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Plant function and evolutionary biology
RESEARCH ARTICLE

Is leaf age a predictor for cold tolerance in winter oilseed rape plants?

Ali Doğru https://orcid.org/0000-0003-0060-4691 A C and Hüsnü Çakırlar B
+ Author Affiliations
- Author Affiliations

A Sakarya University, Faculty of Arts and Sciences, Department of Biology, Esentepe, 54187, Sakarya, Turkey.

B Hacettepe University, Faculty of Science, Department of Biology, 06800, Beytepe, Ankara, Turkey.

C Corresponding author. Email: adogru@sakarya.edu.tr

Functional Plant Biology 47(3) 250-262 https://doi.org/10.1071/FP19200
Submitted: 13 July 2019  Accepted: 2 November 2019   Published: 6 February 2020

Abstract

In the present study, low temperature-dependent physiological changes were investigated through photosynthetic activity and some endogenous mechanisms in two winter oilseed rape cultivars (Brassica napus L. ssp. oleifera cvv. Eurol and Hansen) on the basis of leaf age. Chlorophyll fluorescence measurements demonstrated that low temperature caused decreased photosynthetic activity in both cultivars. However, photosynthetic apparatus in the young leaves of Hansen is more tolerant to low temperature as demonstrated by lower F0 (minimum fluorescence yield) and 1–qp (excitation pressure of photosystem II), higher Fm (maximum fluorescence yield), Fv/Fm and non-photochemical quenching (NPQ) compared with Eurol. In addition, young leaves of Hansen represented marked increase in some antioxidant enzyme activities (superoxide dismutase (SOD), ascorbate peroxidase (APX) and glutathione reductase (GR)) during cold exposure. In the young leaves of Eurol, however, APX and GR activity was decreased by low temperature, indicating lower efficiency of ascorbate-glutathione cycle. Lower antioxidant activity in the young leaves of Eurol may be responsible for increased malondialdehyde (MDA), H2O2 and membrane damage and decreased chlorophyll content as a result of oxidative damage during cold exposure. In the cold-stressed mature leaves, both cultivars represented similar antioxidant capacities and photosynthetic efficiency. As a consequence, coordinated increase in SOD, APX and GR activities, increased capacity to keep quinone A (QA) in an oxidised state (as indicated by lower 1–qp) and accumulation of soluble sugar and proline could be mainly attributed to higher level of tolerance of the young leaves of Hansen to low temperature when compared with Eurol.

Additional keywords: antioxidative response, Brassica spp., chlorophyll fluorescence, cold tolerance, photosynthesis.


References

Alia P, Saradhi PP, Mohanty P (1997) Involvement of proline in protecting thylakoid membranes against free radical-induced photodamage. Journal of Photochemistry and Photobiology 38, 253–257.
Involvement of proline in protecting thylakoid membranes against free radical-induced photodamage.Crossref | GoogleScholarGoogle Scholar |

Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends in Plant Science 6, 36–42.
Impacts of chilling temperatures on photosynthesis in warm-climate plants.Crossref | GoogleScholarGoogle Scholar | 11164376PubMed |

Alscher RG, Donahue JL, Cramer C (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiologia Plantarum 100, 224–233.
Reactive oxygen species and antioxidants: relationships in green cells.Crossref | GoogleScholarGoogle Scholar |

Aroca R, Irigoyen JJ, Sanchez-Diaz M (2001) Photosynthetic characteristics and protective mechanisms against oxidative stress during chilling and subsequent recovery in two maize varieties differing in chilling sensitivity. Plant Science 161, 719–726.
Photosynthetic characteristics and protective mechanisms against oxidative stress during chilling and subsequent recovery in two maize varieties differing in chilling sensitivity.Crossref | GoogleScholarGoogle Scholar |

Asada K (1996) Radical production and scavenging in the chloroplasts. In ‘Photosynthesis and environment’. (Ed NR Baker) pp. 123–150. (Kluwer: Dordrecht, The Netherlands)

Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons.Crossref | GoogleScholarGoogle Scholar | 15012221PubMed |

Ballottari M, Girardon J, Dall’Osto L, Bassi R (2012) Evolution and functional properties of photosystem II light harvesting complex in eukaryotes. Biochimica et Biophysica Acta. Bioenergetics 1817, 143–157.
Evolution and functional properties of photosystem II light harvesting complex in eukaryotes.Crossref | GoogleScholarGoogle Scholar |

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar |

Benavides MP, Marconi PL, Gallego SM, Comba ME, Tomaro ML (2000) Relationship between antioxidant defence systems and salt tolerance in Solanum tuberosum. Australian Journal of Plant Physiology 27, 273–278.
Relationship between antioxidant defence systems and salt tolerance in Solanum tuberosum.Crossref | GoogleScholarGoogle Scholar |

Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry 161, 559–566.
Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions.Crossref | GoogleScholarGoogle Scholar | 3034103PubMed |

Boothe JG, de Beus MD, Johnson-Flanagan AM (1995) Expression of a low temperature-induced protein in Brassica napus. Plant Physiology 108, 795–803.
Expression of a low temperature-induced protein in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 12228511PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |

Demmig-Adams B, Stewart JJ, Baker CR, Adams WW (2018) Optimization of photosynthetic productivity in contrasting environment by regulons controlling plant form and function. International Journal of Molecular Sciences 19, 872–893.
Optimization of photosynthetic productivity in contrasting environment by regulons controlling plant form and function.Crossref | GoogleScholarGoogle Scholar |

Ding F, Wang M, Zhang S (2017) Overexpression of a Calvin cycle enzymes SBPase improves tolerance to chilling-induced oxidative stress in tomato plants. Scientia Horticulturae 214, 27–33.
Overexpression of a Calvin cycle enzymes SBPase improves tolerance to chilling-induced oxidative stress in tomato plants.Crossref | GoogleScholarGoogle Scholar |

DuBois M, Gilles KA, Hamilton KJ, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
Colorimetric method for determination of sugars and related substances.Crossref | GoogleScholarGoogle Scholar |

Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant, Cell & Environment 17, 507–523.
Protection against oxygen radicals: an important defence mechanism studied in transgenic plants.Crossref | GoogleScholarGoogle Scholar |

Fracheboud Y, Haldimann P, Leipner J, Stamp P (1999) Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). Journal of Experimental Botany 50, 1533–1540.
Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |

Georgieva K, Lichtenthaler HL (1999) Photosynthetic activity and acclimation ability of pea plants to low and high temperature treatment as studied by means of chlorophyll fluorescence. Journal of Plant Physiology 155, 416–423.
Photosynthetic activity and acclimation ability of pea plants to low and high temperature treatment as studied by means of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |

Gharechahi J, Sharifi G, Komatsu S, Salekdeh GH (2016) Proteomic analysis of crop plants under low temperature: a review of cold responsive proteins. Agricultural Proteomics 2, 97–127.
Proteomic analysis of crop plants under low temperature: a review of cold responsive proteins.Crossref | GoogleScholarGoogle Scholar |

Graßes T, Pesaresi P, Schiavon F, Varotto C, Salamini F, Jahns P, Leister D (2002) The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against light-induced in Arabidopsis thaliana. Plant Physiology and Biochemistry 40, 41–49.
The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against light-induced in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Gray GR, Cauvin L-P, Sarhan F, Huner NPA (1997) Cold acclimation and freezing tolerance. A complex interaction of light and temperature. Plant Physiology 114, 467–474.
Cold acclimation and freezing tolerance. A complex interaction of light and temperature.Crossref | GoogleScholarGoogle Scholar | 12223720PubMed |

Guo YY, Tian SS, Liu SS, Wang WQ, Sui N (2018) Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress. Photosynthetica 56, 861–872.
Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress.Crossref | GoogleScholarGoogle Scholar |

