Plant Responses to Freezing

Abstract

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.

Keywords: intracellular freezing; extracellular freezing; cold acclimation and deacclimation; deep supercooling; supercooling‐promoting (antiice nucleation) substances; extraorgan freezing

Figure 1. (a–c) Diverse responses of plant cells to freezing by observation with Cryo‐SEM. (a1–2) Freezing response of cortical parenchyma cells of a mulberry tree harvested in autumn exhibiting adaptation by extracellular freezing. As compared with control cells before freezing (a1), equilibrium freezing to −10 °C caused production of extracellular ice (*) among shrunken cells by dehydration (a2). (b1–3) Freezing response of xylem parenchyma cells of a birch tree harvested in summer exhibiting adaptation by deep supercooling. As compared with control cells before freezing (b1), cells supercooled at −15 °C showed the same appearance as that of control cells (b2). Intracellular freezing occurs by cooling to −20 °C. Arrows indicate some intracellular ice (b3). Reproduced with permission from Kasuga et al. 2013 © Springer. (c1–2). Freezing response of dormant buds in larch harvested in winter exhibiting adaptation by extraorgan freezing. By slow freezing to −30 °C, large masses of extracellular ice (*) were produced in basal areas of scales and subtending areas of the shoot primordium as observed by a light microscope (c1). In the shoot primordium under freezing at −30 °C, no extracellular ice was produced and packed primordial cells were slightly shrunken showing adaptation by deep supercooling with incomplete dehydration (c2). Reproduced from Endoh et al. 2009 © Elsevier.
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References

Arora R, Wisniewski ME and Scorza R (1992) Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch): I. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues. Plant Physiology 99: 1562–1568.

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

Ashworth EN, Davis GA and Wisniewski ME (1989) The formation and distribution of ice within dormant and deacclimated peach flower buds. Plant, Cell and Environment 12: 607–612.

Bartolo ME, Wallner SJ and Ketchum RE (1987) Comparison of freezing tolerance in cultured plant cells and their respective protoplasts. Cryobiology 24: 53–57.

Crowe JH, Crowe LM, Carpenter JF, et al (1988) Interaction of sugars with membranes. Biochimica et Biopysica Acta 947: 367–384.

Endoh K, Kasuga J, Arakawa K, Ito T and Fujikawa S (2009) Cryo‐scanning electron microscopic study on freezing behaviors of tissue cells in dormant buds of larch (Larix kaempferi). Cryobiology 59: 214–222.

Endoh K, Kuwabara C, Arakawa K and Fujikawa S (2014) Consideration of the reasons why dormant buds of trees have evolved extraorgan freezing as an adaptation for winter survival. Environmental and Experimental Botany 106: 52–59.

Fujikawa S and 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.) Kuhner). Cryobiology 23: 371–382.

Fujikawa S and Steponkus PL (1990) Freeze‐induced alterations in the ultrastructure of the plasma membrane of rye protoplasts isolated from cold acclimated leaves. Cryobiology 27: 665–666.

Fujikawa S, Kuroda K and Fukazawa K (1994) Ultrastructural study of deep supercooling of xylem ray parenchyma cells from Styrax obassia. Micron 25: 241–252.

Fujikawa S (1994a) Ultrastructural studies of intracellular freezing: diversity of alterations in the plasma membrane upon freezing, thawing and recooling. Cryo‐Letters 15: 223–234.

Fujikawa S (1994b) Seasonal ultrastructural alterations in the plasma membrane produced by slow freezing in cortical tissues of mulberry (Morus bombycis Koidz. Cv. Goloji). Trees – Structure and Function 8: 288–296.

Fujikawa S (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.

Fujikawa S and 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.

Fujikawa S, Jitsuyama Y and Kuroda K (1999) Determination of the role of cold acclimation‐induced diverse changes in plant cells from the viewpoint of avoidance of freezing injury. Journal of Plant Research 112: 237–244.

Fujikawa S and Kuroda K (2000) Cryo‐scanning electron microscopic study on freezing behavior of xylem ray parenchyma cells in hardwood species. Micron 31: 669–686.

Fujikawa S, Ukaji N, Nagao M, et al (2006) Functional role of winter‐accumulating proteins from mulberry tree in adaptation to winter‐induced stresses. In: Chen THH, Uemura M and Fujikawa S (eds) Cold Hardiness in Plants: Molecular genetics, Cell Biology and Physiology, pp. 181–202. Wallingford: CABI.

