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Vol. 65 No. 2: Issue 2

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Simultaneous responses of photosystem II and soluble proteins of rapeseed to cold acclimation

https://doi.org/10.14715/cmb/2019.65.2.7
Ali Arminian
Department of Agronomy and Plant Breeding, Faculty of Agriculture, Ilam University, Ilam, Iran
Reza Dehghani Bidgoli
Department of Rangeland and Watershed Management, University of Kashan, Kashan, Iran

Corresponding Author(s) : Ali Arminian

a.arminian@ilam.ac.ir

Cellular and Molecular Biology, Vol. 65 No. 2: Issue 2

Abstract

This experiment was conducted to assess the quantitative and qualitative changes in soluble proteins as well as some chlorophyll fluorescence parameters in the leaves of a winter canola (Brassica napus L., cv. Licord) under continuous low temperature. Over the experiment, seedlings were initially grown at 15/10 °C (d/n). At fourth fully expanded leafy stage (day 30), a part of the plants were transferred to 4/2°C for 4 weeks. Plants were sampled for protein extraction from leaves in which chlorophyll fluorescence parameters (Fo, Fv, Fm, Fv/Fo, Fm/Fo, Fv/Fm, Fo´, FV´, Fm´ and some other calculated) were also measured. The results showed a clear increase in soluble proteins quantity caused by cold treatment. The enhancements appeared abruptly following the cold exposure to 4°C and lasted. The electrophoretic protein patterns showed changes in the intensity of some polypeptides, besides, induction a new probable protein weighing 47-kW in response to cold treatment. Cold-triggered reduction in maximum quantum yield of PSII (Fv/Fm) was connected especially with drastic decreasing Fv and Fm. Interestingly, high quantitative amounts of soluble proteins along with induction of the new probable polypeptide induced at cold temperature, were attributed to low deduction of maximum quantum yield of PSII. Additionally, more imperative chlorophyll fluorescence parameters changed e.g. qP, NPQ, qL, Y(II) or Ñ„PSII etc at light. Nowadays, radar charts or spider plots are the most sophisticated multivariate statistical tools representing physiological responses of plants to abiotic stress conditions or even morphophysiological studies of plants. In rapeseed many researches performed by applying the radar charts for low temperature stresses and interpreted their effects more advancely than common statistical tools. We observed a good representation of the chl fluorescence parameters fluctuations using radar plots. Overall, cold-induced soluble proteins accumulated after longer cold-acclimation, can contribute in photosynthetic apparatus protection against low-temperature damages.

Keywords

Canola Chlorophyll fluorescence Cold acclimation Protein.
Arminian, A., & Dehghani Bidgoli, R. (2019). Simultaneous responses of photosystem II and soluble proteins of rapeseed to cold acclimation. Cellular and Molecular Biology, 65(2), 37–49. https://doi.org/10.14715/cmb/2019.65.2.7
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References
  1. References
  2. Moieni-Korbekandi Z, Karimzadeh G, Sharifi M. Cold-induced changes of proline, malondialdehyde and chlorophyll in spring canola cultivars. J Plant Physiol Breed 2014; 4(1): 1-11. (In Persian).
  3. Beckman C. Vegetable oils: Competition in a changing market. Bi-weekly Bulletin. Agriculture and Agri-Food Canada: Surinder Kumar Gupta. 2009. Biology and Breeding of Crucifers (Edn.) CRC Press.; 2005.
  4. Rapacz M, Markowski A. Winter hardiness, frost resistance and vernalization requirement of european winter oilseed rape (Brassica napus var. Oleifera) cultivars within the last 20 years. J Agr Crop Sci 1999; 183(4): 243-253.
  5. Espevig T, DaCosta M, Hoffman L et al. Freezing tolerance and carbohydrate changes of two Agrostis species during cold acclimation. Crop Sci 2011; 51: 1188-1197.
  6. Guan H. Physiology of cold acclimation and deacclimation responses of cool-season grasses: carbon and hormone metabolism, University of Massachusetts, Amherst. ; 2014.
  7. Thomashow MF. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Ann Rev Plant Biol 1999; 50(1): 571-599.
  8. Trischuk RG, Schilling BS, Low NH, Gray GR, Gusta LV. Cold acclimation, de-acclimation and re-acclimation of spring canola, winter canola and winter wheat: The role of carbohydrates, cold-induced stress proteins and vernalization. Env Exp Bot 2014; 106: 156-163.
