Neuromodulation of Behavioral Specialization: Tachykinin Signaling Inhibits Task-specific Behavioral Responsiveness in Honeybee Workers

AbstractBehavioral specialization is key to the success of social insects and often compartmentalized among colony members leading to division of labor. Response thresholds to task-specific stimuli proximally regulate behavioral specialization but their neurobiological regulation is not understood. Here, we show that response thresholds to task-relevant stimuli correspond to the specialization of three behavioral phenotypes of honeybee workers. Quantitative neuropeptidome comparisons suggest two tachykinin-related peptides (TRP2 and TRP3) as candidates for the modification of these response thresholds. Based on our characterization of their receptor binding and downstream signaling, we then confirm the functional role of tachykinins: TRP2 injection and RNAi cause consistent, opposite effects on responsiveness to task-specific stimuli of each behaviorally specialized phenotype but not to stimuli that are unrelated to their tasks. Thus, our study demonstrates that TRP-signaling regulates the degree of task-specific responsiveness of specialized honeybee workers and may control the context-specificity of behavior in animals more generally.

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Tachykinin signaling inhibits task-specific behavioral responsiveness in honeybee workers

eLife ◽

10.7554/elife.64830 ◽

2021 ◽

Vol 10 ◽

Author(s):

Bin Han ◽

Qiaohong Wei ◽

Fan Wu ◽

Han Hu ◽

Chuan Ma ◽

...

Keyword(s):

Apis Mellifera ◽

Functional Role ◽

Apis Cerana ◽

Context Specificity ◽

Downstream Signaling ◽

Behavioral Specialization ◽

Behavioral Responsiveness ◽

Response Thresholds

Behavioral specialization is key to the success of social insects and leads to division of labor among colony members. Response thresholds to task-specific stimuli are thought to proximally regulate behavioral specialization but their neurobiological regulation is complex and not well-understood. Here, we show that response thresholds to task-relevant stimuli correspond to the specialization of three behavioral phenotypes of honeybee workers in the well-studied and important Apis mellifera and Apis cerana. Quantitative neuropeptidome comparisons suggest two tachykinin-related peptides (TRP2 and TRP3) as candidates for the modification of these response thresholds. Based on our characterization of their receptor binding and downstream signaling, we confirm a functional role of tachykinin signaling in regulating specific responsiveness of honeybee workers: TRP2 injection and RNAi-mediated downregulation cause consistent, opposite effects on responsiveness to task-specific stimuli of each behaviorally specialized phenotype but not to stimuli that are unrelated to their tasks. Thus, our study demonstrates that TRP-signaling regulates the degree of task-specific responsiveness of specialized honeybee workers and may control the context-specificity of behavior in animals more generally.

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Structural and Thermodynamic Characterization of theEscherichia coliRelBE Toxin−Antitoxin System: Indication for a Functional Role of Differential Stability†

Biochemistry ◽

10.1021/bi701037e ◽

2007 ◽

Vol 46 (43) ◽

pp. 12152-12163 ◽

Cited By ~ 26

Author(s):

Izhack Cherny ◽

Martin Overgaard ◽

Jonas Borch ◽

Yaron Bram ◽

Kenn Gerdes ◽

...

Keyword(s):

Functional Role ◽

Thermodynamic Characterization ◽

Differential Stability

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Phosphatidylinositol 3-Kinase and Prostaglandylinositol Cyclic Phosphate (Cyclic PIP), a Mediator of Insulin Action, in the Signal Transduction of Insulin

Biological Chemistry ◽

10.1515/bc.2000.140 ◽

2000 ◽

Vol 381 (11) ◽

pp. 1139-1141 ◽

Cited By ~ 1

Author(s):

A. Gypakis ◽

H.K. Wasner

Keyword(s):

