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The Second Stage of Plant Acclimation to Low Temperatures: the Forgotten Step in Frost Hardening?

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Plant Tolerance to Abiotic Stresses in Agriculture: Role of Genetic Engineering

Part of the book series: NATO Science Series ((ASHT,volume 83))

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Abstract

The primary goal of the contemporary studies on plant acclimation to cold is to understand molecular mechanisms which allow plants to survive freezing stress. However, it has been forgotten that the term “cold acclimation”, originally used (in the 1950’s) by animal physiologists, describe physiological changes in organisms when exposed to low non-freezing temperature. In the 60’s, the term used for plants was defined as “the process of plant adjustment to low temperature (2°C) which occurs in varying degree in hardy and non hardy varieties” (Kenefick, 1963). The results of further studies led to the conclusion that cold acclimation of biennial plants leads to two distinct effects: (1) improved performance of cells at low temperature and (2) increased resistance to freezing (Kacperska, 1989). Similar opinion was presented by Guy (1990) who stated that “The more precise view of cold acclimation (CA) would include two major functions: the more universal adjustment of metabolism and basic cellular function to the biophysical constraints imposed by low temperature (LT), and the induction of freezing tolerance. The first function of CA differentiates chilling-sensitive from chilling-resistant species. The second function of CA discriminates chilling tolerant but freezing sensitive species from those that are freezing tolerant.” In contrast to the above opinions, Palta and Weiss (1993) indicate “cold acclimation per se” as a process which leads to an increase in plant tolerance to freeze-thaw stress. It seems that such a constriction of the term meaning is rather confusing since both cold-induced phenomena, i.e.metabolic adjustment and development of higher resistance to freezing are strongly interrelated.

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References

  • Arora A, Palta JP (1991) A loss in the plasma membrane ATPase activity and its recovery coincides with incipient freeze-thaw injury and postthaw recovery in onion bulb scale tissues. Plant Physiol. 95: 846–852

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Benhamou N (1996) Elicitor-induced plant defence pathways. Trends Plant Science 1(7): 237–240

    Google Scholar 

  • Bertrand A, Robitale G, Castonguay, Nadeau, Boutin R (1997) Changes in ABA and gene expression in cold-acclimated sugar maple. Tree Physiology 17: 31–37

    Article  CAS  PubMed  Google Scholar 

  • Chessin M, Zipf AE, 1990. Alarm system in higher plants. Bot. Rev. 56:193–235

    Google Scholar 

  • Close TJ (1997) Dehydrins: Emergence and a biochemical role of a family of plant dehydration proteins. Physiol. Plant 97: 795–803

    Article  Google Scholar 

  • Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc. Natl. Acad. Sci USA 89: 4938–4941

    Article  Google Scholar 

  • Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N (1998) Accumulation of acidic dehydrin in the vicinity of the plasma membran e during cold acclimation of wheat. Plant Cell 10: 623–638

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • DeNisi P, Zocchi G (1996) The role of calcium in the cold-shock responses. Plant Science 121: (2) 161–166

    Article  CAS  Google Scholar 

  • Derksen J, Wilms FHA, Pierson ES (1990) The plant cytoskeleton: its signifixcance in plant development. Acta Bot. Neerl 39: 1–18

    CAS  Google Scholar 

  • Egierszdorff S., Kacperska A (1999) Low temperature-induced changes in actin cytoskeleton organization in winter rape (Brassica napes L., var. oleifera) suspension cells.. In:Proceedings of the XI Seminar on Plant Frost Hardiness, Kómik, Poland, in press

    Google Scholar 

  • Erlandson G, vonFircks, Jensén P (1987) K’ (Rb+) and Cat+ fluxes in young winter wheat exposed to subzero temperatures. Physiol Plant 69: 258–264

    Article  CAS  Google Scholar 

  • Fluhr R (1998) Ethylene perception: from two-component signal transducers to gene induction. Trend Plant Sci 3 (4): 141–146

    Article  Google Scholar 

  • Goodwin W, Pallas JA, Jenkins GI (1996) Transcripts of a gene encoding a putative cell wall-plasma membrane linker protein are specifically cold-induced in Brassica napus. Plant Mol Biol 31: 771–781

