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A molecular toolkit for superorganisms

Sieriebriennikov, Bogdan; Reinberg, Danny; Desplan, Claude
Social insects, such as ants, bees, wasps, and termites, draw biologists' attention due to their distinctive lifestyles. As experimental systems, they provide unique opportunities to study organismal differentiation, division of labor, longevity, and the evolution of development. Ants are particularly attractive because several ant species can be propagated in the laboratory. However, the same lifestyle that makes social insects interesting also hampers the use of molecular genetic techniques. Here, we summarize the efforts of the ant research community to surmount these hurdles and obtain novel mechanistic insight into the biology of social insects. We review current approaches and propose novel ones involving genomics, transcriptomics, chromatin and DNA methylation profiling, RNA interference (RNAi), and genome editing in ants and discuss future experimental strategies.
PMID: 34116864
ISSN: 0168-9525
CID: 4911092

Building a circuit through correlated spontaneous neuronal activity in the developing vertebrate and invertebrate visual systems

Choi, Ben Jiwon; Chen, Yu-Chieh David; Desplan, Claude
During the development of the vertebrate nervous systems, genetic programs assemble an immature circuit that is subsequently refined by neuronal activity evoked by external stimuli. However, prior to sensory experience, the intrinsic property of the developing nervous system also triggers correlated network-level neuronal activity, with retinal waves in the developing vertebrate retina being the best documented example. Spontaneous activity has also been found in the visual system of Drosophila Here, we compare the spontaneous activity of the developing visual system between mammalian and Drosophila and suggest that Drosophila is an emerging model for mechanistic and functional studies of correlated spontaneous activity.
PMID: 33888564
ISSN: 1549-5477
CID: 4847952

Early behavioral and molecular events leading to caste switching in the ant Harpegnathos

Opachaloemphan, Comzit; Mancini, Giacomo; Konstantinides, Nikos; Parikh, Apurva; Mlejnek, Jakub; Yan, Hua; Reinberg, Danny; Desplan, Claude
Ant societies show a division of labor in which a queen is in charge of reproduction while nonreproductive workers maintain the colony. In Harpegnathos saltator, workers retain reproductive ability, inhibited by the queen pheromones. Following the queen loss, the colony undergoes social unrest with an antennal dueling tournament. Most workers quickly abandon the tournament while a few workers continue the dueling for months and become gamergates (pseudoqueens). However, the temporal dynamics of the social behavior and molecular mechanisms underlining the caste transition and social dominance remain unclear. By tracking behaviors, we show that the gamergate fate is accurately determined 3 d after initiation of the tournament. To identify genetic factors responsible for this commitment, we compared transcriptomes of different tissues between dueling and nondueling workers. We found that juvenile hormone is globally repressed, whereas ecdysone biosynthesis in the ovary is increased in gamergates. We show that molecular changes in the brain serve as earliest caste predictors compared with other tissues. Thus, behavioral and molecular data indicate that despite the prolonged social upheaval, the gamergate fate is rapidly established, suggesting a robust re-establishment of social structure.
PMID: 33602869
ISSN: 1549-5477
CID: 4787162

Neuronal diversity and convergence in a visual system developmental atlas

Özel, Mehmet Neset; Simon, Félix; Jafari, Shadi; Holguera, Isabel; Chen, Yen-Chung; Benhra, Najate; El-Danaf, Rana Naja; Kapuralin, Katarina; Malin, Jennifer Amy; Konstantinides, Nikolaos; Desplan, Claude
Deciphering how neuronal diversity is established and maintained requires a detailed knowledge of neuronal gene expression throughout development. In contrast to mammalian brains1,2, the large neuronal diversity of the Drosophila optic lobe3 and its connectome4-6 are almost completely characterized. However, a molecular characterization of this neuronal diversity, particularly during development, has been lacking. Here we present insights into brain development through a nearly complete description of the transcriptomic diversity of the optic lobes of Drosophila. We acquired the transcriptome of 275,000 single cells at adult and at five pupal stages, and built a machine-learning framework to assign them to almost 200 cell types at all time points during development. We discovered two large neuronal populations that wrap neuropils during development but die just before adulthood, as well as neuronal subtypes that partition dorsal and ventral visual circuits by differential Wnt signalling throughout development. Moreover, we show that the transcriptomes of neurons that are of the same type but are produced days apart become synchronized shortly after their production. During synaptogenesis we also resolved neuronal subtypes that, although differing greatly in morphology and connectivity, converge to indistinguishable transcriptomic profiles in adults. Our datasets almost completely account for the known neuronal diversity of the Drosophila optic lobes, and serve as a paradigm to understand brain development across species.
PMID: 33149298
ISSN: 1476-4687
CID: 4662932

Neuronal differentiation strategies: insights from single-cell sequencing and machine learning

Konstantinides, Nikolaos; Desplan, Claude
Neuronal replacement therapies rely on the in vitro differentiation of specific cell types from embryonic or induced pluripotent stem cells, or on the direct reprogramming of differentiated adult cells via the expression of transcription factors or signaling molecules. The factors used to induce differentiation or reprogramming are often identified by informed guesses based on differential gene expression or known roles for these factors during development. Moreover, differentiation protocols usually result in partly differentiated cells or the production of a mix of cell types. In this Hypothesis article, we suggest that, to overcome these inefficiencies and improve neuronal differentiation protocols, we need to take into account the developmental history of the desired cell types. Specifically, we present a strategy that uses single-cell sequencing techniques combined with machine learning as a principled method to select a sequence of programming factors that are important not only in adult neurons but also during differentiation.
PMID: 33293292
ISSN: 1477-9129
CID: 4722442

Extrinsic activin signaling cooperates with an intrinsic temporal program to increase mushroom body neuronal diversity

