The Phenotypic Plasticity of Duplicated Genes in<i>Saccharomyces cerevisiae</i>and the Origin of Adaptations

Mattenberger, Florian; Sabater-Muñoz, Beatriz; Toft, Christina; Fares, Mario A.

doi:10.1534/g3.116.035329

Cited by 36 publications

(30 citation statements)

References 87 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Deciphering the physiological significance of the RPG regulon of S . cerevisiae may contribute toward our understanding of how the underlying framework of the genome is used in evolutionary adaptations [ 83 ]. The selection of strains that best respond to the contradictory challenges of stressors and nutrients is perhaps the reason for the high retention rate of paralogs among yeast RPGs [ 3 , 84 ].…”

Section: Discussionmentioning

confidence: 99%

Introns provide a platform for intergenic regulatory feedback of RPL22 paralogs in yeast

et al. 2018

View full text Add to dashboard Cite

Ribosomal protein genes (RPGs) in Saccharomyces cerevisiae are a remarkable regulatory group that may serve as a model for understanding genetic redundancy in evolutionary adaptations. Most RPGs exist as pairs of highly conserved functional paralogs with divergent untranslated regions and introns. We examined the roles of introns in strains with various combinations of intron and gene deletions in RPL22, RPL2, RPL16, RPL37, RPL17, RPS0, and RPS18 paralog pairs. We found that introns inhibited the expression of their genes in the RPL22 pair, with the RPL22B intron conferring a much stronger effect. While the WT RPL22A/RPL22B mRNA ratio was 93/7, the rpl22aΔi/RPL22B and RPL22A/rpl22bΔi ratios were >99/<1 and 60/40, respectively. The intron in RPL2A stimulated the expression of its own gene, but the removal of the other introns had little effect on expression of the corresponding gene pair. Rpl22 protein abundances corresponded to changes in mRNAs.Using splicing reporters containing endogenous intron sequences, we demonstrated that these effects were due to the inhibition of splicing by Rpl22 proteins but not by their RNA-binding mutant versions. Indeed, only WT Rpl22A/Rpl22B proteins (but not the mutants) interacted in a yeast three-hybrid system with an RPL22B intronic region between bp 165 and 236. Transcriptome analysis showed that both the total level of Rpl22 and the A/B ratio were important for maintaining the WT phenotype. The data presented here support the contention that the Rpl22B protein has a paralog-specific role.The RPL22 singleton of Kluyveromyces lactis, which did not undergo whole genome duplication, also responded to Rpl22-mediated inhibition in K. lactis cells. Vice versa, the overproduction of the K. lactis protein reduced the expression of RPL22A/B in S. cerevisiae. The extraribosomal function of of the K. lactis Rpl22 suggests that the loop regulating RPL22 paralogs of S. cerevisiae evolved from autoregulation.

show abstract

Section: Discussionmentioning

confidence: 99%

Introns provide a platform for intergenic regulatory feedback of RPL22 paralogs in yeast

et al. 2018

View full text Add to dashboard Cite

show abstract

“…The RNA profiling was performed at the t 0 , t 100 , and t 110 time points as indicated in Fig. 1A, following the same procedures as previously used (22,72). rRNA-depleted RNA (Illumina) libraries were constructed and sequenced at the Genomic Core Facility at Servicio Central de Soporte a la Investigacion Experimental (SCSIE) from the University of Valencia, Spain.…”

Section: Methodsmentioning

confidence: 99%

Transcriptional Rewiring, Adaptation, and the Role of Gene Duplication in the Metabolism of Ethanol of Saccharomyces cerevisiae

