Hormonal control and target genes of ftz‐f1 expression in the honeybee Apis mellifera: a positive loop linking juvenile hormone, ftz‐f1, and vitellogenin

Mello, Tathyana Rachel Palo; Aleixo, Aline Carolina; Pinheiro, Daniel Guariz; Nunes, Francis Morais Franco; Cristino, Alexandre S.; Bitondi, M. M. G.; Barchuk, Angel Roberto; Simões, Zilá Luz Paulino

doi:10.1111/imb.12541

Cited by 27 publications

(34 citation statements)

References 72 publications

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“…This means that there is the potential for diversified types of signaling and response in the eusocial insect colony, as well as elaboration of the molecular mechanisms underlying the response to stimuli. Functional genomic approaches that simultaneously consider multiple socially-interacting individuals, e.g., based on sequencing a time series of interacting nurse workers and larvae 152 shows that even the most fundamentally important conserved genes have distinctly different expression patterns in eusocial insects as compared to solitary insects, as well as expression variation between related eusocial species and among nestmates 31,[158][159][160] . The convention has been to act as if use of an ortholog constitutes conservation, but already for key cases such as PKG we know the same locus can be associated with a trait (e.g.…”

Section: Predictions For Glandsmentioning

confidence: 99%

Distributed physiology and the molecular basis of social life in eusocial insects

Friedman

Johnson

Linksvayer

2020

Hormones and Behavior

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The traditional focus of physiological and functional genomic research is on molecular processes that play out within a single body. In contrast, when social interactions occur, molecular and behavioral responses in interacting individuals can lead to physiological processes that are distributed across multiple individuals. In eusocial insect colonies, such multi-body processes are tightly integrated, involving social communication mechanisms that regulate the physiology of colony members. As a result, conserved physiological mechanisms, for example related to pheromone detection and neural signaling pathways, are deployed in novel contexts and regulate emergent colony traits during the evolutionary origin and elaboration of social complexity. Here we review conceptual frameworks for organismal and colony physiology, and highlight functional genomic, physiological, and behavioral research exploring how colony-level traits arise from physical and chemical interactions among nestmates. We highlight mechanistic work exploring how colony traits arise from physical and chemical interactions among physiologically-specialized nestmates of 1 various developmental stages. We consider similarities and differences between organismal and colony physiology, and make specific predictions based on a decentralized perspective on the function and evolution of colony traits. Integrated models of colony physiological function will be useful to address fundamental questions related to the evolution and ecology of collective behavior in natural systems. Colony Organization = Social Anatomy + Social PhysiologyEusocial colonial insects, such as ants, termites, and honey bees, thrive across almost all terrestrial ecosystems 1,2 . The ecological success of these species rests in their use of colony traits, such as nest architecture 3,4 and collective foraging behavior 5-7 , which are functionally absent in solitary insects yet keenly developed in eusocial taxa. In the eusocial insects, division of labor (DOL) describes how nestmates vary in their form and function. DOL formalizes the extent of specialization among nestmates in the performance of tasks, usually with a physiological or morphological basis or arising from nestmate age (temporal polyethism) and experience [8][9][10][11] . We build off of the conceptual framework of Johnson & Linksvayer 12 that considers eusocial colony organization from the perspective of social anatomy & social physiology : Social anatomy is the notion that colonies are composed of specialized parts with limited roles, like the organs of an individual animal. Specialized colony anatomy allows for greater productivity and efficiency for the completion of many tasks.Physiological specialization exists at multiple levels within the colony. Queen-worker specialization allows for an increased reproductive output of queens alongside increased work output from workers, from the same diploid female genome 13 .Subspecialization among workers can manifest as permanent variation in body morphology 14 , temporal polyet...

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Section: Predictions For Glandsmentioning

confidence: 99%

Distributed physiology and the molecular basis of social life in eusocial insects

Friedman

Johnson

Linksvayer

2020

Hormones and Behavior

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“…For example, Liu et al [45] found that knockdown of FTZ-F1 in final-instar larvae caused significant impairment of pupation in L. decemlineata [45]. In A. mellifera, cuticle pigmentation and wing formation during developmental processes were severely impaired by downregulation of FTZ-F1 [25]. Recently, Li et al [27] reported that FTZ-F1 mediates the expression of CYP6BG1, conferring resistance to chlorantraniliprole in P. xylostella.…”

Section: Discussionmentioning

confidence: 99%

“…[ 45 ] found that knockdown of FTZ-F1 in final-instar larvae caused significant impairment of pupation in L. decemlineata [ 45 ]. In A. mellifera , cuticle pigmentation and wing formation during developmental processes were severely impaired by downregulation of FTZ-F1 [ 25 ]. Recently, Li et al .…”

