Helicoverpa armigera.

Energy metabolism is essential for insect metamorphosis. The accumulation and utilization of energy is still not completely clear during larval-pupal metamorphosis of holometabolous insects. We used metabolome and transcriptome analysis to reveal key metabolic changes in the fat body and plasma and the underlying metabolic regulation mechanism of Helicoverpa armigera, an important global agricultural insect pest, during larval-pupal metamorphosis. During the feeding stage, activation of aerobic glycolysis provided intermediate metabolites and energy for cell proliferation and lipid synthesis. During the non-feeding stages (the initiation of the wandering stage and the prepupal stage), aerobic glycolysis was suppressed, while, triglyceride degradation was activated in the fat body. The blocking of metabolic pathways in the fat body was probably caused by 20-hydroxyecdysone-induced cell apoptosis. 20-hydroxyecdysone cooperated with carnitine to promote the degradation of triglycerides and the accumulation of acylcarnitines in the hemolymph, allowing rapid transportation and supply of lipids from the fat body to other organs, which provided a valuable reference for revealing the metabolic regulation mechanism of lepidopteran larvae during the last instar. Carnitine and acylcarnitines are first reported to be key factors that mediate the degradation and utilization of lipids during larval-pupal metamorphosis of lepidopteran insects.

Oskar acts with the transcription factor Creb to regulate long-term memory in crickets

Novel genes have the potential to drive the evolution of new biological mechanisms, or to integrate into preexisting regulatory circuits and contribute to the regulation of older, conserved biological functions. One such gene, the novel insect-specific gene oskar, was first identified based on its role in establishing the Drosophila melanogaster germ line. We previously showed that this gene likely arose through an unusual domain transfer event involving bacterial endosymbionts and played a somatic role before evolving its well-known germ line function. Here, we provide empirical support for this hypothesis in the form of evidence for a neural role for oskar. We show that oskar is expressed in the adult neural stem cells of a hemimetabolous insect, the cricket Gryllus bimaculatus. In these stem cells, called neuroblasts, oskar is required together with the ancient animal transcription factor Creb to regulate long-term (but not short-term) olfactory memory. We provide evidence that oskar positively regulates Creb, which plays a conserved role in long-term memory across animals, and that oskar in turn may be a direct target of Creb. Together with previous reports of a role for oskar in nervous system development and function in crickets and flies, our results are consistent with the hypothesis that oskar's original somatic role may have been in the insect nervous system. Moreover, its colocalization and functional cooperation with the conserved pluripotency gene piwi in the nervous system may have facilitated oskar's later co-option to the germ line in holometabolous insects.

The snakeflies of the Mediterranean islands: review and biogeographical analysis (Neuropterida, Raphidioptera)

The Mediterranean region representsone of the hotspots of biodiversity of many organisms and among these also of Raphidioptera. With about 250 known species world-wide Raphidioptera is the smallest order of extant holometabolous insects.The Mediterranean region harbors 113 species (= >45% of the world fauna), and of these 33 (= >13% of the world fauna) have been found on islands of the Mediterranean Sea. In the course of the past 50 years most of the larger islands have been intensively explored for Raphidioptera, particularly all islands (except the Baleares) which had no connection to the mainland throughout the whole Pleistocene. Altogether, 11 species of Raphidioptera (9 Raphidiidae, 2 Inocelliidae) are endemic to (usually)one, rarely to a few Mediterranean islands:Phaeostigma (Ph.) euboica (Euboea), Ph. (Aegeoraphidia) prophetica (Rhodes), Ph. (Ae.) karpathana (Karpathos), Ph. (Ae.) biroi (Crete), Ph. (Superboraphidia) minois (Crete),Subilla principiae(Sardinia),S. colossea(Rhodes), Raphidia (R.) peterressli (Chios), R. (R.) ariadne (Crete), Fibla (F.) maclachlani (Corsica, Sardinia, Sicily), F. (Reisserella) pasiphae (Crete).In the Aegean Sea there is a remarkable difference between the eastern and the western islands marked by the so-called Rechinger line based on results of the analysis of the flora. The Raphidioptera confirm this line impressively.It is rather unlikely that further Raphidioptera species endemic to Mediterranean islands are still to be detected – with one exception: the Baleares. A few additional species known from various parts of the continents surrounding the Mediterranean Sea will probably be found on islands so that a total number may be around 40, possibly around 45 species.The possible ways and times of colonization of the islands by Raphidioptera are discussed. The present paper may serve as a basis for studies on natural and particularly on anthropogenic dispersals of snakeflies from island to island, from mainland to islands, and from islands to the mainland in connection with phylogeographic investigations.

Mycotoxin tolerance affects larval competitive ability in Drosophila recens (Diptera: Drosophilidae).

Certain mycophagous Drosophila species are the only known eukaryotes that can tolerate some highly potent mycotoxins. This association between mycophagy and mycotoxin tolerance is well established because Drosophila species that switch hosts from mushrooms to other food sources lose their mycotoxin tolerance trait without any evolutionary lag. These findings suggest that mycotoxin tolerance may be a costly trait to maintain. In this study, we attempted to identify whether mycotoxin tolerance has a fitness cost. Larval competitive ability is a vital fitness trait, especially in holometabolous insects, where the larvae cannot move to a new host. Furthermore, larval competitive ability is known to be associated with many critical life-history traits. Here we studied whether mycotoxin tolerance adversely affects larval competitive ability on isofemale lines from 2 distinct locations. We observed that the extent of mycotoxin tolerance affected larval competitive ability, but only in isofemale lines from one location. Additionally, we observed that the high mycotoxin-tolerant isofemale lines from the same location showed poor survival to eclosion. This study shows that mycotoxin tolerance is associated with fitness costs and provides preliminary evidence of an association between local adaptation and mycotoxin tolerance.

Antagonistic role of the BTB-zinc finger transcription factors Chinmo and Broad-Complex in the juvenile/pupal transition and in growth control.

During development, the growing organism transits through a series of temporally regulated morphological stages to generate the adult form. In humans, for example, development progresses from childhood through to puberty and then to adulthood, when sexual maturity is attained. Similarly, in holometabolous insects, immature juveniles transit to the adult form through an intermediate pupal stage when larval tissues are eliminated and the imaginal progenitor cells form the adult structures. The identity of the larval, pupal, and adult stages depends on the sequential expression of the transcription factors chinmo, Br-C, and E93. However, how these transcription factors determine temporal identity in developing tissues is poorly understood. Here, we report on the role of the larval specifier chinmo in larval and adult progenitor cells during fly development. Interestingly, chinmo promotes growth in larval and imaginal tissues in a Br-C-independent and -dependent manner, respectively. In addition, we found that the absence of chinmo during metamorphosis is critical for proper adult differentiation. Importantly, we also provide evidence that, in contrast to the well-known role of chinmo as a pro-oncogene, Br-C and E93 act as tumour suppressors. Finally, we reveal that the function of chinmo as a juvenile specifier is conserved in hemimetabolous insects as its homolog has a similar role in Blatella germanica. Taken together, our results suggest that the sequential expression of the transcription factors Chinmo, Br-C and E93 during larva, pupa an adult respectively, coordinate the formation of the different organs that constitute the adult organism.