Hormonal pleiotropy and the juvenile hormone regulation ofDrosophila development and life history

Flatt, Thomas; Tu, Meng‐Ping; Tatar, Marc

doi:10.1002/bies.20290

Cited by 446 publications

(463 citation statements)

References 105 publications

(359 reference statements)

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“…These studies support the hypothesis that the evolution of allocation patterns ultimately results from the evolution of key endocrine pathways [57][58][59], potentially providing a simple theme in a complex web of traits at various levels. Thus, while there is no denying acquisition and allocation of resources are highly complex processes, it is clear that hormone pathways serve as major mediators in many cases.…”

Section: (I) Large Effect Mutations Support the Idea That Major Signasupporting

confidence: 75%

How to get the most bang for your buck: the evolution and physiology of nutrition-dependent resource allocation strategies

2017

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All organisms use resources to grow, survive and reproduce. The supply of these resources varies widely across landscapes and time, imposing ultimate constraints on the maximal trait values for allocation-related traits. In this review, we address three key questions fundamental to our understanding of the evolution of allocation strategies and their underlying mechanisms. First, we ask: how diverse are flexible resource allocation strategies among different organisms? We find there are many, varied, examples of flexible strategies that depend on nutrition. However, this diversity is often ignored in some of the best-known cases of resource allocation shifts, such as the commonly observed pattern of lifespan extension under nutrient limitation. A greater appreciation of the wide variety of flexible allocation strategies leads directly to our second major question: what conditions select for different plastic allocation strategies? Here, we highlight the need for additional models that explicitly consider the evolution of phenotypically plastic allocation strategies and empirical tests of the predictions of those models in natural populations. Finally, we consider the question: what are the underlying mechanisms determining resource allocation strategies? Although evolutionary biologists assume differential allocation of resources is a major factor limiting trait evolution, few proximate mechanisms are known that specifically support the model. We argue that an integrated framework can reconcile evolutionary models with proximate mechanisms that appear at first glance to be in conflict with these models. Overall, we encourage future studies to: (i) mimic ecological conditions in which those patterns evolve, and (ii) take advantage of the 'omic' opportunities to produce multi-level data and analytical models that effectively integrate across physiological and evolutionary theory.

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Section: (I) Large Effect Mutations Support the Idea That Major Signasupporting

confidence: 75%

How to get the most bang for your buck: the evolution and physiology of nutrition-dependent resource allocation strategies

2017

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“…We suggest that MET is capable of recruiting different DNA-binding bHLH-PAS partners in a context of various sex-, stage-, tissue-, cell-, and gene-specific conditions. JH is an insectspecific hormone responsible for a plethora of functions and processes (25). The ability of the JH receptor MET to heterodimerize with different partners is likely a key to the pleiotropic action of its ligand.…”

Section: Discussionmentioning

confidence: 99%

bHLH-PAS heterodimer of methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone-induced mosquito genes

Shin

Zou

Saha

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

117

108

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Juvenile hormone (JH) governs a great diversity of processes in insect development and reproduction. It plays a critical role in controlling the gonadotrophic cycles of female mosquitoes by preparing tissues for blood digestion and egg development. Here, we show that in female Aedes aegypti mosquitoes JH III control of gene expression is mediated by a heterodimer of two bHLH-PAS proteins-the JH receptor methoprene-tolerant (MET) and Cycle (CYC, AAEL002049). We identified Aedes CYC as a MET-interacting protein using yeast two-hybrid screening. Binding of CYC and MET required the presence of JH III. In newly eclosed female mosquitoes, the expression of two JH-responsive genes, Kr-h1 and Hairy, was dependent on both the ratio of light to dark periods and JH III. Their expression was compromised by in vivo RNA interference (RNAi) depletions of CYC, MET, and the steroid receptor coactivator SRC/FISC. Moreover, JH III was not effective in induction of Krh1 and Hairy gene expression in vitro in fat bodies of female mosquitoes with RNAi-depleted CYC, MET or SRC/FISC. A sequence containing an E-box-like motif from the Aedes Kr-h1 gene promoter specifically interacted with a protein complex, which included MET and CYC from the female mosquito fat body nuclear extract. These results indicate that a MET/CYC heterodimer mediates JH III activation of Kr-h1 and Hairy genes in the context of light-dependent circadian regulation in female mosquitoes during posteclosion development. This study provides an important insight into the understanding of the molecular basis of JH action.hormone receptor | insect hormone | transcriptional control M osquitoes serve as vectors of harmful human diseases because blood feeding is required for their egg development; disease pathogens use hematophagous female mosquitoes for obligatory stages of their life cycles. An insect-specific sesquiterpenoid juvenile hormone III (JH III) is essential for a newly eclosed female mosquito to reach a competence stage for blood feeding and egg maturation (1, 2). Although several aspects of the JH III-dependent development have been characterized (3-6), our understanding of molecular mechanisms underlying JH regulation of female mosquito posteclosion development is limited.Methoprene-tolerant (MET), which is a basic helix-loop-helix (bHLH)-Per-Arnt-Sim (PAS) protein, was discovered in Drosophila melanogaster (7), and its role in mediating a JH response has been established (8). MET binds to JH with a high affinity, suggesting that it is the JH receptor (9, 10). As a bHLH protein, MET requires either a homo-or heterodimer partner for its activity (11). Studies in Aedes aegypti, the beetle Tribolium castaneum, and the silkworm Bombyx mori have shown a bHLH-PAS domain-containing steroid receptor coactivator (SRC/FISC/ Taiman) to interact with MET (10,[12][13][14]. Whether, an additional bHLH transcription factor with DNA-binding properties is required as a Met partner remains to be established.Using yeast two-hybrid (Y2H) screening, we identified an Aedes ortholo...

