High ice nucleation activity located in blueberry stem bark is linked to primary freeze initiation and adaptive freezing behaviour of the bark

Kishimoto, Tadashi; Yamazaki, Hideyuki; Saruwatari, Atsushi; Murakawa, Hiroki; Sekozawa, Yoshihiko; Kuchitsu, Kazuyuki; Price, William S.; Ishikawa, Masaya

doi:10.1093/aobpla/plu044

Cited by 32 publications

(43 citation statements)

References 40 publications

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“…This was autonomically induced in Cornus flower buds without exogenous ice‐inoculation (Figs ) and likely intrinsically triggered by the presence of INA in the extracellularly frozen tissues in flower buds (Table ). Similar intrinsic INA has been observed in extracellularly frozen tissues such as blueberry bark and azalea bud scales (Kishimoto et al, , ; Ishikawa et al, ). The high INA likely works as a subfreezing sensor to promote ice nucleation at warmer temperatures in favourable intercellular spaces of the tissues (Kishimoto et al, , ).…”

Section: Discussionsupporting

confidence: 69%

“…Similar intrinsic INA has been observed in extracellularly frozen tissues such as blueberry bark and azalea bud scales (Kishimoto et al, , ; Ishikawa et al, ). The high INA likely works as a subfreezing sensor to promote ice nucleation at warmer temperatures in favourable intercellular spaces of the tissues (Kishimoto et al, , ). This ultimately allows reduction of excess supercooling, resulting in avoidance of lethal intracellular ice formation.…”

Section: Discussionsupporting

confidence: 69%

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Freezing behaviours in winteringCornus floridaflower bud tissues revisited using MRI

Ishikawa

Ide

Yamazaki

et al. 2016

Plant Cell & Environment

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How plant tissues control their water behaviours (phase and movement) under subfreezing temperatures through adaptative strategies (freezing behaviours) is important for their survival. However, the fine details of freezing behaviours in complex organs and their regulation mechanisms are poorly understood, and non-invasive visualization/analysis is required. The localization/density of unfrozen water in wintering Cornus florida flower buds at subfreezing temperatures was visualized with high-resolution magnetic resonance imaging (MRI). This allowed tissue-specific freezing behaviours to be determined. MRI images revealed that individual anthers and ovules remained stably supercooled to -14 to -21 °C or lower. The signal from other floral tissues decreased during cooling to -7 °C, which likely indicates their extracellular freezing. Microscopic observation and differential thermal analyses revealed that the abrupt breakdown of supercooled individual ovules and anthers resulted in their all-or-nothing type of injuries. The distribution of ice nucleation activity in flower buds determined using a test tube-based assay corroborated which tissues primarily froze. MRI is a powerful tool for non-invasively visualizing unfrozen tissues. Freezing events and/or dehydration events can be located by digital comparison of MRI images acquired at different temperatures. Only anthers and ovules preferentially remaining unfrozen are a novel freezing behaviour in flower buds. Physicochemical and biological mechanisms/implications are discussed.

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Section: Discussionsupporting

confidence: 69%

Section: Discussionsupporting

confidence: 69%

Freezing behaviours in winteringCornus floridaflower bud tissues revisited using MRI

Ishikawa

Ide

Yamazaki

et al. 2016

Plant Cell & Environment

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“…Maintenance of supercooling in the bud cells may-alongside structural prerequisites such as ice barriers (Kuprian et al, 2017;Kuprian, Briceno, Wagner, & Neuner, 2014) and freeze dehydration -require additional currently unknown molecular components (Ishikawa et al, 2009;Ishikawa, Ishikawa, Toyomasu, Aoki, & Price, 2015;Kishimoto et al, 2014;Wisniewski, Gusta, Fuller, & Karlson, 2009;Wisniewski, Gusta, & Neuner, 2014). During supercooling such molecular components could have stabilizing activity, ice nucleation activity, and/or antifreeze activity (Ishikawa, 2014;Ishikawa et al, 2015).…”

mentioning

confidence: 99%

Deep supercooling enabled by surface impregnation with lipophilic substances explains the survival of overwintering buds at extreme freezing

