Introns regulate RNA and protein abundance in yeast

Abstract

The purpose of introns in the architecturally simple genome of Saccharomyces cerevisiae is not well understood. To assay the functional relevance of introns, a series of computational analyses and several detailed deletion studies were completed on the intronic genes of S. cerevisiae. Mining existing data from genomewide studies on yeast revealed that intron-containing genes produce more RNA and more protein and are more likely to be haplo-insufficient than nonintronic genes. These observations for all intronic genes held true for distinct subsets of genes including ribosomal, nonribosomal, duplicated, and nonduplicated. Corroborating the result of computational analyses, deletion of introns from three essential genes decreased cellular RNA levels and caused measurable growth defects. These data provide evidence that introns improve transcriptional and translational yield and are required for competitive growth of yeast.

Figure 1.—

Intronic genes are highly expressed. (A) RNA abundance; (B) protein abundance. The abundance (log₂) of intronic genes (blue) and nonintronic genes (red) is shown. The Density (y-axis) corresponds to the relative number of genes at a given abundance (the distribution is smoothed with a Gaussian kernel). The protein abundance data were from Ghaemmaghami et al. (2003) and the RNA abundance data were from Deutschbauer et al. (2005). Genes containing introns (blue) are more highly expressed at both the protein and the RNA levels.

Figure 2.—

Deletion of introns results in a drug-induced fitness defect for both act1 and glc7. The x-axes denote time in hours; the y-axes denote optical density (OD) of the cell cultures. Top, growth of wild-type diploids (red) vs. glc7Δi/glc7Δi (black). Bottom, growth of wild-type diploids (red) vs. act1Δi/act1Δi (black). Left, untreated YPD media. Right, YPD media plus drug. glc7 experimental cultures contained 10 μm cantharidin, and act1 experimental cultures contained 3.34 μm latrunculin. The doubling time of each strain is expressed in hours and appears color coded under corresponding curves.