Insulin Receptor ◽

Glucose Transport ◽

Functional Role ◽

Specific Inhibitor ◽

Insulin Receptor Substrate ◽

Phosphatidylinositol 3 Kinase ◽

Downstream Signaling ◽

Cyclic Phosphate ◽

Phosphatidylinositol 3

Abstract It has been suggested that downstream signaling from the insulin receptor to the level of the protein kinases and protein phosphatases is accomplished by prostaglandylinositol cyclic phosphate (cyclic PIP), a proposed second messenger of insulin. However, evidence points also to both phosphatidylinositol 3-kinase, which binds to the tyrosine phosphorylated insulin receptor substrate-1, and the Ras complex in insulin's downstream signaling. We have examined whether a correlation exists between these various observations. It was found that wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase, prevented insulin-induced, as well as cyclic PIP-induced activation of glucose transport, indicating that PI 3-kinase action on glucose transport involves downstream signaling of both insulin and cyclic PIP. Wortmannin has no effect on cyclic PIP synthase activity nor on the substrate production for cyclic PIP synthesis either, indicating that the functional role of PI 3-kinase is exclusively downstream of cyclic PIP.

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Structural insights into the functional role of the Hcn sub-domain of the receptor-binding domain of the botulinum neurotoxin mosaic serotype C/D

Biochimie ◽

10.1016/j.biochi.2013.03.006 ◽

2013 ◽

Vol 95 (7) ◽

pp. 1379-1385 ◽

Cited By ~ 7

Author(s):

Yanfeng Zhang ◽

Anna S. Gardberg ◽

Thomas E. Edwards ◽

Banumathi Sankaran ◽

Howard Robinson ◽

...

Keyword(s):

Receptor Binding ◽

Functional Role ◽

Botulinum Neurotoxin ◽

Binding Domain ◽

Receptor Binding Domain ◽

Structural Insights

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Characterization of bacterial communities of rhizosphere and rhizoplane of Early Zhukovsky potato

E3S Web of Conferences ◽

10.1051/e3sconf/202022202050 ◽

2020 ◽

Vol 222 ◽

pp. 02050

Author(s):

Marat Lutfulin ◽

Darya Zaripova ◽

Oksana Moiseeva ◽

Semen Vologin ◽

Ayslu Mardanova

Keyword(s):

Bacterial Communities ◽

Functional Role ◽

Agricultural Crop ◽

Potato Root ◽

Bacterial Microbiota ◽

16S R Rna ◽

Significant Difference ◽

Dominant Bacteria

Identification of patterns of formation of bacterial communities of the rhizosphere and rhizoplane of potato (Solanum tuberosum L.), the most important agricultural crop, is necessary for the introduction and maintenance of sustainable organic farming. The purpose of this work was the study of the biodiversity of the bacterial microbiota of the rhizosphere and rhizoplane of Early Zhukovsky potato, cultivated on gray forest soils. Comparative analysis based on sequencing of the 16S R RNA gene showed a significant difference in the representation of different groups of bacteria in these potato root compartments. Thus, the proportions of the dominant bacteria in the rhizosphere and rhizoplane of the Proteobacteria phylum reach 47.66% ± 7.22 % and 86.35 % ± 0.53%, respectively (P < 0.05). In contrast, the representation of phylum Bacteroidetes and Firmicutes in the rhizosphere is significantly higher and reaches 41.45 % ± 10.42% and 6.49 % ± 3.23%, respectively, compared to the rhizoplane (7.84 % ± 1.24 % and 0.43 % ± 0.48 %, (P < 0.05). At the same time, Actinobacteria phylum bacteria are present in both compartments in approximately equal amounts (4.40 % ± 1.81% in the rhizosphere and 5.37 % ± 1.42% in the rhizoplane). Thus, it was found that potato forms different bacterial communities in the rhizosphere and rhizoplane in quantitative proportions, which is probably determined by the functional role of these microorganisms in the plant physiology.

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The Close Linkage between Nutrition and Environment through Biodiversity and Sustainability: Local Foods, Traditional Recipes, and Sustainable Diets

Sustainability ◽

10.3390/su11102876 ◽

2019 ◽

Vol 11 (10) ◽

pp. 2876 ◽

Cited By ~ 3

Author(s):

Alessandra Durazzo

Keyword(s):

Dietary Patterns ◽

Functional Role ◽

Close Correlation ◽

Close Linkage ◽

Local Foods ◽

Special Issue ◽

Sustainable Diets ◽

Potential Benefits

This special issue, “The Close Linkage between Nutrition and Environment through Biodiversity and Sustainability: Local Foods, Traditional Recipes, and Sustainable Diets” is focused on the close correlation between the potential benefits and “functional role” of a food and the territory, including papers on the characterization of local foods and traditional recipes, on the promotion of traditional dietary patterns and sustainable diets.

