Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect

Rapid cold hardening (RCH) is a type of beneficial phenotypic plasticity that occurs on extremely short time scales (minutes to hours) to enhance insects' ability to cope with cold snaps and diurnal temperature fluctuations. RCH has a well-established role in extending lower lethal limits, but...

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Published in:Journal of Experimental Biology
Main Authors: Teets, Nicholas M., Kawarasaki, Yuta, Potts, Leslie J., Philip, Benjamin N., Gantz, J. D., Denlinger, David L., Lee, Richard E.
Format: Text
Language:English
Published: The Company of Biologists Ltd 2019
Subjects:
Online Access:http://jeb.biologists.org/cgi/content/short/222/15/jeb206011
https://doi.org/10.1242/jeb.206011
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spelling fthighwire:oai:open-archive.highwire.org:jexbio:222/15/jeb206011 2023-05-15T13:43:52+02:00 Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect Teets, Nicholas M. Kawarasaki, Yuta Potts, Leslie J. Philip, Benjamin N. Gantz, J. D. Denlinger, David L. Lee, Richard E. 2019-08-07 04:15:48.0 text/html http://jeb.biologists.org/cgi/content/short/222/15/jeb206011 https://doi.org/10.1242/jeb.206011 en eng The Company of Biologists Ltd http://jeb.biologists.org/cgi/content/short/222/15/jeb206011 http://dx.doi.org/10.1242/jeb.206011 Copyright (C) 2019, Company of Biologists RESEARCH ARTICLE TEXT 2019 fthighwire https://doi.org/10.1242/jeb.206011 2019-10-03T17:08:28Z Rapid cold hardening (RCH) is a type of beneficial phenotypic plasticity that occurs on extremely short time scales (minutes to hours) to enhance insects' ability to cope with cold snaps and diurnal temperature fluctuations. RCH has a well-established role in extending lower lethal limits, but its ability to prevent sublethal cold injury has received less attention. The Antarctic midge, Belgica antarctica , is Antarctica's only endemic insect and has a well-studied RCH response that extends freeze tolerance in laboratory conditions. However, the discriminating temperatures used in previous studies of RCH are far below those ever experienced in the field. Here, we tested the hypothesis that RCH protects against non-lethal freezing injury. Larvae of B. antarctica were exposed to control (2°C), direct freezing (−9°C for 24 h) or RCH (−5°C for 2 h followed by −9°C for 24 h). All larvae survived both freezing treatments, but RCH larvae recovered more quickly from freezing stress and had a significantly higher metabolic rate during recovery. RCH larvae also sustained less damage to fat body and midgut tissue and had lower expression of two heat shock protein transcripts ( hsp60 and hsp90 ), which is consistent with RCH protecting against protein denaturation. The protection afforded by RCH resulted in energy savings; directly frozen larvae experienced a significant depletion in glycogen energy stores that was not observed in RCH larvae. Together, these results provide strong evidence that RCH protects against a variety of sublethal freezing injuries and allows insects to rapidly fine-tune their performance in thermally variable environments. Text Antarc* Antarctic Antarctic midge Antarctica Belgica antarctica HighWire Press (Stanford University) Antarctic The Antarctic Journal of Experimental Biology
institution Open Polar
collection HighWire Press (Stanford University)
op_collection_id fthighwire
language English
topic RESEARCH ARTICLE
spellingShingle RESEARCH ARTICLE
Teets, Nicholas M.
Kawarasaki, Yuta
Potts, Leslie J.
Philip, Benjamin N.
Gantz, J. D.
Denlinger, David L.
Lee, Richard E.
Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect
topic_facet RESEARCH ARTICLE
description Rapid cold hardening (RCH) is a type of beneficial phenotypic plasticity that occurs on extremely short time scales (minutes to hours) to enhance insects' ability to cope with cold snaps and diurnal temperature fluctuations. RCH has a well-established role in extending lower lethal limits, but its ability to prevent sublethal cold injury has received less attention. The Antarctic midge, Belgica antarctica , is Antarctica's only endemic insect and has a well-studied RCH response that extends freeze tolerance in laboratory conditions. However, the discriminating temperatures used in previous studies of RCH are far below those ever experienced in the field. Here, we tested the hypothesis that RCH protects against non-lethal freezing injury. Larvae of B. antarctica were exposed to control (2°C), direct freezing (−9°C for 24 h) or RCH (−5°C for 2 h followed by −9°C for 24 h). All larvae survived both freezing treatments, but RCH larvae recovered more quickly from freezing stress and had a significantly higher metabolic rate during recovery. RCH larvae also sustained less damage to fat body and midgut tissue and had lower expression of two heat shock protein transcripts ( hsp60 and hsp90 ), which is consistent with RCH protecting against protein denaturation. The protection afforded by RCH resulted in energy savings; directly frozen larvae experienced a significant depletion in glycogen energy stores that was not observed in RCH larvae. Together, these results provide strong evidence that RCH protects against a variety of sublethal freezing injuries and allows insects to rapidly fine-tune their performance in thermally variable environments.
format Text
author Teets, Nicholas M.
Kawarasaki, Yuta
Potts, Leslie J.
Philip, Benjamin N.
Gantz, J. D.
Denlinger, David L.
Lee, Richard E.
author_facet Teets, Nicholas M.
Kawarasaki, Yuta
Potts, Leslie J.
Philip, Benjamin N.
Gantz, J. D.
Denlinger, David L.
Lee, Richard E.
author_sort Teets, Nicholas M.
title Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect
title_short Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect
title_full Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect
title_fullStr Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect
title_full_unstemmed Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect
title_sort rapid cold hardening protects against sublethal freezing injury in an antarctic insect
publisher The Company of Biologists Ltd
publishDate 2019
url http://jeb.biologists.org/cgi/content/short/222/15/jeb206011
https://doi.org/10.1242/jeb.206011
geographic Antarctic
The Antarctic
geographic_facet Antarctic
The Antarctic
genre Antarc*
Antarctic
Antarctic midge
Antarctica
Belgica antarctica
genre_facet Antarc*
Antarctic
Antarctic midge
Antarctica
Belgica antarctica
op_relation http://jeb.biologists.org/cgi/content/short/222/15/jeb206011
http://dx.doi.org/10.1242/jeb.206011
op_rights Copyright (C) 2019, Company of Biologists
op_doi https://doi.org/10.1242/jeb.206011
container_title Journal of Experimental Biology
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