et al. 2020

Self Cite

View full text Add to dashboard Cite

Ethanol is the main by-product of yeast sugar fermentation that affects microbial growth parameters, being considered a dual molecule, a nutrient and a stressor. Previous works demonstrated that the budding yeast arose after an ancient hybridization process resulted in a tier of duplicated genes within its genome, many of them with implications in this ethanol “produce-accumulate-consume” strategy. The evolutionary link between ethanol production, consumption, and tolerance versus ploidy and stability of the hybrids is an ongoing debatable issue. The implication of ancestral duplicates in this metabolic rewiring, and how these duplicates differ transcriptionally, remains unsolved. Here, we study the transcriptomic adaptive signatures to ethanol as a nonfermentative carbon source to sustain clonal yeast growth by experimental evolution, emphasizing the role of duplicated genes in the adaptive process. As expected, ethanol was able to sustain growth but at a lower rate than glucose. Our results demonstrate that in asexual populations a complete transcriptomic rewiring was produced, strikingly by downregulation of duplicated genes, mainly whole-genome duplicates, whereas small-scale duplicates exhibited significant transcriptional divergence between copies. Overall, this study contributes to the understanding of evolution after gene duplication, linking transcriptional divergence with duplicates’ fate in a multigene trait as ethanol tolerance. IMPORTANCE Gene duplication events have been related with increasing biological complexity through the tree of life, but also with illnesses, including cancer. Early evolutionary theories indicated that duplicated genes could explore alternative functions due to relaxation of selective constraints in one of the copies, as the other remains as ancestral-function backup. In unicellular eukaryotes like yeasts, it has been demonstrated that the fate and persistence of duplicates depend on duplication mechanism (whole-genome or small-scale events), shaping their actual genomes. Although it has been shown that small-scale duplicates tend to innovate and whole-genome duplicates specialize in ancestral functions, the implication of duplicates’ transcriptional plasticity and transcriptional divergence on environmental and metabolic responses remains largely obscure. Here, by experimental adaptive evolution, we show that Saccharomyces cerevisiae is able to respond to metabolic stress (ethanol as nonfermentative carbon source) due to the persistence of duplicated genes. These duplicates respond by transcriptional rewiring, depending on their transcriptional background. Our results shed light on the mechanisms that determine the role of duplicates, and on their evolvability.

show abstract

“…The aspects of NGE activity on cellular genomes that facilitate the positive adaptations detailed above include active nucleotide sequence modification ( Table 15 ), the capacity for both homologous and non-homologous DNA exchanges, interactions with viral genomes, the presence of mobile DNA elements, and the formation of genome duplications [ 325 , 700 , 701 , 702 , 703 , 704 , 705 , 706 , 707 ]. In prokaryotes, the most numerous organisms in the biosphere, mobile DNA, includes transmissible plasmids and other conjugative elements.…”

Section: Further Reflections On Genome Rewriting By Nge As a Core mentioning

confidence: 99%

Living Organisms Author Their Read-Write Genomes in Evolution

Shapiro

2017

Biology

View full text Add to dashboard Cite

Evolutionary variations generating phenotypic adaptations and novel taxa resulted from complex cellular activities altering genome content and expression: (i) Symbiogenetic cell mergers producing the mitochondrion-bearing ancestor of eukaryotes and chloroplast-bearing ancestors of photosynthetic eukaryotes; (ii) interspecific hybridizations and genome doublings generating new species and adaptive radiations of higher plants and animals; and, (iii) interspecific horizontal DNA transfer encoding virtually all of the cellular functions between organisms and their viruses in all domains of life. Consequently, assuming that evolutionary processes occur in isolated genomes of individual species has become an unrealistic abstraction. Adaptive variations also involved natural genetic engineering of mobile DNA elements to rewire regulatory networks. In the most highly evolved organisms, biological complexity scales with “non-coding” DNA content more closely than with protein-coding capacity. Coincidentally, we have learned how so-called “non-coding” RNAs that are rich in repetitive mobile DNA sequences are key regulators of complex phenotypes. Both biotic and abiotic ecological challenges serve as triggers for episodes of elevated genome change. The intersections of cell activities, biosphere interactions, horizontal DNA transfers, and non-random Read-Write genome modifications by natural genetic engineering provide a rich molecular and biological foundation for understanding how ecological disruptions can stimulate productive, often abrupt, evolutionary transformations.

show abstract

The Phenotypic Plasticity of Duplicated Genes inSaccharomyces cerevisiaeand the Origin of Adaptations

Cited by 36 publications

References 87 publications

Introns provide a platform for intergenic regulatory feedback of RPL22 paralogs in yeast

Introns provide a platform for intergenic regulatory feedback of RPL22 paralogs in yeast

Transcriptional Rewiring, Adaptation, and the Role of Gene Duplication in the Metabolism of Ethanol of Saccharomyces cerevisiae

Living Organisms Author Their Read-Write Genomes in Evolution

Contact Info

Product

Resources

About