The specific expression patterns of sensory neuron membrane proteins are retained throughout the development of the desert locust Schistocerca gregaria

Cassau, Sina; Degen, Angelina; Krüger, Stephanie; Krieger, Jürgen

doi:10.1016/j.cris.2023.100053

Cited by 3 publications

(7 citation statements)

References 55 publications

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“…6). These morphological features appear to match the topographic expression of odorant binding proteins in sensilla on the antenna (Jiang et al 2018) that appear to be retained throughout development (Cassau et al 2023). A similar developmental pattern is also present in the cockroach where meristal annuli are progressively added to the base of the agellum during postembryonic development so that more sensilla form proximally as nymphal development progresses (Watanabe et al 2018).…”

Section: Labeled Lines In Developmentmentioning

confidence: 69%

“…These apical annuli bear a spectrum of sensilla that encode environmental stimuli (Hansson et al 1996;Ochieng et al 1998; Chapman 2002) and whose sensory neurons project to the brain (see Hansson et al 1996). Among these sensilla are the basiconic-type bristles (see Slifer et al 1957Slifer et al , 1959) that have been implicated in olfaction, gustation and mechanoreception (Hansson et al 1996; Ochieng et al 1998;Boronat-Garcia et al 2022;Cassau et al 2023). The nding that on hatching, basiconic-type sensilla are found at conserved locations on each apical annular segment (Ochieng et al 1998; Chapman 2002) suggests these might serve as a model system for studying how information transfer from the antenna to the brain along labeled communication lines becomes established.…”

Section: Introductionmentioning

confidence: 99%

“…In our developmental study here we examine a labeled-line system in the locust Schistocerca gregaria involving basiconic-type sensilla (see Suppl. Figure1;Slifer et al 1957Slifer et al , 1959 implicated in olfaction, gustation and mechanoreception(Hansson et al 1996;Ochieng et al 1998;Boronat-Garcia et al 2022;Cassau et al 2023). On hatching, these sensilla are found at conserved locations on each apical segment (or annulus) of the antenna(Hansson et al 1996;Ochieng et al 1998;…”

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confidence: 99%

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From bristle to brain: embryonic development of labeled lines in the antennal nervous system of the locust Schistocerca gregaria

Boyan,

Ehrhardt

2024

Preprint

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The antennal flagellum of the locust S. gregaria is an articulated structure bearing a spectrum of sensory sensilla that encode environmental stimuli mediating adaptive behavior. In this study we focus on the basiconic-type bristles as a model for sensory system development in the antenna. At the end of embryogenesis these bristles are found at conserved locations on each apical segment of the flagellum, are innervated by a dendrite from a sensory cell cluster in the underlying epithelium with each cluster directing an axon topographically to an antennal tract and the brain. We employ confocal imaging and immunolabeling to (a) identify mitotically active sense organ precursors for sensory cell clusters in the most apical annuli of the early embryonic antenna; (b) follow the subsequent differentiation of their neuronal progeny; and (c) map the spatial and temporal organization of axonal projections into the antennal tracts. We show that early in embryogenesis proliferative precursors are localized circumferentially within discrete epithelial domains of the flagellum. Differentiation of their clonal progeny begins apically and proceeds in a basal direction along the antenna so that the oldest neuronal populations are near the antennal tip with progressively younger populations located more basally. Autotracing reveals that axon fasciculation with a tract is sequential and reflects the location and age of the cell cluster along the flagellum. Cell cluster location and bristle location on the cuticle are therefore encoded topographically and temporally within the axon profile of the tract and its projection to the brain.

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Section: Labeled Lines In Developmentmentioning

confidence: 69%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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From bristle to brain: embryonic development of labeled lines in the antennal nervous system of the locust Schistocerca gregaria

Boyan,

Ehrhardt

2024

Preprint

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“…In our developmental study here, we examine a sensory system in the locust Schistocerca gregaria involving basiconic-type sensilla (see Suppl. Figure 1 ; Slifer et al 1957 , 1959 ) implicated in olfaction, gustation, and mechanoreception (Hansson et al 1996 ; Ochieng et al 1998 ; Boronat-Garcia et al 2022 ; Cassau et al 2023 ). On hatching, these sensilla are found at fixed locations on only the six most distal segments (or annuli) of the antenna (Hansson et al 1996 ; Ochieng et al 1998 ; Chapman 2002 ) and project axons to the brain (see Hansson et al 1996 ).…”