Section: Discussionmentioning

confidence: 99%

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Transcription factor FTZ-F1 regulates mosquito cuticular protein CPLCG5 conferring resistance to pyrethroids in Culex pipiens pallens

Yang

Sun

et al. 2020

Parasites Vectors

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Background Culex pipiens pallens poses a serious threat to human health because of its widespread distribution, high carrier capacity for several arboviruses, frequent human-biting, and growth in urban environments. Pyrethroid insecticides have been mainly used to control adult Cx. pipiens pallens during outbreaks of mosquito-borne diseases. Unfortunately, mosquitoes have developed resistance, rendering the insecticides ineffective. Cuticular resistance is the primary mechanism of pyrethroid resistance. Previously, we revealed that cuticular protein of low complexity CPLCG5 is a major cuticular protein associated with deltamethrin resistance in Cx. pipiens pallens, which is enriched in the cuticle of mosquitoes’ legs and participates in pyrethroid resistance by forming a rigid matrix. However, the regulatory mechanisms of its transcription remain unknown. Results First, qRT-PCR analysis revealed that the expression of FTZ-F1 (encoding Fushi tarazu-Factor 1) was ~ 1.8-fold higher in the deltamethrin-resistant (DR) than deltamethrin-susceptible (DS) strains at 24 h post-eclosion (PE) and ~ 2.2-fold higher in the DR strain than in the DS strain at 48 h PE. CPLCG5 and FTZ-F1 were co-expressed in the legs, indicating that they might play an essential role in the legs. Dual luciferase reporter assays and EMSA (electrophoretic mobility shift experiments) revealed that FTZ-F1 regulates the transcription of CPLCG5 by binding to the FTZ-F1 response element (− 870/− 864). Lastly, knockdown of FTZ-F1 not only affected CPLCG5 expression but also altered the cuticle thickness and structure of the legs, increasing the susceptibility of the mosquitoes to deltamethrin in vivo. Conclusions The results revealed that FTZ-F1 regulates the expression of CPLCG5 by binding to the CPLCG5 promoter region, altering cuticle thickness and structure, and increasing the susceptibility of mosquitoes to deltamethrin in vivo. This study revealed part of the mechanism of cuticular resistance, providing a deeper understanding of insecticide resistance.

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“…Broad and Ftz-F1 mediate the transcription-dependent effects of JH on cell physiology during development in other insect species (Bonneton and Laudet, 2012) and (at least in the case of Ftz-F1) in pharate adult bees (Mello et al, 2018). JH plays a strong role in regulating honey bee behavioral maturation (Robinson, 1992).…”

Section: Jh Analog Administrationmentioning

confidence: 99%

Division of labor in honey bees is associated with transcriptional regulatory plasticity in the brain

Hamilton

Traniello

Ray

et al. 2019

Journal of Experimental Biology

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Studies in evolutionary and developmental biology show that relationships between transcription factors (TFs) and their target genes can be altered to result in novel regulatory relationships that generate phenotypic plasticity. We hypothesized that contextdependent shifts in the nervous system associated with behavior may also be linked to changes in TF-target relationships over physiological time scales. We tested this hypothesis using honey bee (Apis mellifera) division of labor as a model system by performing bioinformatic analyses of previously published brain transcriptomic profiles together with new RNAi and behavioral experiments. The bioinformatic analyses identified five TFs that exhibited strong signatures of regulatory plasticity as a function of division of labor. RNAi targeting of one of these TFs (broad complex) and a related TF that did not exhibit plasticity (fushi tarazu transcription factor 1) was administered in conjunction with automated analyses of foraging behavior in the field, laboratory assays of aggression and brood care behavior, and endocrine treatments. The results showed that changes in the regulatory relationships of these TFs were associated with behavioral state, social context and endocrine state. These findings provide the first empirical evidence that TF-target relationships in the brain are altered in conjunction with behavior and social context. They also suggest that one mechanism for this plasticity involves pleiotropic TFs high up in regulatory hierarchies producing behavior-specific transcriptional responses by activating different downstream TFs to induce discrete context-dependent transcriptional cascades. These findings provide new insights into the dynamic nature of the transcriptional regulatory architecture underlying behavior in the brain.

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Hormonal control and target genes of ftz‐f1 expression in the honeybee Apis mellifera: a positive loop linking juvenile hormone, ftz‐f1, and vitellogenin

Cited by 27 publications

References 72 publications

Distributed physiology and the molecular basis of social life in eusocial insects

Distributed physiology and the molecular basis of social life in eusocial insects

Transcription factor FTZ-F1 regulates mosquito cuticular protein CPLCG5 conferring resistance to pyrethroids in Culex pipiens pallens

Division of labor in honey bees is associated with transcriptional regulatory plasticity in the brain

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