Hsp90 and physiological stress are linked to autonomous transposon mobility and heritable genetic change in nematodes

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Author(s)
Ryan, Calen P.
Brownlie, Jeremy
Whyard, Steve
Griffith University Author(s)
Year published
2016
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Transposable elements (TEs) have been recognized as potentially powerful drivers of genomic evolutionary change, but
factors affecting their mobility and regulation remain poorly understood. Chaperones such as Hsp90 buffer environmental
perturbations by regulating protein conformation, but are also part of the PIWI-interacting RNA pathway, which regulates
genomic instability arising frommobile TEs in the germline. Stress-induced mutagenesis from TEmovement could thus arise
from functional trade-offs in the dual roles of Hsp90. We examined the functional constraints of Hsp90 and its role as a
regulator of TE mobility by ...
View more >Transposable elements (TEs) have been recognized as potentially powerful drivers of genomic evolutionary change, but factors affecting their mobility and regulation remain poorly understood. Chaperones such as Hsp90 buffer environmental perturbations by regulating protein conformation, but are also part of the PIWI-interacting RNA pathway, which regulates genomic instability arising frommobile TEs in the germline. Stress-induced mutagenesis from TEmovement could thus arise from functional trade-offs in the dual roles of Hsp90. We examined the functional constraints of Hsp90 and its role as a regulator of TE mobility by exposing nematodes (Caenorhabditis elegans and Caenorhabditis briggsae) to environmental stress, with and without RNAi-induced silencing of Hsp90. TE excision frequency increased with environmental stress intensity at multiple loci in several strains of each species. These effectswere compounded by RNAi-induced knockdown of Hsp90. Mutation frequencies at the unc-22 marker gene in the offspring of animals exposed to environmental stress and Hsp90 RNAi mirrored excision frequency in response to these treatments. Our results support a role for Hsp90 in the suppression of TE mobility, and demonstrate that that the Hsp90 regulatory pathway can be overwhelmed with moderate environmental stress. By compromising genomic stability in germline cells, environmentally induced mutations arising from TEmobility and insertion can have permanent and heritable effects on both the phenotype and the genotype of subsequent generations.
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View more >Transposable elements (TEs) have been recognized as potentially powerful drivers of genomic evolutionary change, but factors affecting their mobility and regulation remain poorly understood. Chaperones such as Hsp90 buffer environmental perturbations by regulating protein conformation, but are also part of the PIWI-interacting RNA pathway, which regulates genomic instability arising frommobile TEs in the germline. Stress-induced mutagenesis from TEmovement could thus arise from functional trade-offs in the dual roles of Hsp90. We examined the functional constraints of Hsp90 and its role as a regulator of TE mobility by exposing nematodes (Caenorhabditis elegans and Caenorhabditis briggsae) to environmental stress, with and without RNAi-induced silencing of Hsp90. TE excision frequency increased with environmental stress intensity at multiple loci in several strains of each species. These effectswere compounded by RNAi-induced knockdown of Hsp90. Mutation frequencies at the unc-22 marker gene in the offspring of animals exposed to environmental stress and Hsp90 RNAi mirrored excision frequency in response to these treatments. Our results support a role for Hsp90 in the suppression of TE mobility, and demonstrate that that the Hsp90 regulatory pathway can be overwhelmed with moderate environmental stress. By compromising genomic stability in germline cells, environmentally induced mutations arising from TEmobility and insertion can have permanent and heritable effects on both the phenotype and the genotype of subsequent generations.
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Journal Title
Genome Biology and Evolution
Volume
8
Issue
12
Copyright Statement
© The Author(s) 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits
non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Subject
Evolutionary Biology not elsewhere classified
Biochemistry and Cell Biology
Evolutionary Biology
Genetics