Proteins accumulate in the apoplast of winter rye leaves during cold acclimation

Marentes, Eduardo; Griffith, Marilyn; Mlynarz, Andrzej; Brush, Ruth Anne

doi:10.1034/j.1399-3054.1993.870409.x

Cited by 13 publications

(18 citation statements)

References 16 publications

(22 reference statements)

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“…4). The level of freezing tolerance in the suspension cells in this work was lower than we expected based on the concentration of AFPs found in maximally freezing‐tolerant winter rye leaves (Marentes et al 1993). This suggests that AFPs do not occur as oligomeric complexes in suspensions, as they do in the intact leaves (Yu and Griffith 1999), and that other intracellular and/or extracellular solutes than AFPs, share the responsibility for freezing tolerance with AFPs in winter rye cells.…”

Section: Discussioncontrasting

confidence: 60%

“…5). The concentration of apoplastic protein used in this experiment was chosen on the basis of our pilot experiments and previously reported concentrations of AFPs in CA rye leaves (Marentes et al 1993).…”

Section: Resultsmentioning

confidence: 99%

“…Winter rye and other over‐wintering cereals tolerate the formation of ice in the extracellular space of their tissues during freezing (Levitt 1980,Pearce 1988). They also secrete antifreeze proteins (AFPs) into the leaf apoplast that have the ability to bind to the surface of ice and modify its growth (Griffith et al 1992, Marentes et al 1993, Antikainen and Griffith 1997). Winter rye produces six AFPs ranging in size from 16 to 35 kDa (Hon et al 1994) that may have two distinct functions in planta because they are similar in sequence and enzyme activity to pathogenesis‐related (PR) proteins (Hon et al 1995).…”

Section: Introductionmentioning

confidence: 99%

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Antifreeze proteins are secreted by winter rye cells in suspension culture

Pihakaski-Maunsbach¹,

Tamminen²,

Pietiäinen³

et al. 2003

Physiologia Plantarum

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During cold‐acclimation, winter rye (Secale cereale L) leaves secrete antifreeze proteins (AFPs) into the apoplast. The AFPs bind to ice and modify its growth, which is easily observed in vitro. However, it is not yet known whether in planta AFPs interact with ice or whether they exert cryoprotective effects. These experiments are difficult to conduct with intact plants, so the aim of this work was to determine whether AFPs are produced in response to cold temperature in cell culture and to examine their function by using suspension cells. We showed that suspension cells secreted three of the six known winter rye AFPs into the culture medium during acclimation at 4°C. These AFPs were not present in washed suspension cells, thus indicating that they are not firmly bound to the cell walls. In order to examine the function of extracellular AFPs, non‐acclimated (NA) winter rye suspension cells and protoplasts isolated from NA winter rye leaves were then frozen and thawed in the presence of AFPs extracted from cold‐acclimated winter rye leaves. The AFPs had no effect on the survival of NA protoplasts after freezing; however, they lowered the lethal temperature at which 50% of the cells are killed by freezing (LT50) of NA suspension cells by 2.5°C. We conclude that low above‐zero temperatures induce winter rye suspension cells to secrete AFPs free in solution where they can protect intact suspension cells, but not protoplasts, from freezing injury, presumably by interacting with extracellular ice.

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Section: Discussioncontrasting

confidence: 60%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Antifreeze proteins are secreted by winter rye cells in suspension culture

Pihakaski-Maunsbach¹,

Tamminen²,

Pietiäinen³

et al. 2003

Physiologia Plantarum

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“…The loss of ice-binding activity in transgenic lines was observed in crude cell extracts containing both intracellular and extracellular components, but also in the apoplastic extracts of IBP knockdowns (Fig 10). Most plant IBPs have been shown to localize to the apoplast [7,14,20,52–53] and recent research has demonstrated that localization of IBPs to the extracellular space may be required for full freeze protection [20]. In addition to the identification of putative extracellular signal peptides in the N-terminal domain of all 7 Bd IRIs (Fig 1), the presence of IRI and TH activity, as well as ice shaping in the apoplastic extracts of wild-type B .…”