    Article  CAS  PubMed  Google Scholar 

  • Guerro FD, Jones JT, Mullet JE (1990) Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Mol Biol 15: 11–26

    Article  Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Anna Rev. Plant Physiol. Mol. Biol. 41: 187–223

    Article  CAS  Google Scholar 

  • Hellergren J, Widell S, Lundborg T (1987) Freezing injury in purified plasma membranes from cold-acclimated and non-acclimated needles of Pinus sylvestris: is the plasma membrane-bound ion-stimulated ATPase the primary site of freezing injury? In Li PH. ed. Plant Cold Hardiness. Alan R. Liss, Inc. New York, pp.211–220

    Google Scholar 

  • Hiilovaara-Teijo M, Palva E (1999) Molecular responses in cold-adapted plants In Margesin R and Schinner F, eds. Cold-Adapted Organisms. Ecology, Physiology, Enzymology and Molecular Biology. Springer, Berlin, Heidelberg, New York, pp. 349–384

    Google Scholar 

  • Hincha DK, Meins FM Jr, Schmidt JM (1997) ß-1,3-glucanase is cryoprotective in vitro and is accumulated in leaves during cold acclimation. Plant Physiol 114: 1077–1083

    PubMed Central  CAS  PubMed  Google Scholar 

  • Howell GS, Weiser CJ (1970) The environmental control of cold acclimation in apple. Plant Physiol 45: 390–394

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes MA, Dunn MA (1996) The molecular biology of plant acclimation and freezing tolerance. J. Exp. Bot. 47: 291–305

    Article  CAS  Google Scholar 

  • Jian LC, Sun LH, Dong HZ, Sun DL (1982) Changes in AtPase activity during freezing injury and cold hardening. ? In PH Li and A. Sakai, eds. Plant Cold Hardiness and Freezing Stress: Mechanisms and Crop Implications, Vol. 2. Academic Press, New York, London, pp. 243–260

    Google Scholar 

  • Jian LC, Sun LH, Wei XY (1993) Microtubules cytoskeleton in relation to plant cold hardiness In PH Li, L. Christersson, eds. Advances in Plant Cold Hardiness, CRC Press, Boca Raton, Ann Arbor, London, Tokyo, pp. 125–138

    Google Scholar 

  • Kacperska A (1989) Metabolic consequences of low temperature stress in chilling-insensitive plants. In PH. Li, ed. Low Temperature Stress Physiology in Crops. CRC Press, Boca Raton, Fl. pp. 27–40

    Google Scholar 

  • Kacperska A (1993) Water potential alterations — a prerequisite or triggering stimulus for the development freezing tolerance in overwintering herbaceous plants? In PH Li, Christersson L, eds. Advances in Plant Cold Hardiness, CRC Press, Boca Raton, Ann Arbor, London, Tokyo, pp.73–92

    Google Scholar 

  • Kacperska A (1997) Ethylene synthesis and a role in plant responses to different stressors In Kanellis AK, Chang C, Kende H, Grierson D, eds. Biology and Biotechnology of the Plant Hormone Ethylene, Kluwer Academic Publishers, Dordrecht, Boston, London, pp. 207–216

    Chapter  Google Scholar 

  • Kacperska A (1999) Plant responses to low temperature: signaling pathways involved in plant acclimation In: Margesin R Schirmer F, eds. Cold-Adapted Organisms. Ecology, Physiology, Enzymology and Molecular Biology, Springer-Verlag, Berlin, Heidelberg, New York, pp. 79–104

    Google Scholar 

  • Kacperska-Palacz A (1978) Mechanisms of cold acclimation in herbaceous plants. In Li PH, Sakai A, ads. Plant Cold Hardiness and Freezing Stress, Academic Press, New York, pp.139–152

    Chapter  Google Scholar 

  • Kacperska A, Kubacka-Z@balska M (1987) Is lipoxygenase involved in the formation of ethylene from ACC? Physiol. Plant 64: 333–338

    Google Scholar 

  • Kacperska A, Kulesza L (1987) Frost resistance of winter rape leaves as related to the changes in water potential and growth capability. Physiol. Plant 71: 483–488

