Bridging the gap between postembryonic cell lineages and identified embryonic neuroblasts in the ventral nerve cord ofDrosophila melanogaster

Abstract

The clarification of complete cell lineages, which are produced by specific stem cells, is fundamental for understanding mechanisms, controlling the generation of cell diversity and patterning in an emerging tissue. In the developing Central Nervous System (CNS) of Drosophila, neural stem cells (neuroblasts) exhibit two periods of proliferation: During embryogenesis they produce primary lineages, which form the larval CNS. After a phase of mitotic quiescence, a subpopulation of them resumes proliferation in the larva to give rise to secondary lineages that build up the CNS of the adult fly. Within the ventral nerve cord (VNC) detailed descriptions exist for both primary and secondary lineages. However, while primary lineages have been linked to identified neuroblasts, the assignment of secondary lineages has so far been hampered by technical limitations. Therefore, primary and secondary neural lineages co-existed as isolated model systems. Here we provide the missing link between the two systems for all lineages in the thoracic and abdominal neuromeres. Using the Flybow technique, embryonic neuroblasts were identified by their characteristic and unique lineages in the living embryo and their further development was traced into the late larval stage. This comprehensive analysis provides the first complete view of which embryonic neuroblasts are postembryonically reactivated along the anterior/posterior-axis of the VNC, and reveals the relationship between projection patterns of primary and secondary sublineages.

Lineage-associated tracts defining the anatomy of the Drosophila first instar larval brain

“…This has been recently achieved for the lineages of the ventral nerve cord (Birkholz et al, 2015), and a few select lineages of the brain, including the mushroom body (Kunz et al, 2012). In Birkholz et al (2015), the prior use of labeled embryonic clones was instrumental to identify larval lineages with specific neuroblasts, and we anticipate the same to be true for brain lineages.…”

“…This has been recently achieved for the lineages of the ventral nerve cord (Birkholz et al, 2015), and a few select lineages of the brain, including the mushroom body (Kunz et al, 2012). In Birkholz et al (2015), the prior use of labeled embryonic clones was instrumental to identify larval lineages with specific neuroblasts, and we anticipate the same to be true for brain lineages. Our L1 lineage atlas, translated into the late embryonic brain, will provide an anatomical scaffold with discrete landmarks to which embryonic neuroblast clones, as well as lineage-specific markers expressed from the neuroblast stage towards the late embryo, can be related.…”

Programmed cell death acts at different stages of Drosophila neurodevelopment to shape the central nervous system

“…Exceptions are observed in the thorax; neuroblasts 5-6, 6-4 and 7-3 die at stage 16 (Baumgardt, Karlsson et al 2009, Lacin and Truman 2016). Also, the lineages of neuroblasts 2-2, 5-1, 5-4, 5-5 and 6-2 differ between wild type and H99 deficiency clones (Rogulja-Ortmann, Luer et al 2007, Birkholz, Rickert et al 2015, Lacin and Truman 2016). Such differences might arise due to neuroblast or neuronal apoptosis.…”

Neurogenesis reunited

“…This means that for decades these two fields of research have remained largely disconnected, as if they concerned two different beasts. However, last year, Gerhard Technau and colleagues at the University of Mainz started to bridge this gap by studying these two phases of neurogenesis in D. melanogaster (Birkholz et al, 2015). Now, in eLife, Haluk Lacin and James Truman of the Janelia Research Campus report how they have built on this work to complete the job (Lacin and Truman, 2016).…”

“…Technau and colleagues used an approach called the “Flybow” technique to track neuroblast cells (plus the cells descended from these neuroblasts) from the embryo to the late-stage larva just before metamorphosis (Birkholz et al, 2015; Hadjieconomou et al, 2011). Lacin and Truman, on the other hand, used new genetic tools that allowed them to follow lineages of specific neuroblasts and their descendants all the way into the pupal and adult stages (Lacin and Truman, 2016; Awasaki et al, 2014).…”