Hormonal control of growth in the wing imaginal disks of <i>Junonia coenia</i>: the relative contributions of insulin and ecdysone

Nijhout, H. Frederik; Laub, Emily C.; Grunert, Laura W.

doi:10.1242/dev.160101

Cited by 19 publications

(13 citation statements)

References 43 publications

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“…4A ) to identify genes that regulate the growth of lateral tergal regions in T2 and T3. The steroid hormone 20-hydroxyecdysone (20E) promotes wing growth by increasing both cell number and cell size in lepidopteran insects (Nijhout & Grunert, 2002; Nijhout et al ., 2018). We thus examined the expression level of two ecdysone responsive genes, E74 and E75 , as proxies for hemolymph ecdysone titer to determine the timing of tissue sampling for RNA-seq analysis (Ashburner & Richards, 1976; Li et al ., 2003).…”

Section: Resultsmentioning

confidence: 99%

A wing growth organizer in a hemimetabolous insect suggests wing origin

Ohde

Mito

Niimi

2021

Preprint

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The origin and evolution of insect wings remain enigmatic after a century-long discussion. Molecular dissection of wing development in hemimetabolous insects, in which the first functional wings evolved, is key to understand genetic changes required for wing evolution. We investigated Drosophila wing marker genes in the cricket, Gryllus bimaculatus, and found apterous and vestigial show critical functions in nymphal tergal identity and margin formation, respectively. We further demonstrate that margin cells in the lateral-anterior tergal region constitute a growth organizer of wing blades. Transcriptome and RNAi analyses unveiled that Wnt, Fat-Dachsous, and Hippo pathways are involved in disproportional growth of Gryllus wings. Our data collectively support the idea that tergal margin cells of a wingless ancestor gave rise to the body wall extension required for evolution of the first powered flight.

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Section: Resultsmentioning

confidence: 99%

A wing growth organizer in a hemimetabolous insect suggests wing origin

Ohde

Mito

Niimi

2021

Preprint

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“…The decay in JH titer is an essential condition for the release of ecdysone by the prothoracic gland and wing imaginal discs growth. Components of the insulin signaling pathway are involved in this process [ 55 , 56 ]. Insulin prevents the suppressive effect of JH on the expression of broad (a molecular marker of pupal commitment) and wing discs differentiation [ 12 ].…”

Section: Discussionmentioning

confidence: 99%

Transcriptome dynamics during metamorphosis of imaginal discs into wings and thoracic dorsum in Apis mellifera castes

et al. 2021

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Background Much of the complex anatomy of a holometabolous insect is built from disc-shaped epithelial structures found inside the larva, i.e., the imaginal discs, which undergo a rapid differentiation during metamorphosis. Imaginal discs-derived structures, like wings, are built through the action of genes under precise regulation. Results We analyzed 30 honeybee transcriptomes in the search for the gene expression needed for wings and thoracic dorsum construction from the larval wing discs primordia. Analyses were carried out before, during, and after the metamorphic molt and using worker and queen castes. Our RNA-seq libraries revealed 13,202 genes, representing 86.2% of the honeybee annotated genes. Gene Ontology analysis revealed functional terms that were caste-specific or shared by workers and queens. Genes expressed in wing discs and descendant structures showed differential expression profiles dynamics in premetamorphic, metamorphic and postmetamorphic developmental phases, and also between castes. At the metamorphic molt, when ecdysteroids peak, the wing buds of workers showed maximal gene upregulation comparatively to queens, thus underscoring differences in gene expression between castes at the height of the larval-pupal transition. Analysis of small RNA libraries of wing buds allowed us to build miRNA-mRNA interaction networks to predict the regulation of genes expressed during wing discs development. Conclusion Together, these data reveal gene expression dynamics leading to wings and thoracic dorsum formation from the wing discs, besides highlighting caste-specific differences during wing discs metamorphosis.

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“…Independent regulation of growth and pattern is likely to arise, at least in part, from the fact that growth in the wing disc relies not only on ecdysone, but also on insulin D. melanogaster, Manduca sexta, and J. coenia [7,[74][75][76][77][78]. In fact, early in the third instar the growth of wing discs and ovaries relies more on insulin signalling than ecdysone signalling in D. melanogaster [60,63].…”

Section: Discussionmentioning

confidence: 99%

Ecdysone coordinates plastic growth with robust pattern in the developing wing

Oliveira

Kaburagi

et al. 2020

Preprint

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Animals develop in unpredictable, changing environments. To do this, they adjust their development according to environmental conditions to generate plastic variation in traits, while also buffering against environmental change to produce robust phenotypes. However, how organ development is coordinated to accommodate both plastic and robust developmental responses is poorly understood. Here, we propose that the steroid hormone ecdysone coordinates both plasticity in organ size and robustness of organ pattern in the developing wings of the fruit fly Drosophila melanogaster. Ablating the prothoracic glands (PGX), which synthesise and secrete ecdysone, resulted in wing discs that were reduced in size and delayed in the progression of Achaete and Senseless pattern. These effects were rescued by adding ecdysone to the food. Further, while wing growth was driven by both ecdysone and nutrition, ecdysone alone induced the progression of wing patterning. To further explore this difference in response, we quantified wing growth and patterning in PGX larvae that were either fed on standard diet or starved of yeast across a range of ecdysone concentrations. Disc growth rates increased in a graded, linear manner with ecdysone concentration in starved larvae. In contrast, Achaete and Senseless patterning rates showed threshold responses regardless of diet. This means that ecdysone confers robustness by turning on patterning once it exceeds threshold concentrations, while inducing graded responses for disc growth, tuning growth to environmental conditions. This potentially represents a generalizable mechanism through which hormones coordinate plastic growth with robust patterning in the face of environmental change.

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Hormonal control of growth in the wing imaginal disks of Junonia coenia: the relative contributions of insulin and ecdysone

Cited by 19 publications

References 43 publications

A wing growth organizer in a hemimetabolous insect suggests wing origin

A wing growth organizer in a hemimetabolous insect suggests wing origin

Transcriptome dynamics during metamorphosis of imaginal discs into wings and thoracic dorsum in Apis mellifera castes

Ecdysone coordinates plastic growth with robust pattern in the developing wing

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