    Google Scholar 

  • Kenefick D (1963). Crop Science 3: 202–205

    Google Scholar 

  • Kerr GP, Carter JV (1990) Relationship between freezing tolerance of root-tip cells and cold stability of microtubules in rye (Secale cereale L. cv Puma). Plant Physiol. 93: 77–82

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation Plant Cell 8: 489–503

    CAS  Google Scholar 

  • Kozbial PZ, Jerzmanowski A, Shirsat AH, Kacperska A (1998) Transient freezing regulates expression of extensin-type genes in winter oilseed rape. Physiol. Plant 103:264–270

    Article  CAS  Google Scholar 

  • Kozbial P, Pukacki P, Jerzmanowski A, Kacperska I (1997) New approach to the identification of proteins involved in plant resistance to cold. In:Sowiiíski P, Zagdaríska B, Aniol A, Pithan K, eds. Crop development for the cool and wet regions of Europe, COST 814, European Communities, Luxembbourg, pp. 269–273

    Google Scholar 

  • Kubacka-Zębalska M, Kacperska A (1999) Low temperature-induced modifications of cell wall content and polysaccharide composition in leaves of winter oilseed rape Brassica napus L. var. oleifera. Plant Sci, in press

    Google Scholar 

  • Leubner-Metzger G, Petruzzelli L, Waldvogel R, Vögeli-Lange, Meins F, Jr (1998) Ethylene-responsive element binding proteins (EREBP) expression and transcriptional regulation of class I (3–1,3-glucanase during tobacco seed germination. Plant Mol. Biol 38: 785–795

    Article  CAS  PubMed  Google Scholar 

  • Lewis BD, Karlin-Neumann K, Davis RW, Spalding EP (1997) Ce-activated anion channels and membrane depolarizations induced by blue light and cold in Arabidopsis seedlings. Plant Physiol 114: 1327–1334

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Livingstone DP III, Henson CA Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening. Plant Physiol 116: 403–408

    Google Scholar 

  • Mauch F, Kmecl A, Schaffrath U, Volrath S, GÖrlach J, Ward E, Ryals J, Dudler R (1997) Mechanosensitive expression of lipoxygenase gene in wheat. Plant Physiol 114: 1567–1560

    Article  Google Scholar 

  • Minorsky PV (1985) An heuristic hypothesis of chilling injury in plants: a role for calciu as the primary physiological transducer of injury. Plant, Cell Environ 8: 75–94

    Article  CAS  Google Scholar 

  • Minorsky PV (1989) Temperature sensing by plants: a review and hypothesis. Plant Cell Environ 12: 119–135

    Article  CAS  Google Scholar 

  • Monroy AF, Castonguay Y, Laberge S, Sarhan F, Vezina LP, Dhindsa RS (1993) A new cold-induced alfalfa gene is associated with enhanced hardening at subzero temperature. Plant Physiol 102: 873–879

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Monroy AF, Dhindsa RS (1995) Low temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 °C. Plant Cell 7: 321–331

    PubMed Central  CAS  PubMed  Google Scholar 

  • Monroy AF, Labbé E, Dhindsa RS (1997) Low temperature perception in plants: effects of cold on protein phosphorylation in cell-free extracts. FEBS Letters 410: 206–209

    Article  CAS  PubMed  Google Scholar 

  • Monroy AF, Sangwan V, Dhindsa RS (1998) Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold-inactivation. Plant Journal 13 (5): 653–660

    Article  CAS  Google Scholar 

  • Monroy AF, Sarhan F, Dhindsa RS (1993) Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression. Evidence for a role of calcium Plant Physiol 102: 1227–1235

    CAS  Google Scholar 

  • Morelli JK, Zhou W, Yu J, Lu C, Vayda ME (1998). Actin depolymerization affects stress-induced translational activity of potato tuber tissue. Plant Physiol 116: 1227–1237

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Munnik T, Arisz S, de Vrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7: 2197–2210

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115: 875–879 Olien CR (1984) An adaptive response of rye to freezing. Crop Sci 24: 51–54

    Google Scholar 

  • Palta JP, Jensen KG, Li PH (1982) Cell membrane alterations following freeze-thaw cycle: ion leakage injury and recovery In PH Li and A Sakai, eds. Plant Cold Hardiness and Freezing Stress: Mechanisms and Crop Implications, Vol. 2. Academic Press, New York, London, pp. 221–242