  9. Fiebelkorn D, Rahman M. Development of a protocol for frost-tolerance evaluation in rapeseed/canola (Brassica napus L.). The Crop J 2016; 4: 147-152.
  10. Rapacz M, Janowiak F. Relationship between prehardening, photosynthetic activity at cold acclimation temperatures and frost tolerance in winter eape (Brassica napus var. oleifera). The consequences for the reliability of fost resistance Estimation under Controlled Conditions. J Agr Crop Sci 1999b; 182(1): 57-63.
  11. Hekneby M, Antolin MC, Sanchez-Diaz M. Frost resistance and biochemical changes during cold acclimation in different annual legumes. Env Exp Bot 2006; 55(3): 305-314.
  12. Rapacz M, Wolanin B, Hura K, Tyrka M. The effects of cold acclimation on photosynthetic apparatus and the expression of COR14b in four genotypes of barley (Hordeum vulgare) contrasting in their tolerance to freezing and high-light treatment in cold conditions. Ann Bot 2008; 101(5): 689-699.
  13. Zhang C, Fei S, Warnke S, Li L, Hannapel D. Identification of genes associated with cold acclimation in perennial ryegrass. J Plant Physiol 2009; 166(13): 1436-1445.
  14. Asghari A, Mohammadi SA, Moghaddam M, Toorchi M, Mohammadinasab AD. Analysis of quantitative trait loci associated with freezing tolerance in rapeseed (Brassica napus L.). Biotech Biotech Equipment 2008; 220: 548-552.
  15. Hincha DK. Cryoprotectin: a plant lipid–transfer protein homologue that stabilizes membranes during freezing. Philosophical Transactions Royal Soc London Series B: Biol Sci 2002; 357(1423): 909-916.
  16. Iba K. Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Ann Rev Plant Biol 2002; 53(1): 225-245.
  17. McClinchey SL, Kott LS. Production of mutants with high cold tolerance in spring canola (Brassica napus). Euphytica 2008; 162(1): 51-67.
  18. Asghari A, Mohammadi SA, Moghaddam M, Mohammaddoost HR. QTL analysis for cold resistance-related traits in Brassica napus using RAPD markers. J Food Agr Env 2007; 5(3): 188-192.
  19. Guy CL. Cold accelimation and freezing stress tolerance: role of protein metabolism. Ann Rev Plant Physiol Plant Mol Biol 1990; 41(1): 187-223.
  20. Huner NPA, í–quist G, Hurry VM, Krol M, Falk S, Griffith M. Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photos Res 1993; 37(1): 19-39.
  21. Levitt J. Responses of plants to environmental stresses. v1. Chilling, freezing, and high temperature Stresses: Academic Press. New York; 1980.
  22. Gray GR, Cauvin LP, Sarhan F, Huner NPA. Cold acclimation and freezing tolerance. A complex interaction of light and temperature. Plant Physiol 1997; 114: 467–474.
  23. Chinnusamy V, Zhu J, Zhu JK. Cold stress regulation of gene expression in plants. Trends Plant Sci 2007; 12(10): 444-451.
  24. Howarth CJ, Ougham HJ. Gene expression under temperature stress. New Phytologist 1993; 125(1): 1-26.
  25. Hughes MA, Dunn MA. The molecular biology of plant acclimation to low temperature. J Exp Bot 1996; 47: 291-305.
  26. Theocharis A, Clement C, Barka EA. Physiological and molecular changes in plants grown at low temperatures. Planta 2012; 235: 1091–1105.
  27. Monroy AF, Sarhan F, Dhindsa RS. Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression (evidence for a role of calcium). Plant Physiol 1993; 102(4): 1227-1235.
  28. Siegenthaler P-A, Murata N. Lipids in Photosynthesis: Structure, Function and Genetics: KLUWER ACADEMIC PUBLISHERS.; 1998.
  29. Wanner LA, Junttila O. Cold-induced freezing tolerance in Arabidopsis. Plant Physiol 1999; 120(2): 391-399.
  30. Thomashow MF. Genes induced during cold acclimation in higher plants. Advances in Low-temperature Biology 1993; 2: 183-210.
  31. Vátámvás P, Prášil IT. WCS120 protein family and frost tolerance during cold acclimation, deacclimation and reacclimation of winter wheat. Plant Physiol Biochem 2008; 46(11): 970-976.
  32. Saez-Vasquez J, Gallois P, Delseny M. Accumulation and nuclear targeting of BnC24, a Brassica napus ribosomal protein corresponding to a mRNA accumulating in response to cold treatment. Plant Sci 2000; 156(1): 35-46.
