Abstract
Environmental stress during early development in animals can have profound effects on adult phenotypes via programmed changes in gene expression. Using the nematode C. elegans, we demonstrated previously that adults retain a cellular memory of their developmental experience that is manifested by differences in gene expression and life history traits; however, the sophistication of this system in response to different environmental stresses, and how it dictates phenotypic plasticity in adults that contribute to increased fitness in response to distinct environmental challenges, was unknown. Using transcriptional profiling, we show here that C. elegans adults indeed retain distinct cellular memories of different environmental conditions. We identified approximately 500 genes in adults that entered dauer due to starvation that exhibit significant opposite (“seesaw”) transcriptional phenotypes compared to adults that entered dauer due to crowding, and are distinct from animals that bypassed dauer. Moreover, we show that two-thirds of the genes in the genome experience a 2-fold or greater seesaw trend in gene expression, and based upon the direction of change, are enriched in large, tightly linked regions on different chromosomes. Importantly, these transcriptional programs correspond to significant changes in brood size depending on the experienced stress. In addition, we demonstrate that while the observed seesaw gene expression changes occur in both somatic and germline tissue, only starvation-induced changes require a functional GLP-4 protein necessary for germline development, and both programs require the Argonaute CSR-1. Thus, our results suggest that signaling between the soma and the germ line can generate phenotypic plasticity as a result of early environmental experience, and likely contribute to increased fitness in adverse conditions and the evolution of the C. elegans genome.
Highlights
Phenotypic plasticity in response to environmental stress is a critical component of organismal fitness
We identified 1,121 and 551 genes that exhibited significant upand downregulation, respectively, in wild-type PDStv compared to wild-type CONStv (WTStv) (Fig 1A and S1 Table)
We identified 441 and 560 genes that were significantly up- or downregulated, respectively, in wild-type PDPhe compared to wild-type CONPhe (WTPhe) (Fig 1B and S1 Table)
Summary
Phenotypic plasticity in response to environmental stress is a critical component of organismal fitness. In C. elegans, the observed increased longevity is dependent upon the inheritance of starvation-induced non-coding small RNAs, likely imported into the germ line from the soma [3] While this example is intriguing, an important and unresolved question is to what extent does environmentally-induced phenotypic plasticity mediated by changes in epigenetic marks result in adaptive variation of traits that is favored by natural selection [5, 6]. A potential prerequisite for the evolution of mechanisms that modulate adult phenotypes in response to specific stressors is that early environmental conditions are predictive of future conditions The sensitivity of this developmental system to different dauer-inducing conditions, and how this may contribute to distinct phenotypic trajectories, is unknown. Numerous molecular cues may have the potential to propagate information regarding early-life experiences to modulate adult developmental outcomes
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