Habibi G, Vaziri A (2017) High salicylic acid concentration alters the electron flow associated with photosystem II in barley. Acta Agriculturae Slovenica 109, 393–402.
High salicylic acid concentration alters the electron flow associated with photosystem II in barley.Crossref | GoogleScholarGoogle Scholar |

Hashimoto H, Uragami C, Cogdell RJ (2016) Carotenoids and Photosynthesis. In ‘Carotenoids in nature. Subcellular biochemistry. Vol. 79’. (Ed. C Stange) pp. 111–139. (Springer: Cham, Germany)

Havaux M, Kloppstech K (2001) The protective function of carotenoids and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213, 953–966.
The protective function of carotenoids and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants.Crossref | GoogleScholarGoogle Scholar |

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I. Kinetic and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
Photoperoxidation in isolated chloroplasts I. Kinetic and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |

Hodgins RRW, van Huystee RB (1986) Porphyrin metabolism in chill-stressed maize (Zea mays L.). Plant Physiology 125, 325–336.
Porphyrin metabolism in chill-stressed maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |

Hu Z, Fan J, Xie Y, Amombo E, Liu A, Gitau MM, Khaldun ABM, Chen L, Fu J (2016) Comparative photosynthetic and metabolic analysis reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatonin. Plant Physiology and Biochemistry 100, 94–104.
Comparative photosynthetic and metabolic analysis reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatonin.Crossref | GoogleScholarGoogle Scholar | 26807934PubMed |

Huang X, Chen MH, Yang LT, Li YR, Wu JM (2015) Effects of exogenous abscisic acid on cell membrane and endogenous hormone contents in leaves of sugarcane seedlings under cold stress. Sugar Tech 17, 59–64.
Effects of exogenous abscisic acid on cell membrane and endogenous hormone contents in leaves of sugarcane seedlings under cold stress.Crossref | GoogleScholarGoogle Scholar |

Huner NPA, Öqüist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold-tolerant plants. Photosynthesis Research 37, 19–39.
Photosynthesis, photoinhibition and low temperature acclimation in cold-tolerant plants.Crossref | GoogleScholarGoogle Scholar |

Huner NPA, Öquist G, Sahran F (1998) Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224–230.
Energy balance and acclimation to light and cold.Crossref | GoogleScholarGoogle Scholar |

Hurry VM, Huner NPA (1991) Low growth temperature effects a differential inhibition of photosynthesis in spring and winter wheat. Plant Physiology 96, 491–497.
Low growth temperature effects a differential inhibition of photosynthesis in spring and winter wheat.Crossref | GoogleScholarGoogle Scholar | 16668213PubMed |

Hurry VM, Strand A, Tobiaeson M, Gardeström P, Öquist G (1995) Cold hardening of spring and winter wheat and oilseed rape results in differential effects of on growth, carbon metabolism, and carbohydrate content. Plant Physiology 109, 697–706.
Cold hardening of spring and winter wheat and oilseed rape results in differential effects of on growth, carbon metabolism, and carbohydrate content.Crossref | GoogleScholarGoogle Scholar | 12228623PubMed |

Igarashi Y, Yoshiba Y, Takeshita T, Nomura S, Otomo J, Yamaguchi-Shinozaki K, Shinozaki K (2000) Molecular cloning and characterization of a cDNA encoding proline transporter in rice. Plant & Cell Physiology 41, 750–756.
Molecular cloning and characterization of a cDNA encoding proline transporter in rice.Crossref | GoogleScholarGoogle Scholar |

Imanishi HT, Suzuki T, Masuda K, Harada T (1998) Accumulation of raffinose and stachyose in shoot apices of Lonicera caerulea L. during cold acclimation. Scientia Horticulturae 72, 255–263.
Accumulation of raffinose and stachyose in shoot apices of Lonicera caerulea L. during cold acclimation.Crossref | GoogleScholarGoogle Scholar |

Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta. Bioenergetics 1817, 182–193.
The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II.Crossref | GoogleScholarGoogle Scholar |

Janda T, Szalai G, Rios-Gonzales K, Veisz O, Paldi E (2003) Comparative study of frost tolerance and antioxidant activity in cereals. Plant Science 164, 301–306.
Comparative study of frost tolerance and antioxidant activity in cereals.Crossref | GoogleScholarGoogle Scholar |

Kacperska A, Szaniawski RK (1993) Frost resistance and water status of winter rape leaves as affected by differential shoot/root temperature. Physiologia Plantarum 89, 775–782.
Frost resistance and water status of winter rape leaves as affected by differential shoot/root temperature.Crossref | GoogleScholarGoogle Scholar |

Kalaji HM, Bosa K, Koscielnak J, Zuk-Golaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany 73, 64–72.
Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces.Crossref | GoogleScholarGoogle Scholar |

Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654–657.
Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 10213690PubMed |

Klimov SV, Popov VN, Dubinina IM, Burakhanova EA, Trunova TI (2002) The decreased cold-resistance of chilling-sensitive plants is related to suppressed CO2 assimilation in leaves and sugar accumulation in roots. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 49, 776–781.
The decreased cold-resistance of chilling-sensitive plants is related to suppressed CO2 assimilation in leaves and sugar accumulation in roots.Crossref | GoogleScholarGoogle Scholar |

Kornyeyev D, Logan BA, Payton P, Allen RD, Holaday AS (2001) Enhanced photochemical light utilization and decreased chilling-induced photoinhibition of photosystem II in cotton overexpression genes encoding chloroplast-targeted antioxidant enzymes. Physiologia Plantarum 113, 323–331.
Enhanced photochemical light utilization and decreased chilling-induced photoinhibition of photosystem II in cotton overexpression genes encoding chloroplast-targeted antioxidant enzymes.Crossref | GoogleScholarGoogle Scholar | 12060276PubMed |

Li XG, Meng QW, Jiang GQ, Zou Q (2003) The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water–water cycle. Photosynthetica 41, 259–265.
The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water–water cycle.Crossref | GoogleScholarGoogle Scholar |

Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic membranes. Methods in Enzymology 148, 350–382.
Chlorophylls and carotenoids: pigments of photosynthetic membranes.Crossref | GoogleScholarGoogle Scholar |

Liu P, Meng WM, Zou Q, Xhao SJ, Liu Z (2001) Effects of cold-hardening on chilling-induced photoinhibition of photosynthesis and on xanthophyll cycle pigments in sweet pepper. Photosynthetica 39, 467–472.
Effects of cold-hardening on chilling-induced photoinhibition of photosynthesis and on xanthophyll cycle pigments in sweet pepper.Crossref | GoogleScholarGoogle Scholar |

Maciejewska U, Bauer H (1992) Effects of cold acclimation on chlorophyll fluorescence in winter rape plants. Photosynthetica 27, 559–562.

Mamode-Cassim A, Gouguet P, Gronnier J, Laurent N, Germain V, Grison M, Boutte Y, Gerbeau-Pissot P, Simon-Plas P, Mongrand S (2019) Plant lipids: key players of plasma membrane organization and function. Progress in Lipid Research 73, 1–27.
Plant lipids: key players of plasma membrane organization and function.Crossref | GoogleScholarGoogle Scholar | 30465788PubMed |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar | 10938857PubMed |

Meravi N, Prajapati SK (2018) Temporal variation in chlorophyll fluorescence of different tree species. Biological Rhythm Research 49, 1–7.

