Abstract
The antennal nervous system of the grasshopper Schistocerca gregaria features two parallel axon tracts each established early in embryogenesis by discrete pairs of pioneer neurons located at the antennal tip and whose growth cones contact so-called base pioneers en route to the brain. Here we present two antennal phenotypes in which a stereotypic dysregulation of axogenesis in a given tract is observed when only the base pioneer associated with that pathway is missing, consistent with a role for this cell type in guided axogenesis. Dysregulation involves defasciculation and aberrant navigation by pioneer axons resulting in a missing or depleted primordial antennal nerve to the brain. The dysregulated phenotypes reveal that axogenesis in each pathway is regulated independently. Previously unseen discrepancies in the navigational decisions made by pioneer neurons which derive sequentially from the same mother cell demonstrate that these progeny have separate identities. Possible mechanisms for the dysregulated phenotypes are considered.
References
Apitz H, Salecker I (2014) A challenge of numbers and diversity: neurogenesis in the Drosophila optic lobe. J Neurogenet 28:233–249
Bate CM (1976) Pioneer neurones in an insect embryo. Nature 260:54–56
Bentley D, Caudy M (1983) Pioneer axons lose directed growth after selective killing of guidepost cells. Nature 304:62–65
Bentley D, O’Connor TP (1992) Guidance and steering of peripheral growth cones in grasshopper embryos. In: Letourneau C, Kater SB, Macagno ER (eds) The nerve growth cone. Raven Press, New York, pp 265–282
Bentley D, Keshishian H, Shankland M, Torian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J Embryol Exp Morphol 54:47–74
Berlot J, Goodman CS (1984) Guidance of peripheral pioneer neurons in the grasshopper: adhesive hierarchy of epithelial and neuronal surfaces. Science 223:493–496
Boyan G, Ehrhardt E (2017) Ontogeny of pioneer neurons in the antennal nervous system of the grasshopper Schistocerca gregaria. Dev Genes Evol 227:11–23
Boyan GS, Williams JLD (2004) Embryonic development of the sensory innervation of the antenna of the grasshopper Schistocerca gregaria. Arthropod Struct Dev 33:381–397
Chang WS, Serikawa K, Allen K, Bentley D (1992) Disruption of pioneer growth cone guidance in vivo by removal of glycosylphosphatidylinositol-anchored cell surface proteins. Development 114:507–519
Ehrhardt E, Liu Y, Boyan GS (2015) Axogenesis in the antennal nervous system of the grasshopper Schistocerca gregaria revisited: the base pioneers. Dev Genes Evol 225:39–45
Ehrhardt EE, Graf P, Kleele T, Liu Y, Boyan GS (2016) Fates of identified pioneer cells in the developing antennal nervous system of the grasshopper Schistocerca gregaria. Arthropod Struct Dev 45:23–30
Ganfornina MD, Sánchez D, Bastiani MJ (1995) Lazarillo, a new GPI-linked surface lipocalin, is restricted to a subset of neurons in the grasshopper embryo. Development 121:123–134
Goodman CS (1996) Mechanisms and molecules that control growth cone guidance. Annu Rev Neurosci 19:341–377
Ho RK, Goodman CS (1982) Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos. Nature 297:404–406
Jan LY, Jan YN (1982) Antibodies to horseradish-peroxidase as specific neuronal markers in Drosophila and grasshopper embryos. Proc Natl Acad Sci USA 79:2700–2704
Jarman AP (2014) Development of the auditory organ (Johnston’s organ) in Drosophila. In: Romand R, Varela-Nieto I (eds) Development of auditory and vestibular systems. Academic Press, Cambridge, pp 31–63
Keil TA (1997) Comparative morphogenesis of sensilla: a review. Int J Insect Morphol Embryol 26:151–160
Keshishian H, Bentley D (1983) Embryogenesis of peripheral nerve pathways in grasshoppers legs. I. The initial nerve pathway to the CNS. Dev Biol 96:89–102
Kutsch W, Bentley D (1987) Programmed death of peripheral pioneer neurons in the grasshopper embryo. Dev Biol 123:517–525
Pearson BJ, Doe CQ (2003) Regulation of neuroblast competence in Drosophila. Nature 425:624–628
Sánchez D, Ganfornina MD, Bastiani MJ (1995) Developmental expression of the lipocalin Lazarillo and its role in axonal pathfinding in the grasshopper embryo. Development 121:135–147
Seidel C, Bicker G (2000) Nitric oxide and cGMP influence axogenesis of antennal pioneer neurons. Development 127:4541–4549
Van Vactor D, Sink H, Fambrough D, Tsoo R, Goodman CS (1993) Genes that control neuromuscular specificity in Drosophila. Cell 73:1137–1153
Acknowledgements
We thank Dr. Tatjana Kleele for assistance with confocal imaging, Dr. Yu Liu for critical reading of an earlier manuscript, and two anonymous referees for their valuable insights. Both authors received financial support for this study from the Graduate School of Systemic Neuroscience, Biocenter, Ludwig-Maximilians-University of Munich.
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Boyan, G., Ehrhardt, E. Dysregulation of axogenesis in the antennal nervous system of the embryonic grasshopper Schistocerca gregaria. Invert Neurosci 19, 3 (2019). https://doi.org/10.1007/s10158-019-0223-0
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DOI: https://doi.org/10.1007/s10158-019-0223-0