Krüppel homolog 1 and E93: The doorkeeper and the key to insect metamorphosis

Bellés, Xavier

doi:10.1002/arch.21609

Cited by 50 publications

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“…Moreover, these authors also showed the existence of an inverse relationship between Kr-h1 and E93 expression resulting from mutual repression effects. Our current findings therefore appear to be in agreement with the MEKRE93-based regulatory model for the control of metamorphosis (as reviewed by Belles, 2019) [ 23 ]. According to this recently proposed model, low JH titres in the final nymphal stage result in decreased signaling via Met, and this leads to reduced Kr-h1 expression, which will further result in de-repression of the E93 gene when a certain threshold is reached.…”

Section: Discussionsupporting

confidence: 90%

“…Significant differences in expression levels of the MEKRE93 pathway components E93 and Kr-h1 were detected in this study. Normally, the expression level of the adult specifier gene E93 increases in the second half of the final nymphal stage, when JH levels drop and ecdysteroid levels rise, to ensure the final transition to an adult [ 23 ]. Significantly downregulated SgE93 transcript levels were detected in the head of dsSgE93 -injected locusts on day four in the fifth nymphal stage, which can explain the transition to a supernumerary nymph instead of an adult locust ( Figure 3 C).…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, Kr-h1 is an early JH response gene, which has been reported in several insect species to mediate the metamorphosis-inhibiting status quo action downstream of the JH signal and its receptor Met [ 7 , 9 , 11 , 13 , 31 , 32 ]. Kr-h1 levels normally drop in the final nymphal stage, when JH titers are low, to ensure a final transition to the adult stage [ 23 ]. The very significantly increased SgKr-h1 expression in dsSgE93 -injected desert locust nymphs may thus have inhibited metamorphosis to the adult stage and instead resulted in supernumerary juvenile stages.…”

Section: Discussionmentioning

confidence: 99%

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RNAi-Mediated Knockdown of Transcription Factor E93 in Nymphs of the Desert Locust (Schistocerca gregaria) Inhibits Adult Morphogenesis and Results in Supernumerary Juvenile Stages

Gijbels

Marchal

Verdonckt

et al. 2020

IJMS

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Postembryonic development of insects is coordinated by juvenile hormone (JH) together with ecdysteroids. Whereas the JH early response gene krüppel-homolog 1 (Kr-h1) plays a crucial role in the maintenance of juvenile characteristics during consecutive larval stages, the ecdysteroid-inducible early gene E93 appears to be a key factor promoting metamorphosis and adult morphogenesis. Here, we report on the developmental and molecular consequences of an RNAi-mediated knockdown of SgE93 in the desert locust, Schistocerca gregaria, a hemimetabolan species. Our experimental data show that injection of gregarious locust nymphs with a double-stranded RNA construct targeting the SgE93 transcript inhibited the process of metamorphosis and instead led to supernumerary nymphal stages. These supernumerary nymphal instars still displayed juvenile morphological features, such as a nymphal color scheme and body shape, while they reached the physical body size of the adult locusts, or even surpassed it after the next supernumerary molt. Interestingly, when compared to control locusts, the total duration of the fifth and normally final nymphal (N5) stage was shorter than normal. This appeared to correspond with temporal and quantitative changes in hemolymph ecdysteroid levels, as well as with altered expression of the rate-limiting Halloween gene, Spook (SgSpo). In addition, the levels of the ecdysone receptor (SgEcR) and retinoïd X receptor (SgRXR) transcripts were altered, indicating that silencing SgE93 affects both ecdysteroid synthesis and signaling. Upon knockdown of SgE93, a very potent upregulation of the SgKr-h1 transcript levels was observed in both head and fat body, while no significant changes were detected in the transcript levels of SgJHAMT and SgCYP15A1, the enzymes that catalyze the two final steps in JH biosynthesis. Moreover, the process of molting was disturbed in these supernumerary nymphs. While attempting ecdysis to the next stage, 50% of the N6 and all N7 nymphal instars eventually died. S. gregaria is a very harmful, swarm-forming pest species that destroys crops and threatens food security in many of the world’s poorest countries. We believe that a better knowledge of the mechanisms of postembryonic development may contribute to the discovery of novel, more selective and sustainable strategies for controlling gregarious locust populations. In this context, identification of molecular target candidates that are capable of significantly reducing the fitness of this devastating swarming pest will be of crucial importance.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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RNAi-Mediated Knockdown of Transcription Factor E93 in Nymphs of the Desert Locust (Schistocerca gregaria) Inhibits Adult Morphogenesis and Results in Supernumerary Juvenile Stages

Gijbels

Marchal

Verdonckt

et al. 2020

IJMS

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“…1 A). In addition, the levels of Scg-Krh1 and Scg-E93 , situated downstream of Met in the MEKRE93 pathway in juvenile insects, were investigated as well (Belles, 2020; Belles and Santos, 2014; Lozano and Belles, 2011; Ureña et al, 2014). The significant reduction in Scg-Krh1 demonstrates that JH signaling was impaired upon silencing Scg -Met (Fig.…”

Section: Discussionmentioning

confidence: 99%

Crucial role of Juvenile Hormone receptor components Methoprene-tolerant and Taiman in sexual maturation of adult male desert locusts (Schistocerca gregaria)