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Characterization of the functional role of asp 141, asp 194, and asp464 residues in the Mn2+-l-malate binding of pigeon liver malic enzyme

Protein Science ◽

10.1110/ps.9.2.242 ◽

2008 ◽

Vol 9 (2) ◽

pp. 242-251 ◽

Cited By ~ 2

Author(s):

Wei-Yuan Chou ◽

Hwei-Ping Chang ◽

Chien-Hsiun Huang ◽

Cheng-Chin Kuo ◽

Gu-Gang Chang ◽

...

Keyword(s):

Malic Enzyme ◽

Functional Role ◽

Pigeon Liver

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Structural and functional analysis of two di-domain aromatase/cyclases from type II polyketide synthases

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1512976112 ◽

2015 ◽

Vol 112 (50) ◽

pp. E6844-E6851 ◽

Cited By ~ 14

Author(s):

Grace Caldara-Festin ◽

David R. Jackson ◽

Jesus F. Barajas ◽

Timothy R. Valentic ◽

Avinash B. Patel ◽

...

Keyword(s):

Functional Analysis ◽

Functional Role ◽

Functional Characterization ◽

Polyketide Synthases ◽

Type Ii ◽

Aromatic Polyketides ◽

Linear Poly ◽

Bacterial Type

Aromatic polyketides make up a large class of natural products with diverse bioactivity. During biosynthesis, linear poly-β-ketone intermediates are regiospecifically cyclized, yielding molecules with defined cyclization patterns that are crucial for polyketide bioactivity. The aromatase/cyclases (ARO/CYCs) are responsible for regiospecific cyclization of bacterial polyketides. The two most common cyclization patterns are C7–C12 and C9–C14 cyclizations. We have previously characterized three monodomain ARO/CYCs: ZhuI, TcmN, and WhiE. The last remaining uncharacterized class of ARO/CYCs is the di-domain ARO/CYCs, which catalyze C7–C12 cyclization and/or aromatization. Di-domain ARO/CYCs can further be separated into two subclasses: “nonreducing” ARO/CYCs, which act on nonreduced poly-β-ketones, and “reducing” ARO/CYCs, which act on cyclized C9 reduced poly-β-ketones. For years, the functional role of each domain in cyclization and aromatization for di-domain ARO/CYCs has remained a mystery. Here we present what is to our knowledge the first structural and functional analysis, along with an in-depth comparison, of the nonreducing (StfQ) and reducing (BexL) di-domain ARO/CYCs. This work completes the structural and functional characterization of mono- and di-domain ARO/CYCs in bacterial type II polyketide synthases and lays the groundwork for engineered biosynthesis of new bioactive polyketides.

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Characterization of glutathione S-transferases from the pine wood nematode, Bursaphelenchus xylophilus

Nematology ◽

10.1163/15685411-00002985 ◽

2016 ◽

Vol 18 (6) ◽

pp. 697-709 ◽

Cited By ~ 8

Author(s):

Margarida Espada ◽

John T. Jones ◽

Manuel Mota

Keyword(s):

Post Infection ◽

Functional Role ◽

Gland Cell ◽

Expression Profiles ◽

Bursaphelenchus Xylophilus ◽

Pine Wood Nematode ◽

Glutathione S Transferases ◽

Pharyngeal Gland

We have previously identified two secreted glutathione S-transferases (GST) expressed in the pharyngeal gland cell of Bursaphelenchus xylophilus, which are upregulated post infection of the host. This study examines the functional role of GSTs in B. xylophilus biology. We analysed the expression profiles of all predicted GSTs in the genome and the results showed that they belong to kappa and cytosolic subfamilies and the majority are upregulated post infection of the host. A small percentage is potentially secreted and none is downregulated post infection of the host. One secreted protein was confirmed as a functional GST and is within a cluster that showed the highest expression fold change in infection. This enzyme has a protective activity that may involve host defences, namely in the presence of terpenoid compounds and peroxide products. These results suggest that GSTs secreted into the host participate in the detoxification of host-derived defence compounds and enable successful parasitism.

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