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Seasonal changes in dehydration tolerance of xylem ray parenchyma cells ofStylax obassia twigs that survive freezing temperatures by deep supercooling

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Summary

Xylem ray parenchyma cells ofStylax obassia twigs undergo supercooling to −26 °C as the terminal temperature of the low temperature exotherm in summer and to −41 °C in winter upon freezing. During supercooling, no evidence of cell dehydration was recognized; cell walls were uncollapsed, no plasmolysis occurred, no ultrastructural changes in the plasma membranes or in cytoplasmic structures occurred, and high survival rates were maintained. Osmotic manipulation with hypertonic solutions of sorbitol did, however, cause dehydration of ray parenchyma cells, in which shrunken protoplasts and plasmolysis were observed. Freeze-fracture replicas showed that, in summer samples, osmotic dehydration produced aparticulate domains accompanied by fracture-jumps in the plasma membranes, which are known as a symptom of dehydration-induced injury, but no such effects were seen in winter samples. By contrast, in winter samples, osmotic dehydration produced conformational changes in the endoplasmic reticulum, which are known as a feature of dehydration tolerance, however, these changes were not seen in the summer samples. These results indicate that the ray parenchyma cells inS. obassia have the ability to tolerate dehydration in winter and lose this ability in summer. Such tolerance is similar to the dehydration tolerance in plant cells that adapt to freezing by extracellular freezing.

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References

  • Ashworth EN, Abeles F (1984) Freezing behavior of water in small pores and the possible role in the freezing of plant tissues. Plant Physiol 76: 201–204

    Google Scholar 

  • Bryant G, Wolf J (1992) Interfacial forces in cryobiology and anhydrobiology. Cryo Lett 7: 23–26

    Google Scholar 

  • Burke MJ, Gusta LV, Quamme HA, Weiser CJ, Li PH (1976) Freezing and injury in plants. Annu Rev Plant Physiol 27: 507–528

    Google Scholar 

  • Fujikawa S (1987) Mechanical force by growth of extracellular ice crystals is widespread cause for slow freezing injury in tertiary hyphae of mushrooms. Cryo Lett 8: 156–161

    Google Scholar 

  • — (1991a) Freeze fracture techniques. In: Harris JR (ed) Electron microscopy in biology: a practical approach. IRL, Oxford, pp 173–201

    Google Scholar 

  • — (1991b) Lamellar to hexagonal II phase transitions in tonoplasts of mushroom hyphae caused by mechanical stress resulting from the formation of extracellular ice crystals. Cryobiology 28: 191–202

    Google Scholar 

  • — (1994a) Ultrastructural studies of intracellular freezing; diversity of alterations in the plasma membrane upon freezing, thawing and recooling. Cryo Lett 15: 223–234

    Google Scholar 

  • — (1994b) Seasonal ultrastructural alterations in the plasma membrane produced by slow freezing in cortical tissues of mulberry (Morus bombycis Koids. cv. Goroji). Trees 8: 288–296

    Google Scholar 

  • — (1995) A freeze-fracture study designed to clarify the mechanisms of freezing injury due to the freezing-induced close apposition of membranes in cortical parenchyma cells of mulberry. Cryobiology 32: 444–454

    Google Scholar 

  • —, Miura K (1986) Plasma membrane ultrastructural changes caused by mechanical stress in the formation of extracellular ice as a primary cause of slow freezing injury in fruit-bodies of basidiomycetes (Lyophyllum ulmarium Fr. Kühner). Cryobiology 23: 371–382

    Google Scholar 

  • — — (1987) Ultrastructural preservation of plasma membranes by non-lethal slow freezing to liquid nitrogen temperature. Cell Struct Funct 12: 63–72

    PubMed  Google Scholar 

  • —, Takabe K (1996) Formation of multiplex lamellae by equilibrium slow freezing of cortical parenchyma cells of mulberry and its possible relationship to freezing tolerance. Protoplasma 190: 189–203

    Google Scholar 

  • —, Kuroda K, Fukazawa K (1994) Ultrastructural study of deep supercooling of xylem ray parenchyma cells fromStylax obassia. Micron 25: 241–252

