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Origins, evolution, and physiological implications of de novo genes in yeast - PubMed

Review

. 2022 Sep;39(9):471-481.

doi: 10.1002/yea.3810. Epub 2022 Aug 24.

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Review

Origins, evolution, and physiological implications of de novo genes in yeast

Saurin B Parikh et al. Yeast. 2022 Sep.

Abstract

De novo gene birth is the process by which new genes emerge in sequences that were previously noncoding. Over the past decade, researchers have taken advantage of the power of yeast as a model and a tool to study the evolutionary mechanisms and physiological implications of de novo gene birth. We summarize the mechanisms that have been proposed to explicate how noncoding sequences can become protein-coding genes, highlighting the discovery of pervasive translation of the yeast transcriptome and its presumed impact on evolutionary innovation. We summarize current best practices for the identification and characterization of de novo genes. Crucially, we explain that the field is still in its nascency, with the physiological roles of most young yeast de novo genes identified thus far still utterly unknown. We hope this review inspires researchers to investigate the true contribution of de novo gene birth to cellular physiology and phenotypic diversity across yeast strains and species.

Keywords: de novo genes; evolutionary biology; genome biology; smORFs; systems biology.

© 2022 The Authors. Yeast published by John Wiley & Sons Ltd.

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Conflict of interest statement

Anne‐Ruxandra Carvunis is a member of the scientific advisory board for Flagship Labs 69 Inc. (ProFound Therapeutics).

Figures

Figure 1
Figure 1

MDF1: A de novo‐evolved gene that integrates into essential biological pathways. (a) Phylogeny‐ and synteny‐based analysis of various fungi revealed that MDF1 emerged specifically in S. cer subsequent to its split from S. cas. At the same time, ADF1, an antisense gene to MDF1, is conserved in all but the most distant member of the hemiascomycete subdivision of fungi. The MDF1 syntenic block is shown to the right of the phylogenetic tree. (Li et al., 2010) (b) Mdf1 promotes vegetative growth by suppressing the mating pathway and enhancing the glucose signaling pathway (Li et al., 2014). A. gos, Ashbya gossypii; C. alb, Candida albicans; C. gla, Candida glabrata; S. cas, Saccharomyces castellii; S. cer, Saccharomyces cerevisiae; S. pom, Schizosaccharomyces pombe; Y. lip, Yarrowia lipolytica.

Figure 2
Figure 2

Pictographic representation of a hypothetical de novo ORF in Saccharomyces cerevisiae. (a) A combination of conserved synteny and phylostratigraphy is used to identify the homologous region of interest (highlighted in yellow) in the closely related species. This region of interest can be used to identify enabling mutations across the lineage that led to the de novo ORF in the focal species (S. cerevisiae in this case). The enabling mutations can include but are not limited to a gain of the start codon (green star), loss of premature stop codon (gray star), insertion–deletion and/or a frameshift (pink star) and a gain of stop codon (red star). Figure inspired by Vakirlis and McLysaght (2019). (b) A hypothetical example of enabling mutations that occurred along the lineage to result in a de novo ORF in the focal genome. Changes highlighted within boxes are possible enablers. Identification of one or more of such mutations (example gain of the start codon) are needed to provide convincing evidence of de novo ORF emergence. ORF, open reading frame; S. cer, Saccharomyces cerevisiae; S. mik, Saccharomyces mikatae; S. par, Saccharomyces paradoxus.

Figure 3
Figure 3

Evolutionary systems biology approach for characterizing the biological role of a candidate de novo gene. The framework proposes a combination of evolutionary and molecular approaches that may be used to identify and investigate a candidate de novo gene. Insights drawn from these varied approaches can then be put together to provide a holistic understanding of the ORF's biology. Overall, this framework represents a circular continuum that is under the influence of natural selection. ORF, open reading frame.

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