Young Genes are More Responsive to Environmental Stress than Ancient Genes in Budding Yeasts

Abstract

The Saccharomycotina subphylum (budding yeasts) spans more than 400 million years of evolution and includes species that thrive in many of Earths harsh environments. Characterizing species that grow in harsh conditions could enable the design of more robust yeast strains for biotechnology. However, tolerance to stressful conditions is a multifactorial response, which is difficult to understand since many of the genes involved are as yet uncharacterized. In this work, three divergent yeast species were grown under multiple stressful conditions to identify stress-induced genes. For each condition, duplicated and non-conserved genes were significantly enriched for stress responsiveness compared to single-copy conserved genes. To understand this further, we developed a sorting method that considers evolutionary origin and duplication timing to assign an evolutionary age to each gene. Subsequent analysis of the sets of genes that changed expression revealed a relationship between stress-induced genes and the youngest gene set, regardless of the species or stress in question. These young genes are rarely essential for growth and evolve rapidly, which may facilitate their functionalization for stress tolerance and may explain their stress-induced expression. These findings show that systems-level analyses that consider gene age can expedite the identification of stress tolerance genes.