  33. Sangwan V, Foulds I, Singh J, Dhindsa RS. Cold activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx. The Plant J 2001; 27(1): 1-12.
  34. Jeong Y, Choy Y, Joo H et al. Identification and analysis of cold stress-inducible genes in Korean rapeseed varieties. J Plant Biol 2012; 55(6): 498-512.
  35. Chen X, Zhu L, Xin L et al. Rice stripe1-2 and stripe1-3 mutants encoding the small subunit of ribonucleotide reductase are temperature sensitive and are required for chlorophyll biosynthesis. PLoS ONE 2015; 10(6): 1-19.
  36. Hahn M, Walbot V. Effects of cold-treatment on protein synthesis and mRNA levels in rice leaves. Plant Physiol 1989; 91(3): 930-938.
  37. Meza-Basso L, Alberdi M, Raynal M, Ferrero-Cadinanos ML, Delseny M. Changes in protein synthesis in rapeseed (Brassica napus) seedlings during a low temperature treatment. Plant Physiol 1986; 82(3): 733-738.
  38. Shakya S, Agrawal VP. RUBISCO screening for cold tolerance in rice. Plant Physiol 1993; 102(1): 80-80.
  39. Singh M, Johnson-Flanagan A. Co-ordination of photosynthetic gene expression during low-temperature acclimation and development in Brassica napus cv. Jet Neuf leaves. Plant Sci 1998; 135(2): 171-181.
  40. Raines CA. Transgenic approaches to manipulate the environmental responses of the C3 carbon ï¬xation cycle. Plant Cell Env 2006; 29: 331-339.
  41. Borawska-Jarmułowicz B, Mastalerczuk G, Kalaji MH, Carpentier R, Pietkiewicz S, Allakhverdiev SI. Photosynthetic efficiency and survival of Dactylis glomerata and Lolium perenne following low temperature stress. Russ J Plant Physiol 2014a; 61: 281-288.
  42. Borawska-Jarmułowicz B, Mastalerczuk G, Pietkiewicz S, Kalaji MH. Low temperature and hardening effects on photosynthetic apparatus efficiency and survival of forage grass varieties. Plant Soil Env 2014b; 60(4): 177-183.
  43. Dai F, Zhou M, Zhang G. The change of chlorophyll fluorescence parameters in winter barley during recovery after freezing shock and as affected by cold acclimation and irradiance. Plant Physiol Biochem 2007; 45(12): 915-921.
  44. Maxwell K, Johnson GN. Chlorophyll fluorescence- a practical guide. J Exp Bot 2000; 51(345): 659-668.
  45. Schreiber U, Berry JA. Heat-induced changes of chlorophyll fluorescence in intact leaves correlated with damage of the photosynthetic apparatus. Planta 1977; 136(3): 233-238.
  46. Mishra A, Heyer AG, Mishra KB. Chlorophyll fluorescence emission can screen cold tolerance of cold acclimated Arabidopsis thaliana accessions. Plant Methods 2014; 10: 38-48.
  47. Baker NR, Rosenqvist E. Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 2004; 55: 1607-1621.
  48. Brestic M, Zivcak M. PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In: Molecular Stress Physiology of Plants (edn): Gyana Ranjan Rout and Anath Bandhu Das. Springer India; 2013.
  49. Routaboul JM, Fischer SF, Browse J. Trienoic fatty acids are required to maintain chloroplast function at low temperatures. Plant Physiol 2000; 124(4): 1697-1705.
  50. Rapacz M, Gsior D, Ko cielniak J, Kosmala A, Zwierzykowski Z, Humphreys MW. The role of the photosynthetic apparatus in cold acclimation of Lolium multiflorum. Characteristics of novel genotypes low-sensitive to PSII over-reduction. Acta Physiologiae Plantarum 2007; 29(4): 309-316.
  51. Rizza F, Pagani D, Stanca AM, Cattivelli L. Use of chlorophyll fluorescence to evaluate the cold acclimation and freezing tolerance of winter and spring oats. Plant Breeding 2001; 120(5): 389-396.
  52. Rapacz M, Janowiak F. Winter hardiness frost resistance and vernalization requirement of european winter oilseed rape (Brassica napus var. Oleifera) cultivars within the last 19 years. J Agr Crop Sci 1999c; 183: 243-253.