Fujikawa S, Kasuga J, Takata N and Arakawa K (2009) Factors related to change of deep supercooling capability in xylem parenchyma cells of trees. In: Gusta LV, Wisniewski ME and Tanino KK (eds) Plant Cold Hardiness. From the Laboratory to the Field, pp. 29–42. Wallingford: CABI.

George MF, Burke MJ, Pellet HM and Johnson AG (1974) Low temperature exotherms and woody plant distribution. HortScience 9: 519–522.

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

George MF, Becwar MR and Burke MJ (1982) Freezing avoidance by deep supercooling of tissue water in winter‐hardy plants. Cryobiology 19: 628–639.

Gordon‐Kamm WJ and Steponkus PL (1984a) Lamellar‐to‐hexagonal II phase transitions in the plasma membrane of isolated protoplasts after freeze‐induced dehydration. Proceedings of the National Academy of Sciences of the United States of America 81: 6373–6377.

Gordon‐Kamm WJ and Steponkus PL (1984b) The behavior of the plasma membrane following osmotic contraction of isolated protoplasts: implication in freezing injury. Protoplasma 123: 83–94.

Gusta LV, Tyler NJ and Chen THH (1983) Deep supercooling in woody taxa growing north of the ‐40C isotherm. Plant Physiology 72: 122–128.

Griffith M and Antikainen M (1996) Extracellular ice formation in freezing‐tolerant plants. In: Steponkus PL (ed) Advances in Low Temperature Biology, 3, pp. 107–139. London: JAI Press.

Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 41: 187–223.

Hincha DK, Espinoza C and Zuther E (2012) Transcriptomic and Metabolomic approaches to the analysis of plant freezing tolerance and cold acclimation. In: Tuteja N, Gill SS, Toburico AF and Tuteja R (eds) Improved Cop Resistance to Abiotic Stress, pp. 255–287. Berlin: Wiley‐Blackwell.

Hunter NPA, Palta JP, Li PH, et al (1981) Anatomical changes in leaves of puma rye in response to growth at cold‐hardning temperatures. Botanical Gazette 142: 55–62.

Ishikawa M and Sakai A (1982) Characteristic of freezing avoidance in comparison with freezing tolerance. In: Li PH and Sakai A (eds) Plant Cold Hardiness and Freezing Stress, vol. II, pp. 325–340. London: Academic Press.

Kasuga J, Mizuno K, Miyaji N, et al (2006) Role of intracellular contents to facilitate supercooling capability in beech (Fagus crenata) xylem parenchyma cells. CryoLetters 27: 305–310.

Kasuga J, Arakawa K and Fujikawa S (2007a) High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytologist 174: 569–579.

Kasuga J, Mizuno K, Arakawa K and Fujikawa S (2007b) Anti‐ice nucleation activity in xylem extracts from trees that contain deep supercooling xylem parenchyma cells. Cryobiology 55: 305–314.

Kasuga J, Hashidoko Y, Nishioka A, et al. (2008) Deep supercooling xylem parenchyma cells of katsura tree (Cercidiphyllum japocum) contain flavonol glycosides exhibiting high anti‐ice nucleation activity. Plant, Cell and Environment 31: 1335–1348.

Kasuga J, Endoh K, Yoshiba M, et al. (2013) Roles of cell walls and intracellular contents in supercooling capability of xylem parenchyma cells of boreal trees. Physiologia Plantarum 148: 25–35.

Koster KL, Webb MS, Bryant G, et al (1994) Interactions between soluble sugars and POPC (1‐palmitoyl‐2‐oleoylphosphatidylcholine) during dehydration. Vitrification of sugars alter the phase behavior of the phospholipid. Biochimica et Biophysica Acta 1193: 143–150.

Kuroda K, Ohtani J and Fujikawa S (1997) Supercooling of xylem parenchyma cells in tropical and sub‐tropical hardwood species. Trees – Structure and Function 12: 97–106.

Kuroda K, Kasuga J, Arakawa K and Fujikawa S (2003) Xylem ray parenchyma cells in boreal hardwood species respond to subfreezing temperatures by deep supercooling that is associated by incomplete desiccation. Plant Physiology 131: 736–744.

Kuwabara C, Kasuga J, Wang D, et al. (2011) Changes of supercooling capability in solutions containing different kinds of ice nucleators by flavonol glycosides from deep supercooling xylem parenchyma cells in trees. Cryobiology 63: 157–163.

Kuwabara C, Wang D, Kasuga J, et al (2012) Freezing activities of flavonoids in solutions containing different ice nucleators. Cryobiology 64: 279–285.

Kuwabara C, Wang D, Endoh K, et al (2013) Analysis of supercooling activity of tannin‐related polyphenols. Cryobiology 67: 40–49.

