Extreme positive epistasis for fitness in monosomic yeast strains
- Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Poland
- Doctoral School of Exact and Natural Sciences, Jagiellonian University, Poland
Figures
Figure 1
Diploid yeast strains lacking single chromosomes (monosomics).
(A) Representative colonies of wild-type diploid (WT) and monosomic mutant strains (M1...M16) when grown together for 24 hr at 30°C on agar-solidified YPD medium. (B) DNA whole-genome sequencing coverage. (C) Examples of large colonies emerging among the small monosomic ones.
Figure 2
Contribution of positive epistasis to fitness of monosomics.
(A) Growth performance of heterozygous single-gene deletion strains tested in this study. Left: list of chromosomes with numbers of assayed deletion strains. Right: frequency distribution of rDR (doubling rate related to that of the control). (B) Growth performance of monosomics. Colored bars represent expected performance calculated as a sum of the single-gene effects per chromosome, rDRE = 1 + ∑di, where di = rDRi−1 (deviation from the control). Gray bars show the observed performance of monosomic strains, rDRM. White arrows mark the expected departure from wild-type fitness (expected genetic load), gray the observed one. Black arrows show the extent and direction of epistasis. Three monosomics were not included in these assays (see the main text).
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Figure 2—source data 1
Relative doubling rates of individual heterozygous deletion strains and monosomic strains related to Figure 2A and B.
- https://cdn.elifesciences.org/articles/87455/elife-87455-fig2-data1-v1.xlsx
Figure 3
Absence of transcriptional compensation in monosomic strains.
(A) Halved RNA production on monosomic chromosomes. For every open reading frame (ORF), the obtained number of RNA-seq reads was divided by the number expected for it under expression being constant over an entire genome. (B) Expression under monosomy vs. single-deletion fitness (rDR). X-axis shows the length of a monosomic chromosome with centromeres marked as circles and gene deletions as bars; colors show the effect of monosomy on the level of a particular mRNA with a particular color showing a range of log2 fold change (FC) relative to the control. Y-axis: the difference in rDR between a single-gene deletion strain and the control, d = rDR − 1. The correlation between fitness effect (rDR − 1) and shift in expression (log2FC) is reported as Spearman’s coefficient rs with associated and p-value (not corrected for the multiplicity of comparisons).
Figure 4 with 1 supplement
Parallel and divergent shifts in transcriptomes of monosomic strains.
Heat maps show monosomic mRNA frequencies divided by respective diploid (control) ones. (A) Gene Ontology categories selected to demonstrate similarities in transcriptional profiles of monosomic strains. (B) Regulons demonstrating differences in gene expression between monosomic strains. Expanded versions of all panels can be found in Figure 4—figure supplement 1.
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Figure 4—source data 1
Differential gene expression in monosomic strains related to Figures 3B and 4A, B.
- https://cdn.elifesciences.org/articles/87455/elife-87455-fig4-data1-v1.xlsx
Figure 4—figure supplement 1
Parallel and divergent shifts in transcriptomes of monosomic strains.
Heat maps show monosomic mRNA frequencies divided by respective diploid (control) ones. (A) Gene Ontology categories selected to demonstrate similarities in transcriptional profiles of monosomic strains. (B) Regulons demonstrating differences in gene expression between monosomic strains.
Figure 5
Correlation of counts of individual mRNAs between wild-type and monosomic strains.
Counts are expressed as fractions of either wild-type BY or monosomic M1, M2, and M3 total transcriptomes. Gray circles represent mRNAs from the unaffected 15 chromosomes and group around the diagonal. Blue represent spike mRNAs. Red circles represent mRNAs from the monosomic chromosomes (I, II, or III in the respective graphs). Note that the monosomic counts are, as expected, underrepresented in the respective monosomic strains (red circles are below the diagonal). Monosomic counts of spike are higher than that of BY (blue circles are above the diagonal). As reported in the main text, the total fraction of spike counts in BY is 4.04%. Analogous sums for M1, M2, and M3 are 6.08, 15.6, and 24.2%. This can be seen here as an increasing distance between the gray and blue circles.
Appendix 1—figure 1
DNA whole-genome sequencing coverage after the postulated endoreduplication.
Two isolates descending from the parental diploid strains with marked chromosomes VII or XIII are shown. They were subjected to sequencing after being found to lack phenotypic markers and produce four viable spores.
Tables
Table 1
Yeast Slim GO Biological Process categories of the tested deletions and the predicted and observed relative doubling rate of the monosomic strains.
| Monosomic strain | M1 | M2 | M3 | M8 | M10 | M11 | M14 | M16 |
|---|---|---|---|---|---|---|---|---|
| Subsets of deletions mapping to chromosomes | ||||||||
| Number of GO Slim Biological Process categories | 25 | 47 | 11 | 27 | 39 | 33 | 34 | 57 |
| Number of unique genes | 6 | 40 | 11 | 20 | 31 | 19 | 24 | 41 |
| Number of genes affecting categories constituting PSA (protein synthesis apparatus): | ||||||||
| rRNA processing | 1 | 5 | 3 | 7 | 4 | 5 | 8 | 11 |
| Ribosome large subunit biogenesis | 1 | 1 | 4 | 6 | 7 | |||
| Ribosome small subunit biogenesis | 1 | 4 | 2 | 4 | 3 | 1 | 2 | 5 |
| Ribosomal assembly | 1 | 1 | 1 | 1 | 2 | 1 | 2 | |
| Ribosome subunit export from nucleus | 1 | 2 | 3 | 2 | 4 | |||
| Cytoplasmic translation | 1 | 9 | 5 | 4 | 5 | 3 | 5 | |
| Translational initiation | 1 | 2 | ||||||
| Regulation of translation | 2 | 2 | ||||||
| Total number of unique PSA genes | 1 | 13 | 5 | 8 | 10 | 7 | 12 | 14 |
| Relative doubling rate (rDR) | ||||||||
| Predicted from the total load of deletions (Figure 2B) | 0.85 | –0.95 | 0.66 | 0.27 | –0.82 | –0.33 | –0.04 | –1.52 |
| Predicted from the PSA deletions | 0.95 | 0.37 | 0.78 | 0.63 | 0.22 | 0.49 | 0.22 | –0.07 |
| Observed in monosomic strains | 0.96 | 0.60 | 0.63 | 0.61 | 0.49 | 0.60 | 0.63 | 0.58 |
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Extreme positive epistasis for fitness in monosomic yeast strains
eLife 12:RP87455.
https://doi.org/10.7554/eLife.87455.3