Holtof

Broeck²,

Marchal³

et al. 2020

Preprint

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The desert locust, Schistocerca gregaria, is an infamous migrating insect, generally considered to be one of the most dangerous pest species worldwide. In an area that encompasses one fifth of the Earth’s land surface, desert locust swarms can devastate the agricultural production. Consequently, they pose a serious threat to food security and can have a dramatic socio-economic impact. Currently (in 2020), large parts of East Africa, Southwest and South Asia are experiencing the worst desert locust plague in many decades. Exceptionally high rainfall in different regions has caused the favorable environmental conditions for very successful reproduction and population growth. To better understand the molecular mechanisms responsible for this remarkable reproductive capacity, as well as to fill existing knowledge gaps regarding the regulation of male reproductive physiology, we decided to investigate the role of the methoprene-tolerant (Scg-Met) and taiman (Scg-Tai) genes in adult male desert locusts. Methoprene-tolerant and Taiman belong to the basic helix-loop-helix/Per-Arnt-Sim (bHLH/PAS) family of transcription factors and form a complex that is responsible for transducing the Juvenile Hormone (JH) signal. So far, in vivo research has mainly focused on the role of these JH receptor components in post-embryonic development, as well as in the reproductive physiology of adult female insects. In the current study, we show that silencing these components by RNA interference strongly inhibits sexual maturation of gregarious desert locust males, thereby severely disrupting reproduction. This observation is evidenced by the absence of a yellow colored cuticle, the significant reduction in the relative weight of the testes, the inability to show mating behavior, and the drastically reduced phenylacetonitrile (PAN) pheromone levels of the treated males. In addition, we also observed significant reductions of the relative weight, as well as the relative protein content, of the male accessory glands in Scg-Met knockdown locusts. Interestingly, in these animals the size of the corpora allata (CA), the endocrine glands where JH is synthesized, was significantly increased, and a significant rise was observed in the relative transcript levels of JH acid methyltransferase (JHAMT), a rate-limiting enzyme in the JH biosynthesis pathway. Moreover, other endocrine pathways also appeared to be affected by the knockdown, as evidenced by significant changes in the levels of the transcripts coding for the insulin-related peptide and for two neuroparsins in the fat body. Our results demonstrate that JH signaling pathway components play a crucial role in male reproductive physiology. Since they are crucial for a successful reproduction, they may hold great potential as candidate targets for the design of novel strategies for locust population management.Significance statementDesert locusts can form devastating swarms that threaten the livelihood in many of the world’s poorest countries, as demonstrated by the plagues in East Africa, Southwest and South Asia that are currently covered in the news worldwide. Control of this migratory pest mainly relies on the large-scale use of neurotoxic insecticides, also affecting non-target organisms in their already fragile habitats. Therefore, the identification of novel molecular targets for the design of more sustainable and more selective pest management techniques remains of crucial importance. Potential candidate targets in this respect are pathway components that transduce signals of typical insect hormones, such as ecdysteroids and juvenile hormones. By focusing in our current study on the JH receptor components, we showed that the reproductive capacities of desert locust males can be severely inhibited in an early stage, resulting in individuals that display no mating behavior, do not produce an important pheromone and do not show the characteristic yellow color of sexually mature gregarious males. Specifically targeting molecular components of the JH signaling pathway in future, more biorational control strategies could therefore be a very successful way by which expansion of these devastating plagues might be prevented.

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“…The molecular mechanism that regulates insect metamorphosis is condensed in the MEKRE93 pathway (Belles and Santos, 2014), through which juvenile hormone (JH) bound to its receptor Methoprene tolerant (Met), and induces the expression of Krüppel homolog 1 (Kr-h1); this, in turn, represses the expression of E93. The players most directly involved in regulating metamorphosis are Kr-h1, the transducer of the antimetamorphic signal of JH, and E93, the master trigger of metamorphosis (see (Belles, 2019a)). E93 was originally discovered as an ecdysone-induced late prepupal specific gene, during research into the histolysis of the salivary glands in Drosophila melanogaster metamorphosis, a process in which E93 plays a key role (Baehrecke and Thummel, 1995; Lee et al, 2000; Woodard et al, 1994).…”

Section: Introductionmentioning

confidence: 99%

E93-depleted adult insects preserve the prothoracic gland and molt again

Kamsoi

Bellés

2020

Preprint

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6 7 8 9 Summary statement 1 0The prothoracic gland disintegrates after insect metamorphosis. It was believed that the 1 1 factor FTZ-F1 determines this disintegration. This work reveals that FTZ-F1 action is 1 2 mediated by the factor E93. 1 3 1 4 2 ABSTRACT 1 5 Insect metamorphosis originated around the middle Devonian, associated with the 1 6 innovation of the final molt; this occurs after the histolysis of the prothoracic gland (PG; 1 7which produces the molting hormone) in the first days of adulthood. We previously 1 8 hypothesized that transcription factor E93 was crucial in the emergence of 1 9 metamorphosis, since it triggers metamorphosis in extant insects. This work on the 2 0 cockroach Blattella germanica reveals that E93 also plays a crucial role in the histolysis 2 1 of PG, which fits the above hypothesis. Previous studies have shown that the 2 2 transcription factor FTZ-F1 is essential for PG histolysis. We have found that FTZ-F1 2 3 depletion, towards the end of the final nymphal instar, downregulates the expression of 2 4 E93, while E93-depleted nymphs molt to adults that retain a functional PG. 2 5

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Krüppel homolog 1 and E93: The doorkeeper and the key to insect metamorphosis

Cited by 50 publications

References 49 publications

RNAi-Mediated Knockdown of Transcription Factor E93 in Nymphs of the Desert Locust (Schistocerca gregaria) Inhibits Adult Morphogenesis and Results in Supernumerary Juvenile Stages

RNAi-Mediated Knockdown of Transcription Factor E93 in Nymphs of the Desert Locust (Schistocerca gregaria) Inhibits Adult Morphogenesis and Results in Supernumerary Juvenile Stages

Crucial role of Juvenile Hormone receptor components Methoprene-tolerant and Taiman in sexual maturation of adult male desert locusts (Schistocerca gregaria)

E93-depleted adult insects preserve the prothoracic gland and molt again

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