Gravity perception: molecular, cellular and adaptive behavior

Project Information

SENS_GRAV

Grant agreement ID: 101066134

DOI

10.3030/101066134

Project closed

EC signature date 25 May 2022

Start date 1 July 2022

End date 30 June 2024

Funded under

• Marie Skłodowska-Curie Actions (MSCA)

Total cost

No data

EU contribution

€ 195 914,88

Coordinated by

INSTITUT NATIONAL DE RECHERCHE POUR L'AGRICULTURE, L'ALIMENTATION ET L'ENVIRONNEMENT
France

Periodic Reporting for period 1 - SENS_GRAV (Gravity perception: molecular, cellular and adaptive behavior)

Reporting period: 2022-07-01 to 2024-06-30

Summary of the context and overall objectives of the project

The context of this project lies in the fundamental understanding of how living organisms perceive and adapt to gravitational forces, a question that has gained urgency with advancements in space exploration and our ability to expose biological systems to varying gravity levels. Gravity influences numerous biological functions, including circulatory systems, development, and behavior, yet the molecular, neural, and physiological bases of this sensory modality remain largely unknown. This project focuses on gravity perception in insects, specifically Drosophila melanogaster, using its well-established genetic toolkit to uncover the mechanisms behind gravity sensing and adaptation. Additionally, the project expands to crop pests like Drosophila suzukii and Ostrinia nubilalis, aiming to address ecological and agronomic impacts related to gravity adaptation.
The overall objective is to identify sensory organs, neurons, and molecular pathways involved in gravity perception and understand how these processes influence key developmental stages, such as metamorphosis and post-eclosion, where alterations in gravity sensation may impair circulatory functions. The project's results could lead to novel insights into fundamental biological processes and offer applied benefits in pest control, exploiting gravity adaptation mechanisms to reduce crop damage.
In a broader strategic context, the project's findings will be pivotal in biocontrol strategies for agriculture, reducing reliance on chemical pesticides by targeting gravity adaptation as a vulnerability in pest species. By aligning with global agricultural sustainability goals and European Union strategies for integrated pest management, this project promises to generate significant ecological and economic impact. The research has the potential to inform future space biology studies, offering insights into how organisms, including humans, adapt to space environments, which is crucial for long-term space exploration missions.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The work performed so far has focused on uncovering the neural and molecular mechanisms behind gravity perception and adaptation in Drosophila melanogaster and other insect models. Using a large-scale neuronal inactivation screen combined with a unique geotactic phenotype of pupal spiracles orientation, I identified sensory neurons responsible for gravity detection in larvae. By employing the Gal4-UAS system and the UAS-Kir2.1 effector line to inactivate specific neurons, and using Gal80ts for temporal control, I successfully screened over 280 Gal4 lines, identifying key sensory organs and neurons involved in geotaxis. Confirmatory experiments using additional genetic tools, such as UAS-shibirets, validated the role of these neurons in controlling geotactic behavior.
The project also made significant progress in mapping the neural circuitry involved in geotaxis, utilizing transsynaptic tracing (trans-Tango) to identify second-order neurons involved in integrating gravity signals. The inactivation of these second-order neurons further impaired geotactic behavior, confirming their role in the sensory circuitry. The specific Gal4 lines that target these neurons were identified and will be used to trace third-order neurons, further elucidating the gravity-sensing network.
Additionally, early results in the study of the physiological impacts of gravity adaptation on insect development and post-eclosion processes indicate a correlation between altered geotactic behavior and developmental changes, such as an accelerated metamorphosis or delayed eclosion. Experiments are ongoing to examine the long-term physiological consequences of gravity sensing disruptions, focusing on survival, reproductive fitness, and potential sex-specific effects.
In sum, the main achievements include the identification of sensory neurons and circuits responsible for gravity detection, as well as the initiation of investigations into the broader physiological impacts of these sensory adaptations on insect development and behavior. These results lay the foundation for future applied research into biocontrol strategies for crop pests.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

The project has yielded results that go beyond the current state of the art in understanding gravity perception and its physiological implications in insects. Notably, the large-scale neuronal inactivation screen identified previously unknown sensory neurons and molecular pathways involved in gravity detection, contributing to a deeper understanding of how multi-sensory integration influences behavior. This approach, combining genetic inactivation tools and behavioral assays, represents a significant advancement in dissecting complex sensory behaviors in Drosophila melanogaster and extends to other pest insect models such as Drosophila suzukii and Ostrinia nubilalis. These findings offer a novel perspective on the mechanisms driving geotaxis behavior and the physiological adaptations to gravity.
One of the key results is the identification of specific sensory neurons and circuits that regulate gravity-induced behaviors and their role in broader physiological processes such as metamorphosis, eclosion, and circulatory system function. The mapping of these sensory pathways and the discovery of sex-specific effects on insect development under altered gravity conditions are unprecedented. Furthermore, the project's use of transsynaptic tracing and neuron inactivation techniques offers a cutting-edge approach for defining complex neural circuits involved in sensory perception, which could be applied to other systems beyond gravity sensing.
These advancements pave the way for further research and practical applications, particularly in the field of agricultural biocontrol. By manipulating gravity-sensing pathways, there is potential to disrupt pest behaviors linked to reproduction or survival, offering a novel biocontrol strategy. However, to ensure further uptake and success, additional research is needed to fully characterize the molecular mechanisms underlying sensory neuron activation by gravity forces. Moreover, demonstration projects on pest insects in agricultural settings would be critical for validating these strategies under real-world conditions.
Support in areas such as intellectual property rights (IPR), commercialisation, and international collaboration will be essential for translating these results into applied tools for pest management. Partnerships with regulatory bodies and stakeholders in the agricultural sector will also be important to standardize methods and promote the use of gravity-based pest control techniques. Overall, this work not only advances the scientific understanding of sensory systems but also opens new avenues for sustainable pest management.