Levitt J (1980) Responses of Plants to Environmental Stresses: Chilling, Freezing and High Temperature Stresses, 1. Orland: Academic Press.

Nagao M, Arakawa K, Takezawa D and Fujikawa S (2008) Long‐ and short term freezing induced different types of injury in Arabidopsis thaliana leaf cells. Planta 227: 477–489.

Pearce RS and Willison JHM (1985) A freeze‐etch study of the effects of extracellular freezing on cellular membranes of wheat. Planta 163: 304–316.

Pearce RS (2004) Adaptation of higher plants to freezing. In: Fuller BJ, Lane N and Benson EE (eds) Life in the Frozen State, pp. 171–203. Boca Raton: CRC Press.

Quamme H, Stushnoff C and Weiser CJ (1972) The relationship of exotherms to cold injury in apple stem tissues. Journal of the American Society for Horticultural Science 97: 608–613.

Quamme HA (1995) Deep supercooling in buds of woody plants. In: Lee RE, Warren GJ and Gusta LV (eds) Biological Ice Nucleation and its Application, pp. 183–199, chap. 10. St Paul, MN: APS Press.

Sakai A (1982) Extraorgan freezing of primordial shoots of winter buds of conifer. In: Li PH and Sakai A (eds) Plant Cold Hardiness and Freezing Stress, vol. II, pp. 199–209. London: Academic Press.

Sakai A and Larcher W (1987) Frost Survival of Plants: Responses and Adaptation to Freezing Stress. Berlin: Spring‐Verlag.

Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annual Review of Plant Physiology 35: 543–584.

Steponkus PL and Lynch DV (1989) Freeze/thaw induced destabilization of plasma membrane and the effects of cold acclimation. Journal of Bioenergetics and Biomembranes 21: 21–41.

Steponkus PL and Webb MS (1992) Freeze‐induced dehydration and membrane destabilization in plants. In: Somero GN, Osmond CB and Bolis CL (eds) Water and Life: Comparative Analysis of water Relationships at the Organismic, Cellular and Molecular Level, pp. 338–362. Springer‐Verlag: Berlin.

Steponkus PL, Uemura M and Webb MS (1993) A contrast of the cryostability of the plasma membrane of winter rye and spring oat. Two species that widely differ in their freezing tolerance and plasma membrane lipid composition. In: Steponkus PL (ed) Advances in Low‐Temperature Biology, vol. 2, pp. 211–312. London: JAI Press.

Takata N, Kasuga J, Takezawa D, Arakawa K and Fujikawa S (2007) Gene expression associated with increased supercooling capability in xylem parenchyma cells of larch (Larix kaempferi). Journal of Experimental Botany 58: 3731–3742.

Tanaka S, Nagao M, Funada R, Fujikawa S and Arakawa K (2003) The relation between small diameter capillaries in cell walls and deep supercooling in xylem parenchyma cells of woody plants. Cryobiology and Cryotechnology 49: 209–213.

Uemura M and Yoshida S (1984) Improvement of plasma membrane alterations in cold acclimation of winter rye seedlings (Scale cereal L. cv. Puma). Plant Physiology 75: 818–826.

Uemura M, Joseph RA and Steponkus PL (1995) Cold acclimation of Arabidopsis thaliana. Effects on plasma membrane lipid composition and freeze‐induced lesions. Plant Physiology 109: 15–30.

Yamada T, Kuroda K, Jitsuyama Y, et al. (2002) Roles of the plasma membrane and the cell walls in the responses of plant cells to freezing. Planta 215: 770–778.

Wang D, Kasuga J, Kuwabara C, et al. (2012) Presence of supercooling‐facilitating (anti‐ice nucleation) hydrolyzable tannins in deep supercooling xylem parenchyma cells in Cercidiphyllum japonicum. Planta 235: 747–759.

Further Reading

Chen THH, Burke MJ and Gusta LV (1995) Freezing tolerance in plants: an overview. In: Ree RE Jr, Warren GJ and Gusta LV (eds) Biological Ice Nucleation and Its Application, pp. 115–135. St Paul, MN: APS Press.

Hincha DK and Zutter E (2014) Plant Cold Acclimation: Methods and Protocoles. New York: Humana Press.

Wisniewski M (1995) Deep supercooling and the role of cell wall structure. In: Lee RL Jr, Warren GJ and Gusta LV (eds) Biological Ice Nucleation and Its Application, pp. 163–182. APS Press: St Paul, MN.

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Fujikawa, Seizo(Nov 2016) Plant Responses to Freezing. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023719]