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Mol Biol Evol. 2016 Jul;33(7):1679-96. doi: 10.1093/molbev/msw045. Epub 2016 Feb 28.

Widespread Impact of Chromosomal Inversions on Gene Expression Uncovers Robustness via Phenotypic Buffering.

Author information

1
Computational and Evolutionary Biology Research Theme, Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom.
2
Computational and Evolutionary Biology Research Theme, Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom d.delneri@manchester.ac.uk.

Abstract

The nonrandom gene organization in eukaryotes plays a significant role in genome evolution and function. Chromosomal structural changes impact meiotic fitness and, in several organisms, are associated with speciation and rapid adaptation to different environments. Small sized chromosomal inversions, encompassing few genes, are pervasive in Saccharomyces "sensu stricto" species, while larger inversions are less common in yeasts compared with higher eukaryotes. To explore the effect of gene order on phenotype, reproductive isolation, and gene expression, we engineered 16 Saccharomyces cerevisiae strains carrying all possible paracentric and pericentric inversions between Ty1 elements, a natural substrate for rearrangements. We found that 4 inversions were lethal, while the other 12 did not show any fitness advantage or disadvantage in rich and minimal media. At meiosis, only a weak negative correlation with fitness was seen with the size of the inverted region. However, significantly lower fertility was seen in heterozygote invertant strains carrying recombination hotspots within the breakpoints. Altered transcription was observed throughout the genome rather than being overrepresented within the inversions. In spite of the large difference in gene expression in the inverted strains, mitotic fitness was not impaired in the majority of the 94 conditions tested, indicating that the robustness of the expression network buffers the deleterious effects of structural changes in several environments. Overall, our results support the notion that transcriptional changes may compensate for Ty-mediated rearrangements resulting in the maintenance of a constant phenotype, and suggest that large inversions in yeast are unlikely to be a selectable trait during vegetative growth.

KEYWORDS:

Saccharomyces cerevisiae.; fitness; genome organisation; inversions

PMID:
26929245
PMCID:
PMC4915352
DOI:
10.1093/molbev/msw045
[Indexed for MEDLINE]
Free PMC Article

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