E93 expression and links to the juvenile hormone in hemipteran mealybugs with insights on female neoteny

Vea, Isabelle M.; Tanaka, Sayumi; Tsuji, Tomohiro; Shiotsuki, Takahiro; Jouraku, Akiya; Minakuchi, Chieka

doi:10.1016/j.ibmb.2018.11.008

Cited by 19 publications

(13 citation statements)

References 34 publications

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“…In the neotenic Hemiptera Coccomorpha (Paraneoptera), male postembryonic development includes the quiescent stages of 'prepupa' and 'pupa' that precede the adult. Interestingly, the expression of Kr-h1 decreases in the 'prepupa' phase, while the expression of E93 increases [39,40]. This suggests that in these hemimetabolan species with complex life cycles, the MEKRE93 pathway may operate similarly to the way it does in other hemimetabolan species.…”

Section: E93 and The Mekre93 Pathwaymentioning

confidence: 96%

The innovation of the final moult and the origin of insect metamorphosis

Bellés

2019

Phil. Trans. R. Soc. B

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The three modes of insect postembryonic development are ametaboly, hemimetaboly and holometaboly, the latter being considered the only significant metamorphosis mode. However, the emergence of hemimetaboly, with the genuine innovation of the final moult, represents the origin of insect metamorphosis and a necessary step in the evolution of holometaboly. Hemimetaboly derives from ametaboly and might have appeared as a consequence of wing emergence in Pterygota, in the early Devonian. In extant insects, the final moult is mainly achieved through the degeneration of the prothoracic gland (PG), after the formation of the winged and reproductively competent adult stage. Metamorphosis, including the formation of the mature wings and the degeneration of the PG, is regulated by the MEKRE93 pathway, through which juvenile hormone precludes the adult morphogenesis by repressing the expression of transcription factor E93, which triggers this change. The MEKRE93 pathway appears conserved in extant metamorphosing insects, which suggest that this pathway was operative in the Pterygota last common ancestor. We propose that the final moult, and the consequent hemimetabolan metamorphosis, is a monophyletic innovation and that the role of E93 as a promoter of wing formation and the degeneration of the PG was mechanistically crucial for their emergence. This article is part of the theme issue ‘The evolution of complete metamorphosis’.

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Section: E93 and The Mekre93 Pathwaymentioning

confidence: 96%

The innovation of the final moult and the origin of insect metamorphosis

Bellés

2019

Phil. Trans. R. Soc. B

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“…Typically, these females reproduce asexually for part of the year and only start producing males under times of stress. Expression of E93 is very low in such females, associated with their failure to assume an adult form [6].…”

Section: Reviewmentioning

confidence: 98%

“…As in thrips, in the Japanese mealy bug, Planococcus kraunhiae, broad transcripts appear as the feeding 'larva' molts to a prepupa and then to a pupa [132]. In both thrips [133] and mealy bugs [6], the expression of E93 accompanies the expression of broad as they enter the pupal series, but then E93 carries on alone in making the adult.…”

Section: Reviewmentioning

confidence: 99%

“…Besides Drosophila, this discussion draws on other insect model systems such as Bombyx mori, Manduca sexta, Tribolium castaneum, Oncopeltus fasciatus, Pyrrhocoris apterus and Blattella germanica, for which genomic information and gene suppression techniques can be woven into a rich history of endocrine experimentation. Although these few systems do not begin to cover the amazing range of variation that one sees in the insects, it is heartening that highly derived life history strategies, such as female neoteny in Strepsiptera [4,5] and scale insects [6] or the complete metamorphosis that evolved in parallel in thrips [7], utilize the same molecular switches that regulate more traditional life history patterns. This review explores the developmental changes that accompanied the evolution of the insect larval and pupal stages.…”

Section: Introductionmentioning

confidence: 99%

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The Evolution of Insect Metamorphosis

2019

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The evolution of insect metamorphosis is one of the most important sagas in animal history, transforming small, obscure soil arthropods into a dominant terrestrial group that has profoundly shaped the evolution of terrestrial life. The evolution of flight initiated the trajectory towards metamorphosis, favoring enhanced differences between juvenile and adult stages. The initial step modified postembryonic development, resulting in the nymph-adult differences characteristic of hemimetabolous species. The second step was to complete metamorphosis, holometaboly, and occurred by profoundly altering embryogenesis to produce a larval stage, the nymph becoming the pupa to accommodate the deferred development needed to make the adult. These changing life history patterns were intimately linked to two hormonal systems, the ecdysteroids and the juvenile hormones (JH), which function in both embryonic and postembryonic domains and control the stage-specifying genes Kru¨ppel homolog 1 (Kr-h1), broad and E93. The ecdysteroids induce and direct molting through the ecdysone receptor (EcR), a nuclear hormone receptor with numerous targets including a conserved transcription factor network, the 'Ashburner cascade', which translates features of the ecdysteroid peak into the different phases of the molt. With the evolution of metamorphosis, ecdysteroids acquired a metamorphic function that exploited the repressor capacity of the unliganded EcR, making it a hormonecontrolled gateway for the tissue development preceding metamorphosis. JH directs ecdysteroid action, controlling Kr-h1 expression which in turn regulates the other stage-specifying genes. JH appears in basal insect groups as their embryos shift from growth and patterning to differentiation. As a major portion of embryogenesis was deferred to postembryonic life with the evolution of holometaboly, JH also acquired a potent role in regulating postembryonic growth and development. Details of its involvement in broad expression and E93 suppression have been modified as life cycles became more complex and likely underlie some of the changes seen in the shift from incomplete to complete metamorphosis.

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“…E93 begins to be expressed in the prepupa, but the intervention of Broad expression represses E93 action and directs pupal differentiation. An early propupal expression of E93 is also seen in the neometabolous insects, the thrips (Y. Suzuki, T. Shiotsuki, A. Jouraku, K. Miura, C. Minakuchi 2019, personal communication) and the mealy bug [86].…”

Section: Implications For the Evolution Of The Holometabolamentioning

confidence: 99%

The evolution of insect metamorphosis: a developmental and endocrine view

Truman

Riddiford

2019

Phil. Trans. R. Soc. B

142

116

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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’.

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E93 expression and links to the juvenile hormone in hemipteran mealybugs with insights on female neoteny

Cited by 19 publications

References 34 publications

The innovation of the final moult and the origin of insect metamorphosis

The innovation of the final moult and the origin of insect metamorphosis

The Evolution of Insect Metamorphosis

The evolution of insect metamorphosis: a developmental and endocrine view

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