SUMMARY
The strategies used by living organisms to survive under low and freezing temperatures reveal the extraordinary adaptability of life on Earth.
Understanding the molecular mechanisms underlying cold adaptation and freezing survival will provide new insights into the existing relationships
between living organisms and their environment, and the possibility of developing multiple biotechnological applications. In the case of plants,
the use of classical genetic and new "omics" approaches is allowing to the identification of new elements involved in regulating the cold
acclimation response. The challenge ahead is to determine temperature-perception molecules and mechanisms, to uncover new internodes of multiple
responses, and to integrate the regulation not only at the transcriptome but also at proteome and metabolome levels. Attaining these goals will
significantly contribute global understanding the adaptive strategies plants have evolved to cope with hostile environmental conditions, and to
the development biotechnological strategies to improve crop tolerance to freezing and other important abiotic stresses.
KEY WORDS Arabidopsis; low temperature response; cold acclimation; freezing tolerance; cold signalling
REFERENCES
Abarca D, Madueno F, Martinez-Zapater JM, Salinas J: Dimerization of Arabidopsis 14-3-3 proteins: structural requirements within the N-terminal
domain and effect of calcium. FEBS Lett 462:377-382, 1999.
Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK: A R2R3 type MYB transcription factor is involved in the cold regulation of
CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636-37645, 2006.
Aguilar PS, Cronan JE, Jr., de Mendoza D: A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipids desaturase. J
Bacteriol 180:2194-2200, 1998.
Alboresi A, Ballottari M, Hienerwadel R, Giacometti GM, Morosinotto T: Antenna complexes protect Photosystem I from photoinhibition. BMC Plant
Biol 9:article 71, 2009.
Alonso-Blanco C, Gomez-Mena C, Llorente F, Koornneef M, Salinas J, Martinez-Zapater JM: Genetic and molecular analyses of natural variation
indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol 139:1304-1312,
2005.
Capel J, Jarillo JA, Salinas J, Martinez-Zapater JM: Two homologous low-temperature-inducible genes from Arabidopsis encode highly hydrophobic
proteins. Plant Physiol 115:569-576, 1997.
Capel J, Jarillo JA, Madueno F, Jorquera MJ, Martinez-Zapater JM, Salinas J: Low temperature regulates Arabidopsis Lhcb gene expression in
a light-independent manner. Plant J 13:411-418, 1998.
Catala R, Salinas J: Regulatory mechanisms involved in cold acclimation response. Span J Agric Res 6:211-220, 2008.
Catala R, Santos E, Alonso JM, Ecker JR, Martinez-Zapater JM, Salinas J: Mutations in the Ca2+/H+ transporter CAX1 increase
CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940-2951, 2003.
Chen TH, Gusta LV: Abscisic acid-Induced freezing resistance in cultured plant cells. Plant Physiol 73:71-75, 1983.
Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK: ICE1: a regulator of cold-induced transcriptome and freezing tolerance in
Arabidopsis. Genes Dev 17:1043-1054, 2003.
Christie PJ, Hahn M, Walbot V: Low-temperature accumulation of alcohol dehydrogenase-1 mRNA and protein activity in maize and rice seedlings.
Plant Physiol 95:699-706, 1991.
Christie PJ, Alfenito MR, Walbot V: Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of
transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194:541-549, 1994.
Cossins AR: Temperature Adaptation in Biological Membranes. Portland Press, London 1994, pp. 63-76.
Fowler S, Thomashow MF: Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in
addition to the CBF cold response pathway. Plant Cell 14:1675-1690, 2002.
Fursova OV, Pogorelko GV, Tarasov VA: Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in
Arabidopsis thaliana. Gene 15:98-103, 2009.
Gilmour SJ, Thomashow MF: Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17:1233-1240,
1991.
Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF: Low temperature regulation of the Arabidopsis CBF family of AP2
transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433-442, 1998.
Gilmour SJ, Fowler SG, Thomashow MF: Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol
Biol 54:767-781, 2004.
Gocheva YG, Tosi S, Krumova ET, Slokoska LS, Miteva JG, Vassilev SV, Angelova MB: Temperature downshift induces antioxidant response in fungi
isolated from Antarctica. Extremophiles 13:273-281, 2009.
Gray GR, Chauvin LP, Sarhan F, Huner N: Cold acclimation and freezing tolerance (A complex interaction of light and temperature). Plant Physiol
114:467-474, 1997.