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“…They are important regulators in a wide variety of developmental and physiological events in insects, including development, reproduction, caste determination, behavior, diapauses, polyphenisms, and longevity (2)(3)(4).…”

mentioning

confidence: 99%

Juvenile hormone-activated phospholipase C pathway enhances transcriptional activation by the methoprene-tolerant protein

Liu

Peng

Zhu

2015

Proc. Natl. Acad. Sci. U.S.A.

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Juvenile hormone (JH) is a key regulator of a wide diversity of developmental and physiological events in insects. Although the intracellular JH receptor methoprene-tolerant protein (MET) functions in the nucleus as a transcriptional activator for specific JHregulated genes, some JH responses are mediated by signaling pathways that are initiated by proteins associated with plasma membrane. It is unknown whether the JH-regulated gene expression depends on the membrane-mediated signal transduction. In Aedes aegypti mosquitoes, we found that JH activated the phospholipase C (PLC) pathway and quickly increased the levels of inositol 1,4,5-trisphosphate, diacylglycerol, and intracellular calcium, leading to activation and autophosphorylation of calcium/calmodulin-dependent protein kinase II (CaMKII). When abdomens from newly emerged mosquitoes were cultured in vitro, the JH-activated gene expression was repressed substantially if specific inhibitors of PLC or CaMKII were added to the medium together with JH. In newly emerged female mosquitoes, RNAi-mediated depletion of PLC or CaMKII considerably reduced the expression of JH-responsive genes, including the Krüppel homolog 1 gene (AaKr-h1) and the early trypsin gene (AaET). JH-induced loading of MET to the promoters of AaKr-h1 and AaET was weakened drastically when either PLC or CaMKII was inactivated in the cultured tissues. Therefore, the results suggest that the membraneinitiated signaling pathway modifies the DNA-binding activity of MET via phosphorylation and thus facilitates the genomic responses to JH. In summary, this study reveals an interplay of genomic and nongenomic signaling mechanisms of JH.insect hormone | development | phospholipase C | protein kinase | transcription J uvenile hormones (JH) are a group of acyclic sesquiterpenoids produced in insects by the corpora allata, a pair of endocrine glands connected to the brain (1). They are important regulators in a wide variety of developmental and physiological events in insects, including development, reproduction, caste determination, behavior, diapauses, polyphenisms, and longevity (2-4).Many effects of JH are mediated by the methoprene-tolerant (MET) protein, an intracellular JH receptor (5). MET contains a basic helix-loop-helix (bHLH) DNA-recognition motif near the N terminus, followed by two tandem Per-ARNT-Sim (PAS) domains, PAS-A and PAS-B (6). In vitro studies have demonstrated that JH-III binds MET with relatively high affinity and have identified a putative JH-binding pocket in the PAS-B domain of MET (7,8). In the presence of JH, MET forms a heterodimer with a p160 steroid receptor coactivator (SRC), which also contains the bHLH-PAS domain (7, 9). The orthologs of SRC are called "Taiman" (TAI) in Drosophila melanogaster and "Ftz-F1-interacting steroid receptor coactivator" (FISC) in the yellow fever mosquito Aedes aegypti (10, 11). For simplicity, we will use a single name, Taiman, to describe all its orthologs in insects. TAI acts as the DNA-binding partner of MET; the MET-TAI complex recogni...

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Hormonal pleiotropy and the juvenile hormone regulation ofDrosophila development and life history

Cited by 446 publications

References 105 publications

How to get the most bang for your buck: the evolution and physiology of nutrition-dependent resource allocation strategies

How to get the most bang for your buck: the evolution and physiology of nutrition-dependent resource allocation strategies

bHLH-PAS heterodimer of methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone-induced mosquito genes

Juvenile hormone-activated phospholipase C pathway enhances transcriptional activation by the methoprene-tolerant protein

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