Contribution of trans regulatory eQTL to cryptic genetic variation in C. elegans

Basten L. Snoek, Mark G. Sterken, Roel P.J. Bevers, Rita J.M. Volkers, Arjen van 't Hof, Rachel Brenchley, Joost A.G. Riksen, Andrew Cossins, Jan E. Kammenga

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Abstract


Background

Cryptic genetic variation (CGV) is the hidden genetic variation that can be unlocked by perturbing normal conditions. CGV can drive the emergence of novel complex phenotypes through changes in gene expression. Although our theoretical understanding of CGV has thoroughly increased over the past decade, insight into polymorphic gene expression regulation underlying CGV is scarce. Here we investigated the transcriptional architecture of CGV in response to rapid temperature changes in the nematode Caenorhabditis elegans. We analyzed regulatory variation in gene expression (and mapped eQTL) across the course of a heat stress and recovery response in a recombinant inbred population.


Results

We measured gene expression over three temperature treatments: i) control, ii) heat stress, and iii) recovery from heat stress. Compared to control, exposure to heat stress affected the transcription of 3305 genes, whereas 942 were affected in recovering animals. These affected genes were mainly involved in metabolism and reproduction. The gene expression pattern in recovering animals resembled both the control and the heat-stress treatment. We mapped eQTL using the genetic variation of the recombinant inbred population and detected 2626 genes with an eQTL in the heat-stress treatment, 1797 in the control, and 1880 in the recovery. The cis-eQTL were highly shared across treatments. A considerable fraction of the trans-eQTL (40–57%) mapped to 19 treatment specific trans-bands. In contrast to cis-eQTL, trans-eQTL were highly environment specific and thus cryptic. Approximately 67% of the trans-eQTL were only induced in a single treatment, with heat-stress showing the most unique trans-eQTL.


Conclusions

These results illustrate the highly dynamic pattern of CGV across three different environmental conditions that can be evoked by a stress response over a relatively short time-span (2 h) and that CGV is mainly determined by response related trans regulatory eQTL.
Original languageEnglish
Article number500
Number of pages15
JournalBMC Genomics
Volume18
DOIs
Publication statusPublished - 2017

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Hot Temperature
Gene Expression
Genes
Heat-Shock Response
Temperature
Caenorhabditis elegans
Gene Expression Regulation
Population
Reproduction
Phenotype

Cite this

Snoek, Basten L. ; Sterken, Mark G. ; Bevers, Roel P.J. ; Volkers, Rita J.M. ; van 't Hof, Arjen ; Brenchley, Rachel ; Riksen, Joost A.G. ; Cossins, Andrew ; Kammenga, Jan E. / Contribution of trans regulatory eQTL to cryptic genetic variation in C. elegans. In: BMC Genomics. 2017 ; Vol. 18.
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title = "Contribution of trans regulatory eQTL to cryptic genetic variation in C. elegans",
abstract = "BackgroundCryptic genetic variation (CGV) is the hidden genetic variation that can be unlocked by perturbing normal conditions. CGV can drive the emergence of novel complex phenotypes through changes in gene expression. Although our theoretical understanding of CGV has thoroughly increased over the past decade, insight into polymorphic gene expression regulation underlying CGV is scarce. Here we investigated the transcriptional architecture of CGV in response to rapid temperature changes in the nematode Caenorhabditis elegans. We analyzed regulatory variation in gene expression (and mapped eQTL) across the course of a heat stress and recovery response in a recombinant inbred population.ResultsWe measured gene expression over three temperature treatments: i) control, ii) heat stress, and iii) recovery from heat stress. Compared to control, exposure to heat stress affected the transcription of 3305 genes, whereas 942 were affected in recovering animals. These affected genes were mainly involved in metabolism and reproduction. The gene expression pattern in recovering animals resembled both the control and the heat-stress treatment. We mapped eQTL using the genetic variation of the recombinant inbred population and detected 2626 genes with an eQTL in the heat-stress treatment, 1797 in the control, and 1880 in the recovery. The cis-eQTL were highly shared across treatments. A considerable fraction of the trans-eQTL (40–57{\%}) mapped to 19 treatment specific trans-bands. In contrast to cis-eQTL, trans-eQTL were highly environment specific and thus cryptic. Approximately 67{\%} of the trans-eQTL were only induced in a single treatment, with heat-stress showing the most unique trans-eQTL.ConclusionsThese results illustrate the highly dynamic pattern of CGV across three different environmental conditions that can be evoked by a stress response over a relatively short time-span (2 h) and that CGV is mainly determined by response related trans regulatory eQTL.",
author = "Snoek, {Basten L.} and Sterken, {Mark G.} and Bevers, {Roel P.J.} and Volkers, {Rita J.M.} and {van 't Hof}, Arjen and Rachel Brenchley and Riksen, {Joost A.G.} and Andrew Cossins and Kammenga, {Jan E.}",
year = "2017",
doi = "10.1186/s12864-017-3899-8",
language = "English",
volume = "18",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "Springer Verlag",

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Contribution of trans regulatory eQTL to cryptic genetic variation in C. elegans. / Snoek, Basten L.; Sterken, Mark G.; Bevers, Roel P.J.; Volkers, Rita J.M.; van 't Hof, Arjen; Brenchley, Rachel; Riksen, Joost A.G.; Cossins, Andrew; Kammenga, Jan E.