Harvaux M, Kloppstech K: The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature
investigated in Arabidopsis npq and tt mutants. Planta 213:953-966, 2001.
Hayward SAL, Murray PA, Gracey AY, Cossins AR: Beyond the lipid hypothesis: Mechanisms underlying plasticity in inducible cold tolerance. Adv Exp
Med Biol 594:132-142, 2007.
Heino P, Sandman G, Lang V, Nordin K, Palva ET: Abscisic acid deficiency prevents development of freezing tolerance in Arabidopsis thaliana
(L.) Heynh. Theor Appl Genet 79:801-806, 1990.
Hirschi KD, Zhen RG, Cunningham KW, Rea PA, Fink GR: CAX1, an H+/Ca2+ antiporter from Arabidopsis. Proc Natl Acad Sci USA
93:8782-8786, 1996.
Ishitani M, Xiong L, Stevenson B, Zhu JK: Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and
convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9:1935-1949, 1997.
Jarillo JA, Leyva A, Salinas J, Martinez-Zapater JM: Low temperature induces the accumulation of alcohol dehydrogenase mRNA in Arabidopsis
thaliana, a chilling-tolerant plant. Plant Physiol 101:833-837, 1993.
Jarillo JA, Capel J, Leyva A, Martinez-Zapater JM, Salinas J: Two related low-temperature-inducible genes of Arabidopsis encode proteins showing
high homology to 14-3-3 proteins, a family of putative kinase regulators. Plant Mol Biol 25:693-704, 1994.
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K: Improving plant drought, salt, and freezing tolerance by gene transfer of a single
stress-inducible transcription factor. Nat Biotechnol 17:287-291, 1999.
Kawamura Y, Uemura M: Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold
acclimation. Plant J 36:141-154, 2003.
Knight H: Calcium signalling during abiotic stress in plants. Int Rev Cytol 195:269-324, 2000.
Krol M, Ivanov AG, Jansson S, Kloppstech K, Huner NP: Greening under high light or cold temperature affects the level of xanthophyll-cycle
pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the chlorina f2 mutant. Plant Physiol
120:193-204, 1999.
Lang V, Heino P, Palva ET: Low temperature acclimation and treatment with exogenous abscisic acid induce common polypeptides in Arabidopsis
thaliana (L.) Heinh. Theor Appl Genet 77:729-734, 1989.
Lee BH, Henderson DA, Zhu JK: The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155-3175, 2005.
Levitt J: Responses of Plants to Environmental Stresses: chilling, freezing and high temperatures stresses. Academic Press, New York,
1980.
Leyva A, Jarillo JA, Salinas J, Martinez-Zapater JM: Low temperature Induces the Accumulation of Phenylalanine Ammonia-Lyase and Chalcone Synthase
mRNAs of Arabidopsis thaliana in a Light-Dependent Manner. Plant Physiol 108:39-46, 1995.
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K: Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA
binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in
Arabidopsis. Plant Cell 10:1391-1406, 1998.
Llorente F, Oliveros JC, Martinez-Zapater JM, Salinas J: A freezing-sensitive mutant of Arabidopsis, frs1, is a new aba3 allele.
Planta 211:648-655, 2000.
Llorente F, Lopez-Cobollo RM, Catala R, Martinez-Zapater JM, Salinas J: A novel cold-inducible gene from Arabidopsis, RCI3, encodes a
peroxidase that constitutes a component for stress tolerance. Plant J 32:13-24, 2002.
Mancinelli AL: Photoregulation of anthocyanin synthesis: VIII. Effect of light pretreatments. Plant Physiol 75:447-453, 1984.
Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N,
Toyoda T, Shinozaki K, Seki M: Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling
array. Plant Cell Physiol 49:1135-1149, 2008.
Mazzucotelli E, Belloni S, Marone D, De Leonardis A, Guerra D, Di Fonzo N, Cattivelli L, Mastrangelo A: The E3 ubiquitin ligase gene family
in plants: regulation by degradation. Current Genomics 7:509-522, 2006.
Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J: The Arabidopsis CBF gene family is composed of three genes encoding AP2
domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463-470,
1999.
Medina J, Catala R, Salinas J: Developmental and stress regulation of RCI2A and RCI2B, two cold-inducible genes of Arabidopsis
encoding highly conserved hydrophobic proteins. Plant Physiol 125:1655-1666, 2001.
