Consideration of the reasons why dormant buds of trees have evolved extraorgan freezing as an adaptation for winter survival

Endoh, Keita; Kuwabara, Chikako; Arakawa, Keita; Fujikawa, Seizo

doi:10.1016/j.envexpbot.2014.02.008

Cited by 18 publications

(25 citation statements)

References 27 publications

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“…In cold‐acclimated plants cooled at 2°C hr −1 , a high‐temperature exotherm occurred between −3.5°C and −6.1°C (Figures b,c and b,c, Table ), corresponded with the formation of large ice crystals between the leaf sheath (Figure d) and high leaf sheath INA (Table ). These results are similar to reports in cold‐acclimated tree buds that the high‐temperature exotherm corresponds with bulk water freezing and ice nucleation of the bud scale (Endoh et al, ; Ishikawa & Sakai, ; Ishikawa et al, ).…”

Section: Resultssupporting

confidence: 91%

“…This corroborated our previous report using the viability stain tetrazolium chloride, that partially and fully cold‐acclimated Norstar SAM freezing injury corresponded with the LT 50 (Willick et al, ). In overwintering tree buds, the low‐temperature exotherm corresponds with the freezing of individual florets (Ishikawa & Sakai, ; Ishikawa et al, ) or bud primorida (Endoh et al, ).…”

Section: Resultsmentioning

confidence: 99%

“…Ice crystal formation was observed in longitudinally sectioned crowns according to a modified protocol described by Endoh et al (). Twenty plants per temperature treatment were transferred to test tubes with 200 μl of an INA+ suspension.…”

Section: Methodsmentioning

confidence: 99%

“…The experimental design for DTA was a three‐replicate randomized complete block in which each replicate was composed of seven plants and replicates were separated and repeated over time. DTA was conducted as described by Endoh et al () on four treatment groups (nonacclimated, cold acclimated, nonacclimated cooled in LN 2 , and cold acclimated cooled in LN 2 ). The LN 2 treated plants were tested to determine if the absence of a physical barrier altered exothermic patterns in plant tissue freezing.…”

Section: Methodsmentioning

confidence: 99%

“…Ice nucleation at high, subzero temperatures (approximately −3°C) is crucial to the formation of an ice sink. Slow cooling promotes water migration along a vapour gradient to the ice sink from the freezing‐sensitive tissue, thus promoting supercooling and avoiding lethal nonequilibrium freezing (Endoh, Kuwabara, Arakawa, & Fujikawa, ; Ishikawa & Sakai, ). If the cooling rate is higher than 5°C hr −1 , enough water remains in the freezing‐sensitive tissue to prevent supercooling at a lower temperature (Ishikawa & Sakai, ).…”

Section: Introductionmentioning

confidence: 99%

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Ice segregation in the crown of winter cereals: Evidence for extraorgan and extratissue freezing

Willick

Gusta

Fowler

et al. 2018

Plant Cell & Environment

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Meaningful improvements in winter cereal cold hardiness requires a complete model of freezing behaviour in the critical crown organ. Magnetic resonance microimaging diffusion‐weighted experiments provided evidence that cold acclimation decreased water content and mobility in the vascular transition zone (VTZ) and the intermediate zone in rye (Secale cereale L. Hazlet) compared with wheat (Triticum aestivum L. Norstar). Differential thermal analysis, ice nucleation, and localization studies identified three distinct exothermic events. A high‐temperature exotherm (−3°C to −5°C) corresponded with ice formation and high ice‐nucleating activity in the leaf sheath encapsulating the crown. A midtemperature exotherm (−6°C and −8°C) corresponded with cavity ice formation in the VTZ but an absence of ice in the shoot apical meristem (SAM). A low‐temperature exotherm corresponded with SAM injury and the killing temperature in wheat (−21°C) and rye (−27°C). The SAM had lower ice‐nucleating activity and freezing survival compared with the VTZ when frozen in vitro. The intermediate zone was hypothesized to act as a barrier to ice growth into the SAM. Higher cold hardiness of rye compared with wheat was associated with higher VTZ and intermediate zone desiccation resulting in the formation of ice barriers surrounding the SAM.

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Section: Resultssupporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Ice segregation in the crown of winter cereals: Evidence for extraorgan and extratissue freezing

Willick

Gusta

Fowler

et al. 2018

Plant Cell & Environment

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Plant Responses to Freezing

Fujikawa

2016

Encyclopedia of Life Sciences

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During the course of evolution, plants have developed complex mechanisms to survive under a freezing condition. The ability of temperate plants to endure freezing differs depending on the season and depending on the region they inhabit in relation to the environmental temperatures. The prerequisite for survival of plants under a freezing condition is avoidance of lethal intracellular freezing in living cells. Depending on the function in living cells, such avoidance mechanisms change due to the difference in responses of cell walls as well as the plasma membrane to extracellular ice. Owing to these differences, living plant cells adapt to freezing by extracellular freezing and deep supercooling and also by extraorgan freezing, in which cells adapt by an intermediate form between extracellular freezing and deep supercooling. Key Concepts The first step of freezing resistance is the blocking of cell walls and plasma membranes against inoculation of extracellular ice. Living cells in most temperate plant tissues respond to freezing by extracellular freezing, in which cell walls inhibit ice penetration but allow dehydration. Interbilayer events, which are caused by the close approach of membranes by mechanical stress of freezing, are the main cause of injury by extracellular freezing. Many cold acclimation‐induced changes are related to inhibition of or reduction in the incidence of interbilayer events. Adaptation by deep supercooling occurs in cells with rigid and thick walls, which do not allow penetration of ice or dehydration. Supercooling capacity is changed by intracellular contents, especially by the interaction of antiice nucleation polyphenols with ice nucleators. Dormant buds of many woody plants respond to freezing by extraorgan freezing, in which formation of extracellular ice is excluded in tissues with freezing‐susceptible cells.

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Cryo-Scanning Electron Microscopy to Study the Freezing Behavior of Plant Tissues

Fujikawa¹,

Endoh²

2020

Methods in Molecular Biology

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Consideration of the reasons why dormant buds of trees have evolved extraorgan freezing as an adaptation for winter survival

Cited by 18 publications

References 27 publications

Ice segregation in the crown of winter cereals: Evidence for extraorgan and extratissue freezing

Ice segregation in the crown of winter cereals: Evidence for extraorgan and extratissue freezing

Plant Responses to Freezing

Cryo-Scanning Electron Microscopy to Study the Freezing Behavior of Plant Tissues

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