In: BMC Genomics, Vol. 18, 500, 2017.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Contribution of trans regulatory eQTL to cryptic genetic variation in C. elegans

AU - Snoek, Basten L.

AU - Sterken, Mark G.

AU - Bevers, Roel P.J.

AU - Volkers, Rita J.M.

AU - van 't Hof, Arjen

AU - Brenchley, Rachel

AU - Riksen, Joost A.G.

AU - Cossins, Andrew

AU - Kammenga, Jan E.

PY - 2017

Y1 - 2017

N2 - BackgroundCryptic genetic variation (CGV) is the hidden genetic variation that can be unlocked by perturbing normal conditions. CGV can drive the emergence of novel complex phenotypes through changes in gene expression. Although our theoretical understanding of CGV has thoroughly increased over the past decade, insight into polymorphic gene expression regulation underlying CGV is scarce. Here we investigated the transcriptional architecture of CGV in response to rapid temperature changes in the nematode Caenorhabditis elegans. We analyzed regulatory variation in gene expression (and mapped eQTL) across the course of a heat stress and recovery response in a recombinant inbred population.ResultsWe measured gene expression over three temperature treatments: i) control, ii) heat stress, and iii) recovery from heat stress. Compared to control, exposure to heat stress affected the transcription of 3305 genes, whereas 942 were affected in recovering animals. These affected genes were mainly involved in metabolism and reproduction. The gene expression pattern in recovering animals resembled both the control and the heat-stress treatment. We mapped eQTL using the genetic variation of the recombinant inbred population and detected 2626 genes with an eQTL in the heat-stress treatment, 1797 in the control, and 1880 in the recovery. The cis-eQTL were highly shared across treatments. A considerable fraction of the trans-eQTL (40–57%) mapped to 19 treatment specific trans-bands. In contrast to cis-eQTL, trans-eQTL were highly environment specific and thus cryptic. Approximately 67% of the trans-eQTL were only induced in a single treatment, with heat-stress showing the most unique trans-eQTL.ConclusionsThese results illustrate the highly dynamic pattern of CGV across three different environmental conditions that can be evoked by a stress response over a relatively short time-span (2 h) and that CGV is mainly determined by response related trans regulatory eQTL.

AB - BackgroundCryptic genetic variation (CGV) is the hidden genetic variation that can be unlocked by perturbing normal conditions. CGV can drive the emergence of novel complex phenotypes through changes in gene expression. Although our theoretical understanding of CGV has thoroughly increased over the past decade, insight into polymorphic gene expression regulation underlying CGV is scarce. Here we investigated the transcriptional architecture of CGV in response to rapid temperature changes in the nematode Caenorhabditis elegans. We analyzed regulatory variation in gene expression (and mapped eQTL) across the course of a heat stress and recovery response in a recombinant inbred population.ResultsWe measured gene expression over three temperature treatments: i) control, ii) heat stress, and iii) recovery from heat stress. Compared to control, exposure to heat stress affected the transcription of 3305 genes, whereas 942 were affected in recovering animals. These affected genes were mainly involved in metabolism and reproduction. The gene expression pattern in recovering animals resembled both the control and the heat-stress treatment. We mapped eQTL using the genetic variation of the recombinant inbred population and detected 2626 genes with an eQTL in the heat-stress treatment, 1797 in the control, and 1880 in the recovery. The cis-eQTL were highly shared across treatments. A considerable fraction of the trans-eQTL (40–57%) mapped to 19 treatment specific trans-bands. In contrast to cis-eQTL, trans-eQTL were highly environment specific and thus cryptic. Approximately 67% of the trans-eQTL were only induced in a single treatment, with heat-stress showing the most unique trans-eQTL.ConclusionsThese results illustrate the highly dynamic pattern of CGV across three different environmental conditions that can be evoked by a stress response over a relatively short time-span (2 h) and that CGV is mainly determined by response related trans regulatory eQTL.

U2 - 10.1186/s12864-017-3899-8

DO - 10.1186/s12864-017-3899-8

M3 - Article

VL - 18

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

M1 - 500

ER -