  53. Rapacz M, Tokarz K, Janowiak F. The initiation of elongation growth during long-term low-temperature stay of spring-type oilseed rape may trigger loss of frost resistance and changes in photosynthetic apparatus. Plant Sci 2001; 161(2): 221-230.
  54. Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF. Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Nat Acad Sci (PNAS) 1996; 93: 13404-13409.
  55. Dal Bosco C, Busconi M, Govoni C et al. cor gene expression in barley mutants affected in chloroplast development and photosynthetic electron transport. Plant Physiol 2003; 131(2): 793-802.
  56. Lee B, Lee H, Xiong L, Zhu JK. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. The Plant Cell Online 2002; 14(6): 1235-1251.
  57. Kalaji HM, Guo G. Chlorophyll fluorescence: a useful tool in barley plant breeding programs. In: . In: Sanchez A, Gutierrez, S.J. (Eds.), ed. Photochemistry Research Progress. Nova Publishers, NY, USA,; 2008: pp. 439–463.
  58. Kautsky H, Hirsch A. Neue Versuche zur Kohlensäureassimilation. Naturwissenschaften 1931; 19(48): 964-964.
  59. Hansatech-Instruments L. Thain Wilbur 36/38 King Street King's Lynn Norfolk PE30 1ES England. Http://http://www.hansatech-instruments.com.
  60. Strasser RJ, Srivastava, A., Tsimilli-Michael, M. The fluorescence transient as a tool to characterise and screen photosynthetic samples. In: Yunus, M., Pathre, U., Mohanty, P. (Eds.). London, GB: Taylor & Francis; 2000.
  61. Strasser RJ, Srivastava A, Tsimilli-Michael M. Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou, G., Govinjee, Xu C.H. (Eds.), Advances in Photosynthesis and Respiration, Chlorophyll Fluorescence: a Signature of Photosynthesis, vol. 19: Kluwer Academic Publishers, The Netherlands; 2004.
  62. Rapacz M, Sasal M, Kalaji HM, Kościelniak J. Is the OJIP test a reliable indicator of winter hardiness and freezing tolerance of common wheat and triticale under variable winter environments? PLoS ONE 2015a; 10(7): 1-18. doi:10.1371/journal.pone.0134820.
  63. Athar H-UR, Zafar ZU, Ashraf M. Glycinebetaine improved photosynthesis in canola under salt stress: evaluation of chlorophyll fluorescence parameters as potential indicators. J Agr Crop Sci 2015: doi: 10.1111/jac.12120.
  64. Li H, Zheng Q, Zhang J, Li B, Li Z. The analysis of determining factors and evaluation of tolerance to photoinhibition in wheat (Triticum aestivum L.). Photosynthetica 2017; 55(1): 69-76.
  65. Zhao X, Chen T, Feng B et al. Non-photochemical quenching plays a key role in light acclimation of rice plants differing in leaf color. Frontiers Plant Sci 2017: doi: 10.3389/fpls.2016.01968.
  66. í–quist G, Wass R. A portable, microprocessor operated instrument for measuring chlorophyll fluorescence kinetics in stress physiology. Physiologia Plantarum 1988; 73(2): 211-217.
  67. Baker NR. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Ann Rev Plant Biol 2008; 59: 89-113.
  68. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72(1-2): 248-254.
  69. Boothe JG, de Beus MD, Johnson-Flanagan AM. Expression of a low-temperature-induced protein in Brassica napus. Plant Physiol 1995; 108(2): 795-803.
  70. Kosová K, Ví­támvás P, Práˇsil IT. The role of dehydrins in plant response to cold. Biologia Plantarum 2007; 51: 601-617.
  71. Jurczyka B, Pociechaa E, Grzesiak M, Kalita K, Rapacz M. Enhanced expression of Rubisco activase splicing variants differentially affects Rubisco activity during low temperature treatment in Lolium perenne. J Plant Physiol 2016; 198(1): 49-55.
  72. Parry MAJ, Andralojc PJ, Scales JC et al. Rubisco activity and regulation as targets for crop improvement. J Exp Bot 2013; 64(3): 717–730.
  73. Bacarin MA, Deuner S, Paulino da Silva FS, Cassol D, Moura Silva D. Chlorophyll a fluorescence as indicative of the salt stress on Brassica napus L. Braz J Plant Physiol 2011; 23(4): 245-253.
  74. de Sauza DF, de Paiva DS, das Chagas Noqueli Casari RA et al. A procedure for maize genotypes discrimination to drought by chlorophyll fluorescence imaging rapid light curves. Plant Methods 2017; 13:61.
