Abstract
Massive water loss is a serious challenge for terrestrial animals, which usually has fatal consequences. However, some organisms have developed means to survive this stress by entering an ametabolic state called anhydrobiosis. The molecular and cellular mechanisms underlying this phenomenon are poorly understood. We recently showed that Caenorhabditis elegans dauer larva, an arrested stage specialized for survival in adverse conditions, is resistant to severe desiccation. However, this requires a preconditioning step at a mild desiccative environment to prepare the organism for harsher desiccation conditions. A systems approach was used to identify factors that are activated during this preconditioning. Using microarray analysis, proteomics, and bioinformatics, genes, proteins, and biochemical pathways that are upregulated during this process were identified. These pathways were validated via reverse genetics by testing the desiccation tolerances of mutants. These data show that the desiccation response is activated by hygrosensation (sensing the desiccative environment) via head neurons. This leads to elimination of reactive oxygen species and xenobiotics, expression of heat shock and intrinsically disordered proteins, polyamine utilization, and induction of fatty acid desaturation pathway. Remarkably, this response is specific and involves a small number of functional pathways, which represent the generic toolkit for anhydrobiosis in plants and animals.
Highlights
Terrestrial organisms encounter limited water supplies seasonally or permanently
Our results indicate that desiccation tolerance of C. elegans depends on a small number of functional pathways that are conserved among plants and animals, which can be a generic toolkit for anhydrobiosis
We used a systems approach to elucidate the genes and proteins that are induced or activated in response to desiccation stress. The outcome of this analysis was used to define candidate anhydrobiotic pathways, which were validated by a standardized desiccation tolerance assay on mutant worms or worms treated with RNA interference (RNAi)
Summary
Terrestrial organisms encounter limited water supplies seasonally or permanently. To survive, many organisms have evolved strategies to respond to this challenge. Anhydrobiosis has probably been best studied in resurrection plants, which can survive losing more than 95% of the free water in their vegetative tissues. These plants initially react to desiccation stress by abscisic acid-mediated expression of stress-resistance genes such as aldehyde dehydrogenases, heat shock proteins (HSPs), and late embryogenesis abundant (LEA) proteins [11]. The ability of an animal to sense a change in ambient humidity, known as hygrosensation, was first studied at the molecular level in fruit flies [24] and was recently associated with the transient receptor potential (TRP) channels Nanchung, Inactive, and Water witch that are expressed in neurons [25]. Our results indicate that desiccation tolerance of C. elegans depends on a small number of functional pathways that are conserved among plants and animals, which can be a generic toolkit for anhydrobiosis
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