Section: Discussionmentioning

confidence: 99%

Knockdown of Ice-Binding Proteins in Brachypodium distachyon Demonstrates Their Role in Freeze Protection

2016

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Sub-zero temperatures pose a major threat to the survival of cold-climate perennials. Some of these freeze-tolerant plants produce ice-binding proteins (IBPs) that offer frost protection by restricting ice crystal growth and preventing expansion-induced lysis of the plasma membranes. Despite the extensive in vitro characterization of such proteins, the importance of IBPs in the freezing stress response has not been investigated. Using the freeze-tolerant grass and model crop, Brachypodium distachyon, we characterized putative IBPs (BdIRIs) and generated the first ‘IBP-knockdowns’. Seven IBP sequences were identified and expressed in Escherichia coli, with all of the recombinant proteins demonstrating moderate to high levels of ice-recrystallization inhibition (IRI) activity, low levels of thermal hysteresis (TH) activity (0.03−0.09°C at 1 mg/mL) and apparent adsorption to ice primary prism planes. Following plant cold acclimation, IBPs purified from wild-type B. distachyon cell lysates similarly showed high levels of IRI activity, hexagonal ice-shaping, and low levels of TH activity (0.15°C at 0.5 mg/mL total protein). The transfer of a microRNA construct to wild-type plants resulted in the attenuation of IBP activity. The resulting knockdown mutant plants had reduced ability to restrict ice-crystal growth and a 63% reduction in TH activity. Additionally, all transgenic lines were significantly more vulnerable to electrolyte leakage after freezing to −10°C, showing a 13−22% increase in released ions compared to wild-type. IBP-knockdown lines also demonstrated a significant decrease in viability following freezing to −8°C, with some lines showing only two-thirds the survival seen in control lines. These results underscore the vital role IBPs play in the development of a freeze-tolerant phenotype and suggests that expression of these proteins in frost-susceptible plants could be valuable for the production of more winter-hardy crops.

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“…It has been reported that stress conditions greatly affect the composition of apoplastic proteins both qualitatively and quantitatively [12]. There is strong evidence that apoplast proteins are greatly altered in response to salt [13], chilling [14], salicylic acid [15], metal toxicity [16] and pathogen invasion [17]. When compared to the intracellular signaling pathway components and effectors, the roles of plant apoplastic proteins have been obviously ignored in analyzing the plant stress response.…”

Section: Introductionmentioning

confidence: 99%

Identification of NaCl stress-responsive apoplastic proteins in rice shoot stems by 2D-DIGE

Song

Zhang

et al. 2011

Journal of Proteomics

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Plants have evolved sophisticated systems to cope with adverse environmental conditions such as cold, drought, and salinity. Although a number of stress response networks have been proposed, the role of plant apoplast in plant stress response has been ignored. To investigate the role of apoplastic proteins in the salt-stress response, 10-day-old rice plants were treated with 200 mM NaCl for 1, 6 or 12 hours, and the soluble apoplast proteins of rice shoot stems were extracted for differential analysis, compared with untreated controls, by 2-D DIGE saturation labeling techniques. One hundred twenty-two significantly changed spots were identified by LC-MS/MS, and 117 spots representing 69 proteins have been identified. Of these proteins, 37 are apoplastic proteins according to the bioinformatic analysis. These proteins are mainly involved in the processes of carbohydrate metabolism, oxido-reduction, and protein processing and degradation. According to their functional categories and cluster analysis, a stress response model of apoplastic proteins has been proposed. These data indicate that the apoplast is important in plant stress signal reception and response.

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Proteins accumulate in the apoplast of winter rye leaves during cold acclimation

Cited by 13 publications

References 16 publications

Antifreeze proteins are secreted by winter rye cells in suspension culture

Antifreeze proteins are secreted by winter rye cells in suspension culture

Knockdown of Ice-Binding Proteins in Brachypodium distachyon Demonstrates Their Role in Freeze Protection

Identification of NaCl stress-responsive apoplastic proteins in rice shoot stems by 2D-DIGE

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