4.6 Article

Maternal starvation primes progeny response to nutritional stress

Journal

PLOS GENETICS
Volume 17, Issue 11, Pages -

Publisher

PUBLIC LIBRARY SCIENCE
DOI: 10.1371/journal.pgen.1009932

Keywords

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Funding

  1. Temasek Life Sciences Laboratory

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This study reveals the impact of starvation in Drosophila mothers on their offspring and the role of maternally inherited specific transcripts in starvation response.
Organisms adapt to environmental changes in order to survive. Mothers exposed to nutritional stresses can induce an adaptive response in their offspring. However, the molecular mechanisms behind such inheritable links are not clear. Here we report that in Drosophila, starvation of mothers primes the progeny against subsequent nutritional stress. We found that RpL10Ab represses TOR pathway activity by genetically interacting with TOR pathway components TSC2 and Rheb. In addition, starved mothers produce offspring with lower levels of RpL10Ab in the germline, which results in higher TOR pathway activity, conferring greater resistance to starvation-induced oocyte loss. The RpL10Ab locus encodes for the RpL10Ab mRNA and a stable intronic sequence RNA (sisR-8), which collectively repress RpL10Ab pre-mRNA splicing in a negative feedback mechanism. During starvation, an increase in maternally deposited RpL10Ab and sisR-8 transcripts leads to the reduction of RpL10Ab expression in the offspring. Our study suggests that the maternally deposited RpL10Ab and sisR-8 transcripts trigger a negative feedback loop that mediates intergenerational adaptation to nutritional stress as a starvation response. Author summaryIn the wild, animals need to adapt to frequent changes in the environment. Mothers who are exposed to nutritional stresses are known to produce offspring which are preconditioned to adapt to the mothers' environment. However, it is unclear how such maternal memory is being passed on to the offspring. Here we show that Drosophila mothers exposed to starvation produce offspring which are more resistant to starvation during oogenesis. This process is mediated by maternally inherited RpL10Ab mRNA and a stable intronic sequence RNA (sisR-8), which collectively repress the splicing of RpL10Ab pre-mRNA, leading to lower RpL10Ab expression in the offspring ovaries. As a consequence, lower RpL10Ab expression results in higher TOR pathway activity, conferring greater resistance to starvation during oogenesis. Hence, maternally inherited transcripts may play a role as mediators in conferring intergenerational adaption to starvation.

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