    Google Scholar 

  • — —, Ohtani J (1996) Seasonal changes in the low-temperature behaviour of xylem ray parenchyma cells in red osier dogwood (Cornus sericea L.) with respect to extracellular freezing and supercooling. Micron 27: 181–191

    Google Scholar 

  • George MF, Burke MJ (1977) Cold hardiness and deep supercooling in xylem of shagbark hickory. Plant Physiol 59: 319–325

    Google Scholar 

  • — —, Pellet HM, Johnson AG (1974) Low temperature exotherms and woody plant distribution. HortSci 9: 519–522

    Google Scholar 

  • —, Becwar MR, Burke MJ (1982) Freezing avoidance by deep supercooling of tissue water in winter-hardy plants. Cryobiology 19: 628–639

    PubMed  Google Scholar 

  • Gordon-Kamm WJ, Steponkus PL (1984) The influence of cold acclimation on the behavior of the plasma membrane following osmotic contraction of isolated protoplasts. Protoplasma 123: 161–173

    Google Scholar 

  • Gusta LV, Tyler NJ, Chen TH-H (1983) Deep undercooling in woody taxa gowing north of the −40 °C isotherm. Plant Physiol 72: 122–128

    Google Scholar 

  • Kaku S, Iwaya M (1978) Low temperature exotherms in xylems of evergreen and deciduous broad-leaved trees in Japan with reference to freezing resistance and distribution range. In: Li PH, Sakai A (eds) Plant cold hardiness and freezing tolerance. Academic Press, New York, pp 227–239

    Google Scholar 

  • Niki T, Sakai A (1981) Ultrastructural changes related to frost hardiness in the cortical parenchyma cells from mulberry twigs. Plant Cell Physiol 22: 171–183

    Google Scholar 

  • Pomeroy MK, Siminovich D (1971) Seasonal cytological changes in secondary phloem parenchyma cells inRobinia pseudoacacia in relation to cold hardiness. Can J Bot 56: 786–794

    Google Scholar 

  • Quamme HA (1991) Application of thermal analysis to breeding fruit crops for increased cold hardiness. HortSci 26: 513–517

    Google Scholar 

  • —, Weiser CJ, Stushnoff C (1973) The mechanism of freezing injury in xylem of winter apple twigs. Plant Physiol 51: 273–277

    Google Scholar 

  • Sakai A, Larcher N (1987) Frost survival in plants: responses and adaptations to freezing stress. Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • Steponkus PL, Langis R, Fujikawa S (1992) Cryopreservation of plant tissues by vitrification. Adv Low Temp Biol 1: 1–61

    Google Scholar 

  • Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation ofArabidopsis thaliana. Effects on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol 109: 15–30

    PubMed  Google Scholar 

  • Webb MS, Steponkus PL (1993) Freeze-induced membrane ultrastructural alterations in rye (Secale cereales) leaves. Plant Physiol 104: 467–478

    Google Scholar 

  • Wisniewski M, Ashworth EN (1986) A comparison of seasonal ultrastructural changes in stem tissues of peach (Prunus persica) that exhibit contrasting mechanisms of cold hardiness. Bot Gaz 147: 407–417

    Google Scholar 

  • —, Davis G (1989) Evidence for the involvement of a specific cell wall layer in regulation of deep supercooling of xylem ray parenchyma. Plant Physiol 91: 151–156

    Google Scholar 

  • — —, Schaffer K (1991) Mediation of deep supercooling of peach and dogwood by enzymatic modifications in cell-wall structure. Planta 184: 254–260

    Google Scholar 

  • Zhou B-L, Arakawa K, Fujikawa S, Yoshida S (1994) Cold-induced alterations in plasma membrane proteins that are specifically related to the development of freezing tolerance in cold-hardy winter wheat. Plant Cell Physiol 35: 175–182

    Google Scholar 

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Fujikawa, S., Kuroda, K. & Ohtani, J. Seasonal changes in dehydration tolerance of xylem ray parenchyma cells ofStylax obassia twigs that survive freezing temperatures by deep supercooling. Protoplasma 197, 34–44 (1997). https://doi.org/10.1007/BF01279882

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  • DOI: https://doi.org/10.1007/BF01279882

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