    Chapter  Google Scholar 

  • Palta JP, Simon G (1993) Breeding potential for improvement of freezing stress resistance: genetic separation of freezing tolerance, freezing avoidance, and capacity to cold acclimate. In PH Li, Cristersson, eds. Advances in Plant Cold Hardiness, CRC Press, Boca Raton, Ann Arbor, London, Tokyo, pp. 299–310

    Google Scholar 

  • Palta JP, Weiss L, (1993) Ice formationand freezing injury: an overview on the survival mechanisms and molecular aspects of injury and cold acclimation in herbaceous plants. In PH Li, L. Christersson, eds. Advances in Plant Cold Hardiness, CRC Press, Boca Raton, Ann Arbor, London, Tokyo, pp. 143–176

    Google Scholar 

  • Palva ET (1994) Gene expression under low temperature stress. In Basra AS, ed. Stress-Induced Gene Expression in Plants. Harwood Acad. Pub’, Chur, Switzerland, pp. 103–130

    Google Scholar 

  • Piñeroz M, Tester M (1997). Calcium channels in higher plants: selectivity, regulation and pharmacology. J. Exp. Bot. 48: 551–577

    Article  Google Scholar 

  • Polisensky DH, Braam J (1996) Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant PhysioL 111: 1271–1279

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reaney MJ, Gusta LV (1998). Modeling sequential responses of plant cells to freezing and thawing In Margesin R and Schinner F, eds. Cold-Adapted Organisms. Ecology, Physiology, Enzymology and Molecular Biology. Springer, Berlin, Heidelberg, New York, pp.119–135

    Google Scholar 

  • Repo T, Hiekkala P, Hietala T, Tahvanainen L (1997) Intracellular resistance correlates with initial stage of frost hardening in willow (Salix viminalis). Physiol Plant. 101: 627–634

    Article  CAS  Google Scholar 

  • Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trend Plant Sci 2: 152–159

    Article  Google Scholar 

  • Rickauer M, Fournier J, Pouénat, Berthalon E, Bottin A, Esquerré-Tugayé (1990) Early changes in ethyelen synthesis and lipoxygenase activity during defense induction in tobacco cells. Plant Physiol Biochem 28 (5) 647–653

    CAS  Google Scholar 

  • Saniewski M (1997) The role ofjasmonates in ethylene biosynthesis In Kanellis AK, Chang C, Kende H, Grierson D, eds. Biology and Biotechnology of the Plant Hormone Ethylene, Kluwer Academic Publishers, Dordrecht, Boston, London, pp. 39–46

    Chapter  Google Scholar 

  • Sawicka T, Kacperska A (1995) Soluble and cell wall-associated ß-galactosidases from cold-grown winter rape (Brassica napus L. var. oleifera) leaves. J. Plant Physiol 145: 357–362

    Article  CAS  Google Scholar 

  • Schaller GE, Sussman MR (1988) Phosphorylation of plasma membrane H’-ATPase activity of com roots. Plant Sci 40: 153–159

    Google Scholar 

  • Shirsat AH,Bell A,SpenceJ,Harris JN. 1996a. The Brassica napus extA extensin gene is expressed in regions of the plant subject to tensile stress. Planta 199: 618–624

    Article  CAS  Google Scholar 

  • Shirsat AH, Wieczorek D, Kozbial P (1996b) A gene for Brassica napus extensin is differentially expressed in wounding. Plant Mol Biol 30: 1291–1300

    Article  CAS  PubMed  Google Scholar 

  • Sikorska E, Kacperska A (1982) Freezing-induced membrane alterations: injury or adaptation? In PH Li and A. Sakai, eds. Plant Cold Hardiness and Freezing Stress: Mechanisms and Crop Implications, VoL 2. Academic Press, New York, London, pp. 261–273

    Chapter  Google Scholar 

  • Sikorska E, Kacperska-Palacz (1980) Frost-induced phospholipid changes in cold-acclimated and non-acclimated rape leaves. Physiol Plant 48: 201–206