Rossi, Anthony M; Desplan, Claude
Temporal patterning of neural progenitors leads to the sequential production of diverse neurons. To understand how extrinsic cues influence intrinsic temporal programs, we studied Drosophila mushroom body progenitors (neuroblasts) that sequentially produce only three neuronal types: γ, then α'β', followed by αβ. Opposing gradients of two RNA-binding proteins Imp and Syp comprise the intrinsic temporal program. Extrinsic activin signaling regulates the production of α'β' neurons but whether it affects the intrinsic temporal program was not known. We show that the activin ligand Myoglianin from glia regulates the temporal factor Imp in mushroom body neuroblasts. Neuroblasts missing the activin receptor Baboon have a delayed intrinsic program as Imp is higher than normal during the α'β' temporal window, causing the loss of α'β' neurons, a decrease in αβ neurons, and a likely increase in γ neurons, without affecting the overall number of neurons produced. Our results illustrate that an extrinsic cue modifies an intrinsic temporal program to increase neuronal diversity.
PMID: 32628110
ISSN: 2050-084x
CID: 4606292

The genome of pest Rhynchophorus ferrugineus reveals gene families important at the plant-beetle interface

Hazzouri, Khaled Michel; Sudalaimuthuasari, Naganeeswaran; Kundu, Biduth; Nelson, David; Al-Deeb, Mohammad Ali; Le Mansour, Alain; Spencer, Johnston J; Desplan, Claude; Amiri, Khaled M A
The red palm weevil, Rhynchophorus ferrugineus, infests palm plantations, leading to large financial losses and soil erosion. Pest-host interactions are poorly understood in R. ferrugineus, but the analysis of genetic diversity and pest origins will help advance efforts to eradicate this pest. We sequenced the genome of R. ferrugineus using a combination of paired-end Illumina sequencing (150 bp), Oxford Nanopore long reads, 10X Genomics and synteny analysis to produce an assembly with a scaffold N50 of ~60 Mb. Structural variations showed duplication of detoxifying and insecticide resistance genes (e.g., glutathione S-transferase, P450, Rdl). Furthermore, the evolution of gene families identified those under positive selection including one glycosyl hydrolase (GH16) gene family, which appears to result from horizontal gene transfer. This genome will be a valuable resource to understand insect evolution and behavior and to allow the genetic modification of key genes that will help control this pest.
PMID: 32581279
ISSN: 2399-3642
CID: 4606272

The diversity of lobula plate tangential cells (LPTCs) in the Drosophila motion vision system

Wei, Huayi; Kyung, Ha Young; Kim, Priscilla J; Desplan, Claude
To navigate through the environment, animals rely on visual feedback to control their movements relative to their surroundings. In dipteran flies, visual feedback is provided by the wide-field motion-sensitive neurons in the visual system called lobula plate tangential cells (LPTCs). Understanding the role of LPTCs in fly behaviors can address many fundamental questions on how sensory circuits guide behaviors. The blowfly was estimated to have ~ 60 LPTCs, but only a few have been identified in Drosophila. We conducted a Gal4 driver screen and identified five LPTC subtypes in Drosophila, based on their morphological characteristics: LPTCs have large arborizations in the lobula plate and project to the central brain. We compared their morphologies to the blowfly LPTCs and named them after the most similar blowfly cells: CH, H1, H2, FD1 and FD3, and V1. We further characterized their pre- and post-synaptic organizations, as well as their neurotransmitter profiles. These anatomical features largely agree with the anatomy and function of their likely blowfly counterparts. Nevertheless, several anatomical details indicate the Drosophila LPTCs may have more complex functions. Our characterization of these five LPTCs in Drosophila will facilitate further functional studies to understand their roles in the visual circuits that instruct fly behaviors.
PMID: 31709462
ISSN: 1432-1351
CID: 4195382

Evolution, developmental expression and function of odorant receptors in insects

Yan, Hua; Jafari, Shadi; Pask, Gregory; Zhou, Xiaofan; Reinberg, Danny; Desplan, Claude
Animals rely on their chemosensory system to discriminate among a very large number of attractive or repulsive chemical cues in the environment, which is essential to respond with proper action. The olfactory sensory systems in insects share significant similarities with those of vertebrates, although they also exhibit dramatic differences, such as the molecular nature of the odorant receptors (ORs): insect ORs function as heteromeric ion channels with a common Orco subunit, unlike the G-protein-coupled olfactory receptors found in vertebrates. Remarkable progress has recently been made in understanding the evolution, development and function of insect odorant receptor neurons (ORNs). These studies have uncovered the diversity of olfactory sensory systems among insect species, including in eusocial insects that rely extensively on olfactory sensing of pheromones for social communication. However, further studies, notably functional analyses, are needed to improve our understanding of the origins of the Orco-OR system, the mechanisms of ORN fate determination, and the extraordinary diversity of behavioral responses to chemical cues.
PMID: 32034042
ISSN: 1477-9145
CID: 4301612

Gene regulatory networks during the development of the Drosophila visual system

Chen, Yen-Chung; Desplan, Claude
The Drosophila visual system integrates input from 800 ommatidia and extracts different features in stereotypically connected optic ganglia. The development of the Drosophila visual system is controlled by gene regulatory networks that control the number of precursor cells, generate neuronal diversity by integrating spatial and temporal information, coordinate the timing of retinal and optic lobe cell differentiation, and determine distinct synaptic targets of each cell type. In this chapter, we describe the known gene regulatory networks involved in the development of the different parts of the visual system and explore general components in these gene networks. Finally, we discuss the advantages of the fly visual system as a model for gene regulatory network discovery in the era of single-cell transcriptomics.
PMID: 32450970
ISSN: 1557-8933
CID: 4670342