Evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.

The ability of winter wheat (Triticum aestivum L.) plants to develop freezing tolerance through cold acclimation is a complex rait that responds to many environmental cues including day length and temperature. A large part of the freezing tolerance is conditioned by the C-repeat binding factor (CBF)...

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Main Authors: Daniel Z Skinner, Brian Bellinger, William Hiscox, Gregory L Helms
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC6005534?pdf=render
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spelling doaj-b5153d23dfdb42968b86b24364f4adcd2020-11-25T01:53:42ZengPublic Library of Science (PLoS)PLoS ONE1932-62032018-01-01136e019804210.1371/journal.pone.0198042Evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.Daniel Z SkinnerBrian BellingerWilliam HiscoxGregory L HelmsThe ability of winter wheat (Triticum aestivum L.) plants to develop freezing tolerance through cold acclimation is a complex rait that responds to many environmental cues including day length and temperature. A large part of the freezing tolerance is conditioned by the C-repeat binding factor (CBF) gene regulon. We investigated whether the level of freezing tolerance of 12 winter wheat lines varied throughout the day and night in plants grown under a constant low temperature and a 12-hour photoperiod. Freezing tolerance was significantly greater (P<0.0001) when exposure to subfreezing temperatures began at the midpoint of the light period, or the midpoint of the dark period, compared to the end of either period, with an average of 21.3% improvement in survival. Thus, freezing survival was related to the photoperiod, but cycled from low, to high, to low within each 12-hour light period and within each 12-hour dark period, indicating ultradian cyclic variation of freezing tolerance. Quantitative real-time PCR analysis of expression levels of CBF genes 14 and 15 indicated that expression of these two genes also varied cyclically, but essentially 180° out of phase with each other. Proton nuclear magnetic resonance analysis (1H-NMR) showed that the chemical composition of the wheat plants' cellular fluid varied diurnally, with consistent separation of the light and dark phases of growth. A compound identified as glutamine was consistently found in greater concentration in a strongly freezing-tolerant wheat line, compared to moderately and poorly freezing-tolerant lines. The glutamine also varied in ultradian fashion in the freezing-tolerant wheat line, consistent with the ultradian variation in freezing tolerance, but did not vary in the less-tolerant lines. These results suggest at least two distinct signaling pathways, one conditioning freezing tolerance in the light, and one conditioning freezing tolerance in the dark; both are at least partially under the control of the CBF regulon.http://europepmc.org/articles/PMC6005534?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Daniel Z Skinner
Brian Bellinger
William Hiscox
Gregory L Helms
spellingShingle Daniel Z Skinner
Brian Bellinger
William Hiscox
Gregory L Helms
Evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.
PLoS ONE
author_facet Daniel Z Skinner
Brian Bellinger
William Hiscox
Gregory L Helms
author_sort Daniel Z Skinner
title Evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.
title_short Evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.
title_full Evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.
title_fullStr Evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.
title_full_unstemmed Evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.
title_sort evidence of cyclical light/dark-regulated expression of freezing tolerance in young winter wheat plants.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2018-01-01
description The ability of winter wheat (Triticum aestivum L.) plants to develop freezing tolerance through cold acclimation is a complex rait that responds to many environmental cues including day length and temperature. A large part of the freezing tolerance is conditioned by the C-repeat binding factor (CBF) gene regulon. We investigated whether the level of freezing tolerance of 12 winter wheat lines varied throughout the day and night in plants grown under a constant low temperature and a 12-hour photoperiod. Freezing tolerance was significantly greater (P<0.0001) when exposure to subfreezing temperatures began at the midpoint of the light period, or the midpoint of the dark period, compared to the end of either period, with an average of 21.3% improvement in survival. Thus, freezing survival was related to the photoperiod, but cycled from low, to high, to low within each 12-hour light period and within each 12-hour dark period, indicating ultradian cyclic variation of freezing tolerance. Quantitative real-time PCR analysis of expression levels of CBF genes 14 and 15 indicated that expression of these two genes also varied cyclically, but essentially 180° out of phase with each other. Proton nuclear magnetic resonance analysis (1H-NMR) showed that the chemical composition of the wheat plants' cellular fluid varied diurnally, with consistent separation of the light and dark phases of growth. A compound identified as glutamine was consistently found in greater concentration in a strongly freezing-tolerant wheat line, compared to moderately and poorly freezing-tolerant lines. The glutamine also varied in ultradian fashion in the freezing-tolerant wheat line, consistent with the ultradian variation in freezing tolerance, but did not vary in the less-tolerant lines. These results suggest at least two distinct signaling pathways, one conditioning freezing tolerance in the light, and one conditioning freezing tolerance in the dark; both are at least partially under the control of the CBF regulon.
url http://europepmc.org/articles/PMC6005534?pdf=render
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