    Article  CAS  Google Scholar 

  • Sikorska E, Ondrias K, Farkas (1981) Physical properties of membranes of cold-hardened and non-hardened winter rape plants. Acta Biol. Acad. Sci Hungary 32: 267–272

    CAS  Google Scholar 

  • Siminovitch D, Rheaume B, Pomeroy K, Lepage M (1968) Phospholipid, protein and nucleic acid increases in protoplasm and membrane structure associated with development of extreme freezin resistance in black locusust tree cells. Cryobiology 5: 202–225

    Article  CAS  PubMed  Google Scholar 

  • Smoleñska-Sym, G, Gawroríska H, Kacperska A (1995) Modifications in abscisic acid level in winter oilseed rape leaves during acclimation of plants to freezing temperatures. Plant Growth Regulation 17: 61–65

    Google Scholar 

  • Smoleiíska-Sym G, Kacperska A (1996) Inositol 1,4,5-trisphosphate formation in leaves of winter oilseed

    Google Scholar 

  • rape plants in response to freezing, tissue water potential and abscisic acid. Physiol. Plant 96: 692–698

    Google Scholar 

  • Sobczyk EA, Kacperska-Palacz (1980) Changes in some enzyme activities during cold acclimation of winter rape plants. Acta Physiol. Plant 2: 123–131

    CAS  Google Scholar 

  • Solecka D, Kacperska A (1995) Phenylalanine ammonia-lyase activity in winter oilseed rape plants as affected by acclimation of plants to low temperature. Plant Physiol Biochem 33 (5): 585–591

    CAS  Google Scholar 

  • Stefanowska M, Kural M, Kubacka-Zębalska M, Kacperska A (1990) Low temperature affects pattern of leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var. oleifera) plants. Ann. Bot, in press

    Google Scholar 

  • Tahtiharju S, Sangwan V, Monroy AF, Dhindsa RS, Borg M (1997) The induction ofkin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta 203 (4): 442–447

    Article  CAS  PubMed  Google Scholar 

  • Tao D-L, öquist G, Wingsle G (1998) Active oxygen scavengers during cold acclimation of Scots pine seedlings in relation to freezing tolerance. Cryobiology 37: 38–45

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF (1990) Molecular genetics of cold acclimation in higher plants. Adv. Genet. 28: 99–131

    Article  CAS  Google Scholar 

  • Thomashow MF (1993) Genes induced during cold acclimation in higher plants In P. Steponkus, ed. Advances in Low Temperature Biology, Vol. 2, JAI Press Ltd., Hampton Hill, UK, pp. 183–210

    Google Scholar 

  • Trunova TL (1965) Light and temperature systems in hardening of winter wheat and the significance of oligosaccharides for frost resistance. FizjoL Rast 12: 70–77

    Google Scholar 

  • Tyurina MM, Gogoleva GA, Jegurasdova AS, Bulatova TG (1978) Interaction between development of frost resistance and dormancy in plants. Acta Hortic 81: 51–60

    Google Scholar 

  • Tumanov II, Krasavtsev OA (1959) Zakalivanie sevemych drevesnych rastenii otricatelvnymi temperaturami (Hardening of northern woody plants by negative temperature treatment). Fiziol Rast 10:654-

    Google Scholar 

  • Wang X (1997) Molecular analysis of phospholipase D. Trends Plant Sci 2: 261–266 Weiser CJ (1970) Cold resistance and injury in woody plants. Science 169: 1269–1278

    Google Scholar 

  • Yoshida S (1974) Studies on lipid changes associated with frost hardiness in cortex of woody plants. Contrib. Inst. Low Temp. Sci., Ser B, 18:1–43

    CAS  Google Scholar 

  • Yoshida M, Moriyama M, Shimokawa S, Nakamura Y (1997) Seasonal changes in the physical state of crown water associated with freezing tolerance in winter wheat. Physiol. Plant 99: 363–370

    Article  CAS  Google Scholar 

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Kacperslda, A. (2000). The Second Stage of Plant Acclimation to Low Temperatures: the Forgotten Step in Frost Hardening?. In: Cherry, J.H., Locy, R.D., Rychter, A. (eds) Plant Tolerance to Abiotic Stresses in Agriculture: Role of Genetic Engineering. NATO Science Series, vol 83. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-4323-3_6

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