Freeze dehydration vs. supercooling of mesophyll cells: Impact of cell wall, cellular and tissue traits on the extent of water displacement

Stegner, Matthias; Flörl, Alexander; Lindner, Josef; Plangger, Sandra; Schaefernolte, Tanja; Strasser, Anna-Lena; Thoma, Viktoria; Walde, Janette; Neuner, Gilbert

doi:10.1111/ppl.13793

Cited by 15 publications

(12 citation statements)

References 76 publications

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“…Therefore, conceivably, differential cell wall rigidity of the adaxial (palisade) versus abaxial (spongy parenchyma) sides could also contribute to the anisotropy of freeze‐desiccation in R. maximum leaves. In support of this hypothesis, a recent study involving 11 herbaceous and woody species, including evergreens, noted decreased freeze‐desiccation of mesophyll cells in those species with higher cell wall thickness and rigidity and smaller intercellular spaces (Stegner et al, 2022).…”

Section: Resultsmentioning

confidence: 89%

Infrared thermography of in situ natural freezing and mechanism of winter‐thermonasty in Rhododendron maximum

Arora

Wisniewski

Tuong³

et al. 2023

Physiologia Plantarum

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Evergreen leaves of Rhododendron species inhabiting temperate/montane climates are typically exposed to both high radiation and freezing temperatures during winter when photosynthetic biochemistry is severely inhibited. Cold-induced "thermonasty," that is, lamina rolling and petiole curling, can reduce the amount of leaf area exposed to solar radiation and has been associated with photoprotection in overwintering rhododendrons. The present study was conducted on natural, mature plantings of a cold-hardy and large-leaved thermonastic North American species (Rhododendron maximum) during winter freezes. Infrared thermography was used to determine initial sites of ice formation, patterns of ice propagation, and dynamics of the freezing process in leaves to understand the temporal and mechanistic relationship between freezing and thermonasty. Results indicated that ice formation in whole plants is initiated in the stem, predominantly in the upper portions, and propagates in both directions from the original site. Ice formation in leaves initially occurred in the vascular tissue of the midrib and then propagated into other portions of the vascular system/venation. Ice was never observed to initiate or propagate into palisade, spongy mesophyll, or epidermal tissues. These observations, together with the leafand petiole-histology, and a simulation of the rolling effect of dehydrated leaves using a cellulose-based, paper-bilayer system, suggest that thermonasty occurs due to anisotropic contraction of cell wall cellulose fibers of adaxial versus abaxial surface as the cells lose water to ice present in vascular tissues.

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Section: Resultsmentioning

confidence: 89%

Infrared thermography of in situ natural freezing and mechanism of winter‐thermonasty in Rhododendron maximum

Arora

Wisniewski

Tuong³

et al. 2023

Physiologia Plantarum

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“…Why the mesophyll cells of frozen mountain pine needles succeed in maintaining photosynthesis and their shape might be found in microchemistry and structure (Stegner et al, 2022 ). Arm palisade parenchyma cells are in a strip‐like arrangement between the endodermis and the hypodermis, and tangential cell walls seem to be glued together by lignin.…”

Section: Discussionmentioning

confidence: 99%

Frozen mountain pine needles: The endodermis discriminates between the ice‐containing central tissue and the ice‐free fully functional mesophyll

Stegner

Buchner

Geßlbauer

et al. 2023

Physiologia Plantarum

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Conifer (Pinaceae) needles are the most frost‐hardy leaves. During needle freezing, the exceptional leaf anatomy, where an endodermis separates the mesophyll from the vascular tissue, could have consequences for ice management and photosynthesis. The eco‐physiological importance of needle freezing behaviour was evaluated based on the measured natural freezing strain at the alpine treeline. Ice localisation and cellular responses to ice were investigated in mountain pine needles by cryo‐microscopic techniques. Their consequences for photosynthetic activity were assessed by gas exchange measurements. The freezing response was related to the microchemistry of cell walls investigated by Raman microscopy. In frozen needles, ice was confined to the central vascular cylinder bordered by the endodermis. The endodermal cell walls were lignified. In the ice‐free mesophyll, cells showed no freeze‐dehydration and were found photosynthetically active. Mesophyll cells had lignified tangential cell walls, which adds rigidity. Ice barriers in mountain pine needles seem to be realised by a specific lignification patterning of cell walls. This, additionally, impedes freeze‐dehydration of mesophyll cells and enables gas exchange of frozen needles. At the treeline, where freezing is a dominant environmental factor, the elaborate needle freezing pattern appears of ecological importance.

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“…Freezing stress induces damage in living cells by two main mechanisms: lethal intracellular freezing or frost-induced dessication (through cell membrane injury or protein denaturation), see Burke et al (1976); Arora (2018); Pearce (2001). Living cells can prevent lethal intracellular freezing by two mechanisms: dehydration and deep supercooling (Levitt et al, 1980;Stegner et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Freeze dehydration vs. supercooling in tree stems: physical and physiological modelling

Bozonnet

Saudreau

Badel

et al. 2023

Preprint

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Frost resistance is the major factor affecting the distribution of plant species at high latitude and elevation. The main effects of freeze-thaw cycles are damage to living cells and formation of gas embolism in xylem vessels. Lethal intracellular freezing can be prevented in living cells by two mechanisms: dehydration and deep supercooling. We developed a multiphysics numerical model coupling water flow, heat transfer, and phase change, considering different cell types in plant tissues, to study the dynamics and extent of cell dehydration, xylem pressure changes, and stem diameter changes in response to freezing and thawing. Results were validated using experimental data for stem diameter changes of walnut trees. The effect of cell mechanical properties was found to be negligible as long as the intracellular tension developed during dehydration was sufficiently low compared to the ice induced cryostatic suction. The model was finally used to explore the coupled effects of relevant physiological parameters (initial water and sugar content) and environmental conditions (air temperature variations) on the dynamics and extent of dehydration. It revealed configurations where cell dehydration could be sufficient to protect cells from intracellular freezing, and situations where supercooling was necessary. This model, freely available with this paper, could easily be extended to explore different anatomical structures, different species and more complex physical processes.

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Freeze dehydration vs. supercooling of mesophyll cells: Impact of cell wall, cellular and tissue traits on the extent of water displacement

Cited by 15 publications

References 76 publications

Infrared thermography of in situ natural freezing and mechanism of winter‐thermonasty in Rhododendron maximum

Infrared thermography of in situ natural freezing and mechanism of winter‐thermonasty in Rhododendron maximum

Frozen mountain pine needles: The endodermis discriminates between the ice‐containing central tissue and the ice‐free fully functional mesophyll

Freeze dehydration vs. supercooling in tree stems: physical and physiological modelling

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