Adult-specific transcriptional changes of mating and aging in the major tissues of C. elegans

Abstract

Caenorhabditis elegans is an excellent model organism for aging research. Major questions in aging research include finding phenomena that accelerate the aging process and determining the underlying causes as well as identifying mechanisms that extend lifespan and maintain healthiness in individuals. Here, three major aging questions are addressed: how mating and male pheromone affect Caenorhabditis species, what transcriptional changes occur in the major wild-type tissues and how they compare to each other, and how the neuronal transcriptome of long-lived mutant daf-2 changes with age.

The many closely-related species in the Caenorhabditis genus provide an excellent model for asking questions of the role of reproductive mode in various aspects of mating. Mating and male pheromone are known to shorten the lifespan of C. elegans hermaphrodites. Here, we ask the effects of mating and male pheromone on both androdioecious (having both hermaphrodites and males) and gonochoristic (having both females and males) species. We find that mating-induced-death is an unavoidable cost to mating in all sexes and species tested. Male pheromone, however, selectively kills androdioecious species and males in particular. Mating and pheromone-induced death provide a model for accelerated aging.

Although the adult C. elegans possesses only 959 cells, the four major somatic tissues, neurons, muscle, intestine, and hypodermis, are distinct and experience both autonomous and non-autonomous age-related phenotypes. In order to accurately explore these tissue-specific phenomena, we provide the first adult tissue-specific transcriptomes for each of the four major tissues and, in doing so, discover a novel role for the hypodermis in metabolism.

After identifying the young adult neuronal transcriptome, we next explored how the neuronal wild-type transcriptome changes with age. A clear pattern emerged: expression of genes with distinct neuronal functions declines with age, while expression of genes with nonspecific functions increases. When we examined differential expression with age in neurons of long-lived mutant daf-2, however, fewer genes were found to change. Indeed, while wild-type animals have lost the ability to learn and remember by day 8 of adulthood, daf-2 mutants retain this ability.