Abstract
During prolonged nutrient restriction, developing animals redistribute vital nutrients to favor brain growth at the expense of other organs. In Drosophila, such brain sparing relies on a glia-derived growth factor to sustain proliferation of neural stem cells. However, whether other aspects of neural development are also spared under nutrient restriction is unknown. Here we show that dynamically growing somatosensory neurons in the Drosophila peripheral nervous system exhibit organ sparing at the level of arbor growth: Under nutrient stress, sensory dendrites preferentially grow as compared to neighboring non-neural tissues, resulting in dendrite overgrowth. These neurons express lower levels of the stress sensor FoxO than neighboring epidermal cells, and hence exhibit no marked induction of autophagy and a milder suppression of Tor signaling under nutrient stress. Preferential dendrite growth allows for heightened animal responses to sensory stimuli, indicative of a potential survival advantage under environmental challenges.
Highlights
Proper animal development requires coordinated growth of various organs to achieve the correct relative organ proportions in mature individuals
Our results suggest that among genes known to inhibit mTor signaling under nutrient stress, foxo plays a more significant role in nutrient-dependent dendrite overgrowth of somatosensory neurons
We show that Drosophila C3da and C4da neurons exhibit a growth advantage over neighboring epidermal cells under nutrient restriction, resulting in dendrite overgrowth
Summary
Proper animal development requires coordinated growth of various organs to achieve the correct relative organ proportions in mature individuals. When developing animals face adverse conditions, such as limited availability of nutrients, they reallocate essential resources to favor growth of vital organs at the expense of other organs. This phenomenon of ‘organ sparing’ is exemplified by the preferential growth of the brain in human fetuses experiencing intrauterine growth restriction, resulting in undersized newborns with disproportionately large heads (Gruenwald, 1963). The larval brain is protected against nutrient deprivation and exhibits continuous neurogenesis (Cheng et al, 2011).
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