  75. DeEll JR, Prange RK, Murr DP. Chlorophyll fluorescence techniques to detect atmospheric stress in stored apples. Acta Hort 1998; 464: 127-131.
  76. Mauromicale G, Ierna A, Marchese M. Chlorophyll fluorescence and chlorophyll content in field-grown potato as affected by nitrogen supply, genotype, and plant age. Photosynthetica 2006; 44(1): 76-82.
  77. Fghire R, Anaya F, Issa Ali O, Benlhabib O, Ragab R, Wahbi S. Physiological and photosynthetic response of quinoa to drought stress. Chilean J Agr Res 2015; 45(2): 174-183.
  78. Bjorkman O, Demmig B. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 1987; 170: 489-504.
  79. Kalajia MZ, Carpentier R, Allakhverdiev SI, Bosa K. Fluorescence parameters as early indicators of light stress in barley. J Photochem Photobiol B: Biol 2012; 112: 1-6.
  80. DeEll JR, van Kooten OV, Prange RK, Murr DP. Applications of chlorophyll fluorescence techniques in postharvest physiology. Hort Revi 1999; 23: 69-107.
  81. Butler WL. Energy distribution in the photochemical apparatus of photosynthesis. Ann Rev Plant Physiol 1978; 29(1): 345-378.
  82. Aroca R, Irigoyen JJ, Sanchez–Diaz M. Photosynthetic characteristics and protective mechanisms against oxidative stress during chilling and subsequent recovery in two maize varieties differing in chilling sensitivity. Plant Sci 2001; 161: 719-726.
  83. Rapacz M, Janowiak F. Physiological effects of winter rape (B. napus var. Oleifera). I. frost resistance and photosynthesis during cold acclimation. J Agr Crop Sci 1999a; 181(1): 13-20.
  84. Rapacz M, Sasal M, Wojcik-Jagla M. Direct and indirect measurements of freezing tolerance: advantages and limitations. Acta physiologia Plantarum 2015b: 37-57.
  85. Kramer DM, Johnson G, Kiirats O, Edwards GE. New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photos Res 2004; 79: 209-218.
  86. Hussain MI, Reigosa MJ. Characterization of xanthophyll pigments, photosynthetic performance, photon energy dissipation, reactive oxygen species generation and carbon isotope discrimination during artemisinin-induced stress in Arabidopsis thaliana. PloS ONE 2015; 10(1): e0114826.
  87. Rohacek K, Soukupova J, Bartak M. Chlorophyll fluorescence: a wonderful tool to study plant physiology and plant stress. In: In: Research Signpost T, ed. Schoefs B (ed) Plant cellcompartments – selected topics.; 2008.
  88. Liu M, Qi H, Zhang ZP et al. Response of photosynthesis and chlorophyll fluorescence to drought stress in two maize cultivars. Afric J Agr Res 2012: 4751–4760.
  89. Mathobo R, Marais D, Steyna JM. The effect of drought stress on yield, leaf gaseous exchange and chlorophyll fluorescence of dry beans (Phaseolus vulgaris L.). Agric Water Manag 2017; 180: 118–125.
  90. de Lucena CC, de Siqueira DL, Martinez HEPM, Cecon PR. Salt stress change chlorophyll fluorescence in mango. Rev Bras Frutic, Jaboticabal - SP 2012; 34(4): 1245-1255.
  91. Perks MP, Monaghan S, O'Reilly C, Osborne BA, Mitchell DT. Chlorophyll fluorescence characteristics, performance and survival of freshly lifted and cold stored Douglas fir seedlings. Ann Forest Sci 2001; 58: 225-235.
  92. Li R-h, Guo P-g, Baumb M, Grando S, Ceccarelli S. Evaluation of chlorophyll content and fluorescence parameters as indicators of drought tolerance in barley. Agric Sci China 2006; 5(10): 751-757.
  93. Havaux M, Lannoye R. Drought resistance of hard wheat cultivars measured by rapid chlorophyll fluorescence. JJ Agr Sci Camb 1985; 104: 501-504.
  94. Moustakas M, Ouzounidou G, Lannoye R. Rapid screening for aluminum tolerance in cereals by use of the chlorophyll fluorescence test. Plant Breeding 1993; 111(4): 343-346.
  95. Roháćek K. Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 2002; 40(1): 13-29.
  96. Papageorgiou GC, Govindjee. Chlorophyll fluorescence: a signature of photosynthesis. Advances in Photosynthesis and Respiration. In: Springer D, ed; 2004: pp 820.