Neuner

Kreische

Kaplenig

et al. 2019

Plant Cell & Environment

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The frost survival mechanism of vegetative buds of angiosperms was suggested to be extracellular freezing causing dehydration, elevated osmotic potential to prevent freezing. However, extreme dehydration would be needed to avoid freezing at the temperatures down to −45°C encountered by many trees. Buds of Alnus alnobetula, in common with other frost hardy angiosperms, excrete a lipophilic substance, whose functional role remains unclear. Freezing of buds was studied by infrared thermography, psychrometry, and cryomicroscopy. Buds of A. alnobetula did not survive by extracellular ice tolerance but by deep supercooling, down to −45°C. An internal ice barrier prevented ice penetration from the frozen stem into the bud. Cryomicroscopy revealed a new freezing mechanism. Until now, supercooled buds lost water towards ice masses that form in the subtending stem and/or bud scales. In A. alnobetula, ice forms harmlessly inside the bud between the supercooled leaves. This would immediately trigger intracellular freezing and kill the supercooled bud in other species. In A. alnobetula, lipophilic substances (triterpenoids and flavonoid aglycones) impregnate the surface of bud leaves. These prevent extrinsic ice nucleation so allowing supercooling. This suggests a means to protect forestry and agricultural crops from extrinsic ice nucleation allowing transient supercooling during night frosts.

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“…Moreover, caffeine could inhibit the ice nucleation of calcium oxalate Table 3 . The stem bark of blueberry and various tissues of Rhododendron flower buds contained a compound with high ice nucleation activity for primary freeze initiation and adaptive freezing Kishimoto et al, 2014;Ishikawa et al, 2015 . This high ice nucleation activity was due to the presence of calcium oxalate in the stem bark and tissues of flower Ishikawa et al, 2016 .…”

Section: Characterization Of Scf Activity Of Caffeinementioning

confidence: 99%

Characterization of Anti-Ice Nucleation Activity of the Extract from Coffee Refuse

et al. 2017

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The supercooling-facilitating SCF activities, that is, the anti-ice nucleation activity of the hot water extracts from five types of processed food refuse was examined. The extract with the highest activity among five hot water extracts was coffee refuse, showing 1.50 of SCF activity at a final concentration of 0.1 mg/ml. From the hot water extract of coffee refuse, the coffee refuse extract containing various polyphenols was prepared by the ultrafiltration less than MWCO 10,000 , a solvent fractionation of ethyl acetate. The yield of coffee refuse extract was 0.9% w/w from dried coffee refuse. The SCF activity of the coffee refuse extract at a final concentration of 1.0 mg/ml was 4.2 . HPLC analysis of the coffee refuse extract showed that caffeine and chlorogenic acid, which are major components of coffee, could be found at 173 and 62.3 µg/ml, respectively. However, the SCF activities of both compounds 0.70 and 1.06 at a final concentration of 0.1 mg/ml were lower than those of ferulic acid and coumaric acid, respectively at 3.40 and 2.35 . This is the first report to our knowledge on the SCF activity of caffeine. The SCF activity of caffeine at a final concentration of 1.0 mg/ml was 2.3 . The specificity of caffeine against various ice nuclei containing calcium oxalate, 9-fluorenon, and ice nucleating bacteria was examined. Caffeine at a final concentration of 1.0 mg/ml could inhibit the ice nucleation activity of calcium oxalate, and Pseudomonas fluorescens KUIN-1 at the same level that of as silver iodide. From these results, it was suggested that the extract could be able to be applied to the field to control the frost damage of the vegetables and that the harvested vegetables might be stored unfrozen even at 0 or less.

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High ice nucleation activity located in blueberry stem bark is linked to primary freeze initiation and adaptive freezing behaviour of the bark

Cited by 32 publications

References 40 publications

Freezing behaviours in winteringCornus floridaflower bud tissues revisited using MRI

Freezing behaviours in winteringCornus floridaflower bud tissues revisited using MRI

Deep supercooling enabled by surface impregnation with lipophilic substances explains the survival of overwintering buds at extreme freezing

Characterization of Anti-Ice Nucleation Activity of the Extract from Coffee Refuse

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