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Starvation-associated genome restructuring can lead to reproductive isolation in yeast.

Kroll E, Coyle S, Dunn B, Koniges G, Aragon A, Edwards J, Rosenzweig F - PLoS ONE (2013)

Bottom Line: By contrast, the frequency of point mutations is less than 2-fold greater.In a particular case, we observe that a starved lineage becomes reproductively isolated as a direct result of the stress-related accumulation of a single chromosome.We recapitulate this result by demonstrating that introducing an extra copy of one or several chromosomes into naïve, i.e. unstarved, yeast significantly diminishes their fertility.

View Article: PubMed Central - PubMed

Affiliation: Division of Biological Sciences, University of Montana, Missoula, Montana, United States of America. evgueny.kroll@mso.umt.edu

ABSTRACT
Knowledge of the mechanisms that lead to reproductive isolation is essential for understanding population structure and speciation. While several models have been advanced to explain post-mating reproductive isolation, experimental data supporting most are indirect. Laboratory investigations of this phenomenon are typically carried out under benign conditions, which result in low rates of genetic change unlikely to initiate reproductive isolation. Previously, we described an experimental system using the yeast Saccharomyces cerevisiae where starvation served as a proxy to any stress that decreases reproduction and/or survivorship. We showed that novel lineages with restructured genomes quickly emerged in starved populations, and that these survivors were more fit than their ancestors when re-starved. Here we show that certain yeast lineages that survive starvation have become reproductively isolated from their ancestor. We further demonstrate that reproductive isolation arises from genomic rearrangements, whose frequency in starving yeast is several orders of magnitude greater than an unstarved control. By contrast, the frequency of point mutations is less than 2-fold greater. In a particular case, we observe that a starved lineage becomes reproductively isolated as a direct result of the stress-related accumulation of a single chromosome. We recapitulate this result by demonstrating that introducing an extra copy of one or several chromosomes into naïve, i.e. unstarved, yeast significantly diminishes their fertility. This type of reproductive barrier, whether arising spontaneously or via genetic manipulation, can be removed by making a lineage euploid for the altered chromosomes. Our model provides direct genetic evidence that reproductive isolation can arise frequently in stressed populations via genome restructuring without the precondition of geographic isolation.

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Extra chromosomes decrease (A) sporulation frequency and (B) spore viability, which are cured by tetraploidization to different extents (see text).Light grey, 2N – diploid strain and its derivatives containing one or several supernumerary chromosomes, as indicated. Dark grey, 4N – tetraploid derivatives. Error bars are 95% Wilson's binomial CI.
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pone-0066414-g005: Extra chromosomes decrease (A) sporulation frequency and (B) spore viability, which are cured by tetraploidization to different extents (see text).Light grey, 2N – diploid strain and its derivatives containing one or several supernumerary chromosomes, as indicated. Dark grey, 4N – tetraploid derivatives. Error bars are 95% Wilson's binomial CI.

Mentions: Diploid strains bearing one or several extra chromosomes also exhibited lower sporulation frequencies (in all trisomics vs. diploid control, p<0.0005, Bonferroni-corrected Fisher's exact test) (Fig. 5A). Interestingly, spore viability in the diploid trisomics ranged from 10% to 53%, which was markedly lower than that of the euploid control strain, a statistically significant association (p<0.01 for all four cases, Bonferroni-corrected Fisher's exact test) (Fig. 5B). These experimental results suggest that several unbalanced chromosomes besides Chromosome I can disrupt meiosis in diploid trisomics.


Starvation-associated genome restructuring can lead to reproductive isolation in yeast.

Kroll E, Coyle S, Dunn B, Koniges G, Aragon A, Edwards J, Rosenzweig F - PLoS ONE (2013)

Extra chromosomes decrease (A) sporulation frequency and (B) spore viability, which are cured by tetraploidization to different extents (see text).Light grey, 2N – diploid strain and its derivatives containing one or several supernumerary chromosomes, as indicated. Dark grey, 4N – tetraploid derivatives. Error bars are 95% Wilson's binomial CI.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3722211&req=5

pone-0066414-g005: Extra chromosomes decrease (A) sporulation frequency and (B) spore viability, which are cured by tetraploidization to different extents (see text).Light grey, 2N – diploid strain and its derivatives containing one or several supernumerary chromosomes, as indicated. Dark grey, 4N – tetraploid derivatives. Error bars are 95% Wilson's binomial CI.
Mentions: Diploid strains bearing one or several extra chromosomes also exhibited lower sporulation frequencies (in all trisomics vs. diploid control, p<0.0005, Bonferroni-corrected Fisher's exact test) (Fig. 5A). Interestingly, spore viability in the diploid trisomics ranged from 10% to 53%, which was markedly lower than that of the euploid control strain, a statistically significant association (p<0.01 for all four cases, Bonferroni-corrected Fisher's exact test) (Fig. 5B). These experimental results suggest that several unbalanced chromosomes besides Chromosome I can disrupt meiosis in diploid trisomics.

Bottom Line: By contrast, the frequency of point mutations is less than 2-fold greater.In a particular case, we observe that a starved lineage becomes reproductively isolated as a direct result of the stress-related accumulation of a single chromosome.We recapitulate this result by demonstrating that introducing an extra copy of one or several chromosomes into naïve, i.e. unstarved, yeast significantly diminishes their fertility.

View Article: PubMed Central - PubMed

Affiliation: Division of Biological Sciences, University of Montana, Missoula, Montana, United States of America. evgueny.kroll@mso.umt.edu

ABSTRACT
Knowledge of the mechanisms that lead to reproductive isolation is essential for understanding population structure and speciation. While several models have been advanced to explain post-mating reproductive isolation, experimental data supporting most are indirect. Laboratory investigations of this phenomenon are typically carried out under benign conditions, which result in low rates of genetic change unlikely to initiate reproductive isolation. Previously, we described an experimental system using the yeast Saccharomyces cerevisiae where starvation served as a proxy to any stress that decreases reproduction and/or survivorship. We showed that novel lineages with restructured genomes quickly emerged in starved populations, and that these survivors were more fit than their ancestors when re-starved. Here we show that certain yeast lineages that survive starvation have become reproductively isolated from their ancestor. We further demonstrate that reproductive isolation arises from genomic rearrangements, whose frequency in starving yeast is several orders of magnitude greater than an unstarved control. By contrast, the frequency of point mutations is less than 2-fold greater. In a particular case, we observe that a starved lineage becomes reproductively isolated as a direct result of the stress-related accumulation of a single chromosome. We recapitulate this result by demonstrating that introducing an extra copy of one or several chromosomes into naïve, i.e. unstarved, yeast significantly diminishes their fertility. This type of reproductive barrier, whether arising spontaneously or via genetic manipulation, can be removed by making a lineage euploid for the altered chromosomes. Our model provides direct genetic evidence that reproductive isolation can arise frequently in stressed populations via genome restructuring without the precondition of geographic isolation.

Show MeSH
Related in: MedlinePlus