  97. Guo-li, Zhen-fe G. Effects of chilling stress on photosynthetic rate and the parameters of chlorophyll fluorescence in two rice varieties differing in sensitivity. Chinese J Rice Sci 2005; 19(4): 381-383.
  98. Gururani JMA, Venkatesh J, Ganesan M et al. In vivo assessment of cold tolerance through chlorophyll-afluorescence in transgenic zoysiagrass expressing mutant phytochrome A. PLoS ONE 2015: 1-17. doi::10.1371/journal.pone.0127200.
  99. Dć…browski P, Baczewsk AH, PawluÅ›kiewicz B et al. Prompt chlorophyll a fluorescence as a rapid tool for diagnostic changes in PSII structure inhibited by salt stress in Perennial ryegrass. J Photochem Photobiol B: Biology 2016; 157: 22-31.
  100. Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochimica Biophysica Acta 2010; 1797: 1313–1326.
  101. Dumont E, Bahrman N, Goulas E et al. A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci 2010; 180: 86–98.
  102. Takahashi D, Li B, Nakayama T, Kawamura Y, Uemura M. Plant plasma membrane proteomics for improving cold tolerance. Frontiers Plant Sci 2013; 4: 1-5.
  103. Thomashow MF. So what's new in the field of plant cold acclimation? Lots! Plant Physiol 2001; 125(1): 89-93.
  104. Zakar O, Herman E, Vajrave S et al. Lipid and carotenoid cooperation-driven adaptation to light and temperature stress in Synechocystis sp. PCC6803. Biochimica et Biophysica Acta 2017; 166: 1436-1445.
  105. Uemura M, Steponkus PL. Cold acclimation in plants: relationship between the lipid composition and the cryostability of the plasma membrane. J Plant Res 1999; 112: 245–254.
  106. Mahajan S, Tuteja N. Cold, salinity and drought stresses: An overview. Biochemica et Biophysica Acta 2005; 444: 139-158.
  107. Raison JK, Orr GR. Phase transition in liposomes formed from polar lipids of mitochondria from chilling sensitive plants. Plant Physiol 1986; 81: 807–811.
  108. Williams JP, Kahn MU, Mitchell K, Johnson G. The effect of temperature on the level and biosynthesis of unsaturated fatty acids in diaglycerols of Brassica napus leaves. Plant Physiol 1988; 87: 904-910.
  109. Jeyaramraja PR, Jayakumar D, Pius PK, Raj K. Relation of altered protein expression with chlorophyll fluorescence in tea under water stress. Ind J Plant Physiol 2003; 8(3): 214-218.
  110. Browse J, McCourt P, Somerville C. A mutant of Arabidopsis lacking a chloroplast-specific lipid. Scisnce 1985; 227: 763–765.
  111. Graham D, Patterson BD. Responses of plants to low, non-freezing temperatures: Proteins, metabolism, and acclimation. Ann Rev Plant Physiol 1982; 33: 347–372.
  112. Scotti-Campos P, Pais IP, Partelli FL, Batista-Santos P, Ramalho JC. Phospholipids proï¬le in chloroplasts of Coffea spp. genotypes differing in cold acclimation ability. J Plant Physiol 2014; 171: 243-249.
  113. Lepori G, Belletti P, Lanteri S, Nassi MO, Quagliotti L. Breeding of runner bean for seed germination at low temperature. Acta Hort 1989; 253: 171-178.
  114. Oyanedel E, Wolfe DW, Monforte AJ, Tanksley SD, Owens TG. Using Lycopersicon hirsutum as a source of cold tolerance in processing tomato breeding. Acta Hort 2001: 387-391.
  115. Preil W, Engelhardt M, Walther F. Breeding of low temperature tolerant poinsettia (Euphorbia pulcherrima) and chrysanthemum by means of mutation induction in in vitro culture. Acta Hort 1982: 345-355.
  116. Gusta LV, O'Connor BJ, Gao YP, Jana S. A re-evaluation of controlled freeze-tests and controlled environment hardening conditions to estimate the winter survival potential of hardy winter wheats. Canadian J Plant Sci 2001; 81(2): 241-246.
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Author Biography

Ali Arminian, Department of Agronomy and Plant Breeding, Faculty of Agriculture, Ilam University, Ilam, Iran
Agronomy and Plant Breeding Dept. Ilam University, Iran.
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