Medina J, Rodriguez-Franco M, Penalosa A, Carrascosa MJ, Neuhaus G, Salinas J: Arabidopsis mutants deregulated in RCI2A expression reveal
new signalling pathways in abiotic stress responses. Plant J 42:586-597, 2005.
Medina J, Ballesteros ML, Salinas J: Phylogenetic and functional analysis of Arabidopsis RCI2 genes. J Exp Bot 58:4333-4346, 2007.
Monroy AF, Sangwan V, Dhindsa RS: Low temperature signal transduction during cold acclimation: protein phophatase 2A as an early target for
cold-inactivation. Plant J 13:653-660, 1998.
Murata N, Los DA: Membrane fluidity and temperature perception. Plant Physiol 115:875-879, 1997.
Novillo F, Alonso JM, Ecker JR, Salinas J: CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a
central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101:3985-3990, 2004.
Novillo F, Medina J, Salinas J: Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene
classes in the CBF regulon. Proc Natl Acad Sci USA 104:21002-21007, 2007.
Orvar BL, Sangwan V, Omann F, Dhindsa RS: Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant
J 23:785-794, 2000.
Penfield S: Temperature perception and signal transduction in plants. New Phytol 179:615-628, 2008.
Pineros M, Tester M: Characterization of the high-affinity verapamil binding site in a plant plasma membrane Ca2+-selective channel. J
Membr Biol 157:139-145, 1997.
Roberts MR, Salinas J, Collinge DB: 14-3-3 proteins and the response to abiotic and biotic stress. Plant Mol Biol 50:1031-1039, 2002.
Salinas J: Molecular mechanisms of signal transduction in cold acclimation. In Hames BD, Glover DM: Frontiers in Molecular Biology, Oxford
University Press, Oxford 2002, pp: 116-139.
Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS: Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant
MAP kinase pathways. Plant J 31:629-638, 2002.
Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, Botella MA: Arabidopsis
synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20:3374-3388, 2008.
Schulze ED, Beck E, Muller-Hohenstein K: Plant Ecology. Springer, Berlin/Heidelberg, 2005.
Stockinger EJ, Gilmour SJ, Thomashow MF: Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to
the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc
Natl Acad Sci USA 94:1035-1040, 1997.
Storey KB: Reptile freeze tolerance: metabolism and gene expression. Cryobiology 52:1-16, 2006.
Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N: Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol
Microbiol 40:235-244, 2001.
Tahtiharju S, Sangwan V, Monroy AF, Dhindsa RS, Borg M: The induction of kin genes in cold-acclimating Arabidopsis thaliana.
Evidence of a role for calcium. Planta 203:442-447, 1997.
Van Buskirk HA, Thomashow MF: Arabidopsis transcription factors regulating cold acclimation. Physiol Plant 126:72-80, 2006.
Venketesh S, Dayananda C: Properties, potentials and prospects of antifreezing proteins. Crit Rev on Biotechnol 28:57-82, 2008.
Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF: Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature
transcriptome of Arabidopsis. Plant J 41:195-211, 2005.
Voituron Y, Servais S, Romestaing C, Douki T, Barre H: Oxidative DNA damage and antioxidant defenses in the European common lizard (Lacerta
vivipara) in supercooled and frozen states. Cryobiology 51:74-82, 2005.
Wei H, Dhanaraj AL, Arora R, Rowland LJ, Fu Y, Sun L: Identification of cold acclimation-responsive Rhododendron genes for lipid
metabolism, membrane transport and lignin biosynthesis: importance of moderately abundant ESTs in genomic studies. Plant Cell Environ 29:558-570,
2006.
Xiong L, Ishitani M, Lee H, Zhu JK: The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and
osmotic stress-responsive gene expression. Plant Cell 13:2063-2083, 2001.
Xiong L, Schumaker KS, Zhu JK: Cell signalling during cold, drought, and salt stress. Plant Cell 14 (Suppl):S165-183, 2002.
Yamaguchi-Shinozaki K, Shinozaki K: Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu
Rev Plant Biol 57:781-803, 2006.
Yamazaki T, Kawamura Y, Minami A, Uemura M: Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin
SYT1. Plant Cell 20:3389-3404, 2008.
Yancey PH: Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol
208:2819-2830, 2005.
Zeller G, Henz SR, Widmer CK, Sachsenberg T, Ratsch G, Weigel D, Laubinger S: Stress-induced changes in the Arabidopsis thaliana
transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068-1082, 2009.
Zhu J, Dong CH, Zhu JK: Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin
Plant Biol 10:290-295, 2007.
|
CITED
0
|