Histone H3 and H4 Modifications Point to Transcriptional Suppression as a Component of Winter Freeze Tolerance in the Gall Fly <i>Eurosta solidaginis</i>

The goldenrod gall fly (<i>Eurosta solidaginis)</i> is a well-studied model of insect freeze tolerance. In situations of prolonged winter subzero temperatures, larvae of <i>E. solidaginis</i> accept ice penetration throughout extracellular spaces while protecting the intracel...

Full description

Bibliographic Details
Main Authors: Tighe Bloskie, Kenneth B. Storey
Format: Article
Language:English
Published: MDPI AG 2023-06-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/12/10153
_version_ 1797594261002125312
author Tighe Bloskie
Kenneth B. Storey
author_facet Tighe Bloskie
Kenneth B. Storey
author_sort Tighe Bloskie
collection DOAJ
description The goldenrod gall fly (<i>Eurosta solidaginis)</i> is a well-studied model of insect freeze tolerance. In situations of prolonged winter subzero temperatures, larvae of <i>E. solidaginis</i> accept ice penetration throughout extracellular spaces while protecting the intracellular environment by producing extreme amounts of glycerol and sorbitol as cryoprotectants. Hypometabolism (diapause) is implemented, and energy use is reprioritized to essential pathways. Gene transcription is one energy-expensive process likely suppressed over the winter, in part, due to epigenetic controls. The present study profiled the prevalence of 24 histone H3/H4 modifications of <i>E. solidaginis</i> larvae after 3-week acclimations to decreasing environmental temperatures (5 °C, −5 °C and −15 °C). Using immunoblotting, the data show freeze-mediated reductions (<i>p</i> < 0.05) in seven permissive histone modifications (H3K27me1, H4K20me1, H3K9ac, H3K14ac, H3K27ac, H4K8ac, H3R26me2a). Along with the maintenance of various repressive marks, the data are indicative of a suppressed transcriptional state at subzero temperatures. Elevated nuclear levels of histone H4, but not histone H3, were also observed in response to both cold and freeze acclimation. Together, the present study provides evidence for epigenetic-mediated transcriptional suppression in support of the winter diapause state and freeze tolerance of <i>E. solidaginis</i>.
first_indexed 2024-03-11T02:21:09Z
format Article
id doaj.art-30804cf094bd42768703d7e983c4bd63
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-11T02:21:09Z
publishDate 2023-06-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-30804cf094bd42768703d7e983c4bd632023-11-18T10:49:27ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-06-0124121015310.3390/ijms241210153Histone H3 and H4 Modifications Point to Transcriptional Suppression as a Component of Winter Freeze Tolerance in the Gall Fly <i>Eurosta solidaginis</i>Tighe Bloskie0Kenneth B. Storey1Institute of Biochemistry and Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, ON K1S 5B6, CanadaInstitute of Biochemistry and Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, ON K1S 5B6, CanadaThe goldenrod gall fly (<i>Eurosta solidaginis)</i> is a well-studied model of insect freeze tolerance. In situations of prolonged winter subzero temperatures, larvae of <i>E. solidaginis</i> accept ice penetration throughout extracellular spaces while protecting the intracellular environment by producing extreme amounts of glycerol and sorbitol as cryoprotectants. Hypometabolism (diapause) is implemented, and energy use is reprioritized to essential pathways. Gene transcription is one energy-expensive process likely suppressed over the winter, in part, due to epigenetic controls. The present study profiled the prevalence of 24 histone H3/H4 modifications of <i>E. solidaginis</i> larvae after 3-week acclimations to decreasing environmental temperatures (5 °C, −5 °C and −15 °C). Using immunoblotting, the data show freeze-mediated reductions (<i>p</i> < 0.05) in seven permissive histone modifications (H3K27me1, H4K20me1, H3K9ac, H3K14ac, H3K27ac, H4K8ac, H3R26me2a). Along with the maintenance of various repressive marks, the data are indicative of a suppressed transcriptional state at subzero temperatures. Elevated nuclear levels of histone H4, but not histone H3, were also observed in response to both cold and freeze acclimation. Together, the present study provides evidence for epigenetic-mediated transcriptional suppression in support of the winter diapause state and freeze tolerance of <i>E. solidaginis</i>.https://www.mdpi.com/1422-0067/24/12/10153histone modificationepigeneticsfreeze tolerancehypometabolismgoldenrod gall fly
spellingShingle Tighe Bloskie
Kenneth B. Storey
Histone H3 and H4 Modifications Point to Transcriptional Suppression as a Component of Winter Freeze Tolerance in the Gall Fly <i>Eurosta solidaginis</i>
International Journal of Molecular Sciences
histone modification
epigenetics
freeze tolerance
hypometabolism
goldenrod gall fly
title Histone H3 and H4 Modifications Point to Transcriptional Suppression as a Component of Winter Freeze Tolerance in the Gall Fly <i>Eurosta solidaginis</i>
title_full Histone H3 and H4 Modifications Point to Transcriptional Suppression as a Component of Winter Freeze Tolerance in the Gall Fly <i>Eurosta solidaginis</i>
title_fullStr Histone H3 and H4 Modifications Point to Transcriptional Suppression as a Component of Winter Freeze Tolerance in the Gall Fly <i>Eurosta solidaginis</i>
title_full_unstemmed Histone H3 and H4 Modifications Point to Transcriptional Suppression as a Component of Winter Freeze Tolerance in the Gall Fly <i>Eurosta solidaginis</i>
title_short Histone H3 and H4 Modifications Point to Transcriptional Suppression as a Component of Winter Freeze Tolerance in the Gall Fly <i>Eurosta solidaginis</i>
title_sort histone h3 and h4 modifications point to transcriptional suppression as a component of winter freeze tolerance in the gall fly i eurosta solidaginis i
topic histone modification
epigenetics
freeze tolerance
hypometabolism
goldenrod gall fly
url https://www.mdpi.com/1422-0067/24/12/10153
work_keys_str_mv AT tighebloskie histoneh3andh4modificationspointtotranscriptionalsuppressionasacomponentofwinterfreezetoleranceinthegallflyieurostasolidaginisi
AT kennethbstorey histoneh3andh4modificationspointtotranscriptionalsuppressionasacomponentofwinterfreezetoleranceinthegallflyieurostasolidaginisi