The mechanism underlying overwintering death in poplar: the cumulative effect of effective freeze–thaw damage

Abstract

We analyzed the relationships linking overwintering death and frost cracking to temperature and sunlight as well as the effects of low temperatures and freeze–thaw cycles on bud-burst rates, relative electrical conductivity, and phloem and cambial ultrastructures of poplar.Overwintering death rates of poplar were not correlated with negative accumulated temperature or winter minimum temperature. Freeze–thaw cycles caused more bud damage than constant exposure to low temperatures. Resistance to freeze–thaw cycles differed among clones, and the bud-burst rate decreased with increasing exposure to freeze–thaw cycles. Cold-resistant clones had the lowest relative electrical conductivity. Chloroplasts exhibited the fastest and the most obvious reaction to freeze–thaw damage, whereas a single freeze–thaw cycle caused little damage to cambium ultrastructure. Several such cycles resulted in damage to plasma membranes, severe damage to organelles, dehydration of cells and cell death. We conclude that overwintering death of poplar is mainly attributed to the accumulation of effective freeze–thaw damage beyond the limits of freeze–thaw resistance.

Keywords

Effective freeze–thaw / Freeze–thaw resistance / Mechanism / Overwintering death / Populus / Ultrastructure

References

[1] Asada K, Kanematsu S. Reactivity of thiols with superoxide radicals. Agric Biol Chem, 1976, 40(9): 1891-1892.

[2] Auclair AND, Lill J, Revenga C. The role of climate variability and global warming in the dieback of northern hardwoods. Water Air Soil Pollut, 1996, 91(3–4): 163-186.

[3] Auclair AND, Eglinton PD, Minnemerer SL. Principal forest dieback episodes in Northern hardwoods: development of numeric indices of areal extent and severity. Water Air Soil Pollut, 1997, 93(1–4): 175-198.

[4] Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science, 2006, 312(5776): 1040-1043.

[5] Burke MJ, Gusta LV, Quamme HA, Weiser CJ, Li PH. Freezing and injury in plants. Annu Rev Plant Physiol, 1976, 27(1): 507-528.

[6] Cox RM, Zhu XB. Effects of simulated thaw on xylem cavitation, residual embolism, spring dieback and shoot growth in yellow birch. Tree Physiol, 2003, 23(9): 615-624.

[7] Fracheboud Y, Luquez V, Bjorken L, Sjodin A, Tuominen H, Jansson S. The control of autumn senescence in European aspen. Plant Physiol, 2009, 149(4): 1982-1991.

[8] Groß M, Rainer I, Tranquillini W. Über die Frostresistenzder Fichte mit besonderer Berücksichtigung der Zahl der Gefrierzyklen und der Geschwindigkeit der Temperaturanderung beim Frieren und Auftauen. Forstwiss Cent ver Tharandter Forstl Jahrb, 1991, 110(1): 207-217.

[9] Guy CL, Huber JL, Huber SC. Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol, 1992, 100(1): 502-508.

[10] Hänninen H, Tanino K. Tree seasonality in a warming climate. Trends Plant Sci, 2011, 16(8): 412-416.

[11] Heber U. Freezing injury and uncoupling of phosphorylation from electron transport in chloroplasts. Plant Physiol, 1967, 42(10): 1343-1350.

[12] Heide OM, Prestrud AK. Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol, 2005, 25(1): 109-114.

[13] Hellergren J, Widell S, Lundborg T. Li PH. Freezing injury in purified plasma. Plant cold hardiness, 1987, New York: Alan R. Liss Inc..

[14] Howe GT, Gardner G, Hackett WP, Furnier GR. Phytochrome control of short-day-induced bud set in black cottonwood. Physiol Plant, 1996, 97(1): 95-103.

[15] Iswari S, Palta JP. Plasma membrane ATPase activity following reversible and irreversible freezing injury. Plant Physiol, 1989, 90(3): 1088-1095.

[16] Ko JH, Prassinos C, Keathley D, Han KH. Novel aspects of transcriptional regulation in the winter survival and maintenance mechanism of poplar. Tree Physiol, 2011, 31(2): 208-225.