Section: Discussionmentioning

confidence: 99%

“…These distal annuli bear a spectrum of sensilla that respond to various sensory stimuli (Hansson et al 1996 ; Ochieng et al 1998 ; Chapman 2002 ) and whose sensory neurons direct projections to the brain (see Hansson et al 1996 ). Among these sensilla are the basiconic-type bristles (see Slifer et al 1957 , 1959 ) that have been implicated in olfaction, gustation, and mechanoreception (Hansson et al 1996 ; Ochieng et al 1998 ; Boronat-Garcia et al 2022 ; Cassau et al 2023 ). Strikingly, on hatching, basiconic-type sensilla are not only found at fixed locations on an annulus, but also only on the most distal six annular segments of the antenna that form during embryogenesis (Chapman 2002 ).…”

Section: Introductionmentioning

confidence: 99%

From bristle to brain: embryonic development of topographic projections from basiconic sensilla in the antennal nervous system of the locust Schistocerca gregaria

Boyan,

Ehrhardt

2024

Dev Genes Evol

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The antennal flagellum of the locust S. gregaria is an articulated structure bearing a spectrum of sensilla that responds to sensory stimuli. In this study, we focus on the basiconic-type bristles as a model for sensory system development in the antenna. At the end of embryogenesis, these bristles are found at fixed locations and then on only the most distal six articulations of the antenna. They are innervated by a dendrite from a sensory cell cluster in the underlying epithelium, with each cluster directing fused axons topographically to an antennal tract running to the brain. We employ confocal imaging and immunolabeling to (a) identify mitotically active sense organ precursors for sensory cell clusters in the most distal annuli of the early embryonic antenna; (b) observe the subsequent spatial appearance of their neuronal progeny; and (c) map the spatial and temporal organization of axon projections from such clusters into the antennal tracts. We show that early in embryogenesis, proliferative precursors are localized circumferentially within discrete epithelial domains of the flagellum. Progeny first appear distally at the antennal tip and then sequentially in a proximal direction so that sensory neuron populations are distributed in an age-dependent manner along the antenna. Autotracing reveals that axon fasciculation with a tract is also sequential and reflects the location and age of the cell cluster along the most distal annuli. Cell cluster location and bristle location are therefore represented topographically and temporally within the axon profile of the tract and its projection to the brain.

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SNMP1 is critical for sensitive detection of the desert locust aromatic courtship inhibition pheromone phenylacetonitrile

Lehmann,

Günzel,

Khosravian

et al. 2024

BMC Biol

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Background Accurate detection of pheromones is crucial for chemical communication and reproduction in insects. In holometabolous flies and moths, the sensory neuron membrane protein 1 (SNMP1) is essential for detecting long-chain aliphatic pheromones by olfactory neurons. However, its function in hemimetabolous insects and its role for detecting pheromones of a different chemical nature remain elusive. Therefore, we investigated the relevance of SNMP1 for pheromone detection in a hemimetabolous insect pest of considerable economic importance, the desert locust Schistocerca gregaria, which moreover employs the aromatic pheromone phenylacetonitrile (PAN) to govern reproductive behaviors. Results Employing CRISPR/Cas-mediated gene editing, a mutant locust line lacking functional SNMP1 was established. In electroantennography experiments and single sensillum recordings, we found significantly decreased electrical responses to PAN in SNMP1-deficient (SNMP1−/−) locusts. Moreover, calcium imaging in the antennal lobe of the brain revealed a substantially reduced activation of projection neurons in SNMP1−/− individuals upon exposure to PAN, indicating that the diminished antennal responsiveness to PAN in mutants affects pheromone-evoked neuronal activity in the brain. Furthermore, in behavioral experiments, PAN-induced effects on pairing and mate choice were altered in SNMP1−/− locusts. Conclusions Our findings emphasize the importance of SNMP1 for chemical communication in a hemimetabolous insect pest. Moreover, they show that SNMP1 plays a crucial role in pheromone detection that goes beyond long-chain aliphatic substances and includes aromatic compounds controlling reproductive behaviors.

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The specific expression patterns of sensory neuron membrane proteins are retained throughout the development of the desert locust Schistocerca gregaria

Cited by 3 publications

References 55 publications

From bristle to brain: embryonic development of labeled lines in the antennal nervous system of the locust Schistocerca gregaria

From bristle to brain: embryonic development of labeled lines in the antennal nervous system of the locust Schistocerca gregaria

From bristle to brain: embryonic development of topographic projections from basiconic sensilla in the antennal nervous system of the locust Schistocerca gregaria

SNMP1 is critical for sensitive detection of the desert locust aromatic courtship inhibition pheromone phenylacetonitrile

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