Environmental stress and phenotypic tradeoff modulate the adaptive potential of novel coding sequences for de novo gene birth

De novo protein-coding genes can arise from noncoding sequences, enabling adaptation to environmental stresses. Previous research suggests that the translation of low-expressed open reading frames (ORFs) in these regions provides a vast repository of proto-genes, the acquisition of gene-like qualities, like heightened expression, may face selection based on their phenotypic consequences.

However, the influence of environmental conditions on these consequences remains uncertain. Researchers simulated the evolution of proto-genes in yeast (Saccharomyces cerevisiae) by boosting the expression of nearly a thousand de novo ORFs under osmotic and endoplasmic-reticulum stress, as well as in standard conditions. Phenotyping data showed that growth effects of enhanced expression differed greatly between environments for these ORFs.

An additional screening across 22 varied environments demonstrated a consistent positive relationship between environmental stress intensity and the average growth impact of increased de novo ORF expression. At the individual level, 5.4% of the tested de novo ORFs displayed beneficial traits in at least one environment, while 83.3% of these also generated deleterious effects in other settings, indicating widespread phenotypic tradeoffs.

The study highlights that the increased expression of the de novo translated ORF YLR112W leads to improved growth in the presence of rapamycin by alleviating the growth-suppressing transcriptomic reaction triggered by this drug. Overall, these results demonstrate that stress severity determines the phenotypic impacts of heightened proto-gene expression and illuminate the roles of tradeoffs and transcriptome remodeling in shaping these environmental dependencies.