Loss-of-function mutation survey revealed that genes with background-dependent fitness are rare and functionally related in yeast.

In natural populations, the same mutation can lead to different phenotypic outcomes due to the genetic variation that exists among individuals. Such genetic background effects are commonly observed, including in the context of many human diseases. However, systematic characterization of these effects at the species level is still lacking to date. Here, we sought to comprehensively survey background-dependent traits associated with gene loss-of-function (LoF) mutations in 39 natural isolates of Saccharomyces cerevisiae using a transposon saturation strategy. By analyzing the modeled fitness variability of a total of 4,469 genes, we found that 15% of them, when impacted by a LoF mutation, exhibited a significant gain- or loss-of-fitness phenotype in certain natural isolates compared with the reference strain S288C. Out of these 632 genes with predicted background-dependent fitness effects, around 2/3 impact multiple backgrounds with a gradient of predicted fitness change while 1/3 are specific to a single genetic background. Genes related to mitochondrial function are significantly overrepresented in the set of genes showing a continuous variation and display a potential functional rewiring with other genes involved in transcription and chromatin remodeling as well as in nuclear-cytoplasmic transport. Such rewiring effects are likely modulated by both the genetic background and the environment. While background-specific cases are rare and span diverse cellular processes, they can be functionally related at the individual level. All genes with background-dependent fitness effects tend to have an intermediate connectivity in the global genetic interaction network and have shown relaxed selection pressure at the population level, highlighting their potential evolutionary characteristics.

Impact of the acquired subgenome on the transcriptional landscape in Brettanomyces bruxellensis allopolyploids.

Gene expression variation can provide an overview of the changes in regulatory networks that underlie phenotypic diversity. Certain evolutionary trajectories such as polyploidization events can have an impact on the transcriptional landscape. Interestingly, the evolution of the yeast species Brettanomyces bruxellensis has been punctuated by diverse allopolyploidization events leading to the coexistence of a primary diploid genome associated with various haploid acquired genomes. To assess the impact of these events on gene expression, we generated and compared the transcriptomes of a set of 87 B. bruxellensis isolates, selected as being representative of the genomic diversity of this species. Our analysis revealed that acquired subgenomes strongly impact the transcriptional patterns and allow discrimination of allopolyploid populations. In addition, clear transcriptional signatures related to specific populations have been revealed. The transcriptional variations observed are related to some specific biological processes such as transmembrane transport and amino acids metabolism. Moreover, we also found that the acquired subgenome causes the overexpression of some genes involved in the production of flavor-impacting secondary metabolites, especially in isolates of the beer population.

Evolution and Plasticity of the Transcriptome Under Temperature Fluctuations in the Fungal Plant Pathogen Zymoseptoria tritici.

Most species live in a variable environment in nature. Yet understanding the evolutionary processes underlying molecular adaptation to fluctuations remains a challenge. In this study we investigate the transcriptome of the fungal wheat pathogen Zymoseptoria tritici after experimental evolution under stable or fluctuating temperature, by comparing ancestral and evolved populations simultaneously. We found that temperature regimes could have a large and pervasive effect on the transcriptome evolution, with as much as 38% of the genes being differentially expressed between selection regimes. Although evolved lineages showed different changes of gene expression based on ancestral genotypes, we identified a set of genes responding specifically to fluctuation. We found that transcriptome evolution in fluctuating conditions was repeatable between parallel lineages initiated from the same genotype for about 60% of the differentially expressed genes. Further, we detected several hotspots of significantly differentially expressed genes in the genome, in regions known to be enriched in repetitive elements, including accessory chromosomes. Our findings also evidenced gene expression evolution toward a gain of robustness (loss of phenotypic plasticity) associated with the fluctuating regime, suggesting robustness is adaptive in changing environment. This work provides valuable insight into the role of transcriptional rewiring for rapid adaptation to abiotic changes in filamentous plant pathogens.