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      Frost Survival Mechanism of Vegetative Buds in Temperate Trees: Deep Supercooling and Extraorgan Freezing vs. Ice Tolerance


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          In temperate climates, overwintering buds of trees are often less cold hardy than adjoining stem tissues or evergreen leaves. However, data are scarce regarding the freezing resistance (FR) of buds and the underlying functional frost survival mechanism that in case of supercooling can restrict the geographic distribution. Twigs of 37 temperate woody species were sampled in midwinter 2016 in the Austrian Inn valley. After assessment of FR, infrared-video-thermography and cryo-microscopy were used to study the freezing pattern in and around overwintering vegetative buds. Only in four species, after controlled ice nucleation in the stem (−1.6 ± 0.9°C) ice was observed to immediately invade the bud. These buds tolerated extracellular ice and were the most freezing resistant (−61.8°C mean LT 50). In all other species (33), the buds remained supercooled and free of ice, despite a frozen stem. A structural ice barrier prevents ice penetration. Extraorgan ice masses grew in the stem and scales but in 50% of the species between premature supercooled leaves. Two types of supercooled buds were observed: in temporary supercooling buds (14 species) ice spontaneously nucleated at −20.5 ± 4,6°C. This freezing process appeared to be intracellular as it matched the bud killing temperature (−22.8°C mean LT 50). This response rendered temporarily supercooled buds as least cold hardy. In 19 species, the buds remained persistently supercooled down to below the killing temperature without indication for the cause of damage. Although having a moderate midwinter FR of −31.6°C (LT 50), some species within this group attained a FR similar to ice tolerant buds. The present study represents the first comprehensive overview of frost survival mechanisms of vegetative buds of temperate trees. Except for four species that were ice tolerant, the majority of buds survive in a supercooled state, remaining free of ice. In 50% of species, extraorgan ice masses harmlessly grew between premature supercooled leaves. Despite exposure to the same environmental demand, midwinter FR of buds varied intra-specifically between −17.0 and −90.0°C. Particularly, species, whose buds are killed after temporary supercooling, have a lower maximum FR, which limits their geographic distribution.

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          Knowing when to grow: signals regulating bud dormancy.

          Dormancy regulation in vegetative buds is a complex process necessary for plant survival, development and architecture. Our understanding of and ability to manipulate these processes are crucial for increasing the yield and availability of much of the world's food. In many cases, release of dormancy results in increased cell division and changes in developmental programs. Much can be learned about dormancy regulation by identifying interactions of signals in these crucial processes. Internal signals such as hormones and sugar, and external signals such as light act through specific, overlapping signal transduction pathways to regulate endo-, eco- and paradormancy. Epigenetic-like regulation of endodormancy suggests a possible role for chromatin remodeling similar to that known for the vernalization responses during flowering.
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            European deciduous trees exhibit similar safety margins against damage by spring freeze events along elevational gradients.

            Minimum temperature is assumed to be an important driver of tree species range limits. We investigated during which period of the year trees are most vulnerable to freezing damage and whether the pressure of freezing events increases with increasing elevation. We assessed the course of freezing resistance of buds and leaves from winter to summer at the upper elevational limits of eight deciduous tree species in the Swiss Alps. By reconstructing the spring phenology of these species over the last eight decades using a thermal time model, we linked freezing resistance with long-term minimum temperature data along elevational gradients. Counter-intuitively, the pressure of freeze events does not increase with elevation, but deciduous temperate tree species exhibit a constant safety margin (5-8.5 K) against damage by spring freeze events along elevational gradients, as a result of the later flushing at higher elevation. Absolute minimum temperatures in winter and summer are unlikely to critically injure trees. Our study shows that freezing temperatures in spring are the main selective pressure controlling the timing of flushing, leading to a shorter growing season at higher elevation and potentially driving species distribution limits. Such mechanistic knowledge is important to improve predictions of tree species range limits. © 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.
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              Observations of Ice Nucleation and Propagation in Plants Using Infrared Video Thermography.

              We evaluated the use of infrared (IR) video thermography to observe directly ice nucleation and propagation in plants. An imaging radiometer with an HgCdTe long-wave (8-12 [mu]m) detector was utilized to image the thermal response of plants during freezing. IR images were analyzed in real time and recorded on videotape. Information on the videotape was subsequently accessed and analyzed utilizing IR image analysis software. Freezing of water droplets as small as 0.5 [mu]L was clearly detectable with the radiometer. Additionally, a comparison of temperature tracking data collected by the radiometer with data collected with thermocouples showed close correspondence. Monitoring of an array of plant species under different freezing conditions revealed that ice nucleation and propagation are readily observable by thermal imaging. In many instances, the ice nucleation-active bacterium Pseudomonas syringae placed on test plants could be seen to initiate freezing of the whole plant. Apparent ice nucleation by intrinsic nucleators, despite the presence of ice nucleation-active bacteria, was also evident in some species. Floral bud tissues of peach (Prunus persica) could be seen to supercool below the temperature of stem tissues, and ice nucleation at the site of insertion of the thermocouple was frequently observed. Rates of propagation of ice in different tissues were also easily measured by thermal imaging. This study demonstrates that IR thermography is an excellent method for studying ice nucleation and propagation in plants.

                Author and article information

                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                09 May 2019
                : 10
                Unit Functional Plant Biology, Department of Botany, University of Innsbruck , Innsbruck, Austria
                Author notes

                Edited by: Guenter Hoch, Universität Basel, Switzerland

                Reviewed by: Seizo Fujikawa, Hokkaido University, Japan; YeonKyeong Lee, Norwegian University of Life Sciences, Norway

                *Correspondence: Gilbert Neuner gilbert.neuner@ 123456uibk.ac.at

                This article was submitted to Functional Plant Ecology, a section of the journal Frontiers in Plant Science

                Copyright © 2019 Neuner, Monitzer, Kaplenig and Ingruber.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 56, Pages: 13, Words: 10226
                Funded by: Austrian Science Fund 10.13039/501100002428
                Award ID: P23681
                Plant Science
                Original Research

                Plant science & Botany
                freeze dehydration,freezing pattern,freezing resistance,ice nucleation,stem cells,supercooling,translocated ice,vegetative buds


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