[17] Larcher W. Physiological basis of evolutionary trends in low temperature resistance of vascular plants. Plant Syst Evol, 1981, 137(3): 145-180.

[18] Lund AE, Livingston WH. Freezing cycles enhance winter injury in Picea rubens. Tree Physiol, 1999, 19(1): 65-69.

[19] Lyons JM. Chilling injury in plants. Ann Rev Plant Physiol, 2003, 24(24): 445-466.

[20] Malone SR, Ashworth EN. Freezing stress response in woody tissues observed using low-temperature scanning electron microscopy and freeze substitution techniques. Plant Physiol, 1991, 95(3): 871-881.

[21] Martz F, Sutinen M-L, Kiviniemi S, Palta JP. Changes in freezing tolerance, plasma membrane H⁺-ATPase activity and fatty acid composition in Pinus resinosa needles during cold acclimation and de-acclimation. Tree Physiol, 2006, 26(6): 783-790.

[22] Mölmann JA, Asante DKA, Jensen JB, Krane MN, Ernstsen A, Junttila O, Olsen JE. Low night temperature and inhibition of gibberellin biosynthesis override phytochrome action and induce bud set and cold acclimation, but not dormancy in PHYA overexpressors and wild-type of hybrid aspen. Plant Cell Environ, 2005, 28(12): 1579-1588.

[23] Nagao M, Matsui K, Uemura M. Klebsormidium flaccidum, a charophycean green alga, exhibits cold acclimation that is closely associated with compatible solute accumulation and ultrastructural changes. Plant Cell Environ, 2008, 31(6): 872-885.

[24] Pramsohler M, Hacker J, Neuner G. Freezing pattern and frost killing temperature of apple (Malus domestica) wood under controlled conditions and in nature. Tree Physiol, 2012, 32(7): 819-828.

[25] Ristic Z, Ashworth EN. Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heyn) cv. Columbia during rapid cold acclimation. Protoplasma, 1993, 172(2): 111-123.

[26] Ristic Z, Ashworth EN. Ultrastructural evidence that lntracellular ice formation and possibly cavitation are the sources of freezing lnjury in supercooling wood tissue of Cornus florida L.. Plant Physiol, 1993, 103(3): 753-761.

[27] Sakai A, Larcher W. Frost survival of plants, 1987, Berlin: Springer

[28] Steponkus PL. Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol, 1984, 35(1): 543-584.

[29] Steponkus PL, Wiest SC. Li PH, Sakai A. Plasma membrane alterations following cold acclimation and freezing. Plant cold hardiness and freezing stress, 1978, New York: Academic Press.

[30] Strand Å, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P, Stitt M. Acclimation of Arabidopsis leaves developing at low temperatures: increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol, 1999, 119(4): 1387-1397.

[31] Strimbeck GR, Dehayes DH. Rapid freezing injury in red spruce seasonal changes in sensitivity and effects of temperature range. Tree Physiol, 2000, 20(3): 187-194.

[32] Strimbeck GR, Vann DR, Johnson AH. In situ experimental freezing produces symptoms of winter injury in red spruce foliage. Tree Physiol, 1991, 9(3): 359-367.

[33] Strimbeck GR, Johnson AH, Vann DR. Midwinter needle temperature and winter injury of montane red spruce. Tree Physiol, 1993, 13(2): 131-144.

[34] Strimbeck GR, Kjellsen TD, Schaberg PG. Dynamics of low-temperature acclimation in temperate and boreal conifer foliage in a mild winter climate. Tree Physiol, 2008, 28(9): 1365-1374.

[35] Tanino KK, Kalcsits L, Silim S, Kendall E, Gray GR. Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol Biol, 2010, 73(1–2): 49-65.

[36] Tao DL, Jin YH. Overwintering injury of trees, 2005, New York: Science Press.

[37] Wang JY, Ao H, Zhang J, Qu GQ. Technology and Principle for plant physiological and biochemical experiments, 2003, Haerbin: Northeast Forestry University Press.

[38] Webb MS, Uemura M, Steponkus P. A comparison of freezing lnjury in oat and rye: two cereals at the extremes of freezing tolerance. Plant Physiol, 1994, 104(2): 467-478.