Mironov KS, Sidorov RA, Trofimova MS, Bedbenov VS, Tsydendambaev VD, Allakhverdiev SI, Los DA (2012) Light-dependent cold-induced fatty acid unsaturation, changes in membrane fluidity, and alterations in gene expression in Synechocystis. Biochimica et Biophysica Acta. Bioenergetics 1817, 1352–1359.
Light-dependent cold-induced fatty acid unsaturation, changes in membrane fluidity, and alterations in gene expression in Synechocystis.Crossref | GoogleScholarGoogle Scholar |

Moustaka J, Ouzounidou G, Bayçu G, Moustakas M (2016) Aluminum resistance in wheat involves maintenance of of leaf Ca2+ and Mg 2+ content, decreased lipid peroxidation and Al accumulation, and low photosystem II excitation pressure. Biometals 29, 611–623.
Aluminum resistance in wheat involves maintenance of of leaf Ca2+ and Mg 2+ content, decreased lipid peroxidation and Al accumulation, and low photosystem II excitation pressure.Crossref | GoogleScholarGoogle Scholar | 27188757PubMed |

Mutlu S, Atıcı Ö, Nalbantoğlu B, Mete E (2016) Exogenous salicylic acid alleviates cold damage by regulating antioxidative system in two barley (Hordeum vulgare L.) cultivars. Frontiers in Life Science 9, 99–109.
Exogenous salicylic acid alleviates cold damage by regulating antioxidative system in two barley (Hordeum vulgare L.) cultivars.Crossref | GoogleScholarGoogle Scholar |

Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. The Plant Cell 10, 1121–1134.
Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion.Crossref | GoogleScholarGoogle Scholar | 9668132PubMed |

Nowicka B, Ciura J, Szymanska R, Kruk J (2018) Improving photosynthesis, plant productivity and abiotic stress tolerance-current trends and future perspectives. Journal of Plant Physiology 231, 415–433.
Improving photosynthesis, plant productivity and abiotic stress tolerance-current trends and future perspectives.Crossref | GoogleScholarGoogle Scholar | 30412849PubMed |

Ohkawa H, Ohishi N, Yagi NY (1979) Assay of lipid peroxides in animal tissue by thiobarbituric acid reaction. Analytical Biochemistry 95, 351–358.
Assay of lipid peroxides in animal tissue by thiobarbituric acid reaction.Crossref | GoogleScholarGoogle Scholar |

Oraee A, Tehranifar A, Nezami A, Shoor M (2018) Effects of drought stress on cold hardiness of non-acclimated viola in controlled conditions. Scientia Horticulturae 238, 98–106.
Effects of drought stress on cold hardiness of non-acclimated viola in controlled conditions.Crossref | GoogleScholarGoogle Scholar |

Ort DR (2002) Chilling-induced limitations on photosynthesis in warm-climate plants: contrasting mechanisms. Environment Control in Biology 40, 7–18.
Chilling-induced limitations on photosynthesis in warm-climate plants: contrasting mechanisms.Crossref | GoogleScholarGoogle Scholar |

Park YI, Chow WS, Anderson JM (1997) Antenna size dependency of photo inactivation of photosystem II in light-acclimated pea leaves. Plant Physiology 115, 151–157.
Antenna size dependency of photo inactivation of photosystem II in light-acclimated pea leaves.Crossref | GoogleScholarGoogle Scholar |

Peppino Margutti M, Reyna M, Meringer MV, Racagni GE, Villasuso AL (2017) Lipid signalling mediated by PLD/PA modulates proline and H2O2 levels in barley seedlings exposed to short- and long-term chilling stress. Plant Physiology and Biochemistry 113, 149–160.
Lipid signalling mediated by PLD/PA modulates proline and H2O2 levels in barley seedlings exposed to short- and long-term chilling stress.Crossref | GoogleScholarGoogle Scholar | 28214728PubMed |

Pitcher LH, Brennan E, Hurley A, Dunsmuir P, Tepperman JM, Zilinskas BA (1991) Overproduction of petunia chloroplastic copper/zinc superoxide dismutase does not confer ozone tolerance in transgenic tobacco. Plant Physiology 97, 452–455.
Overproduction of petunia chloroplastic copper/zinc superoxide dismutase does not confer ozone tolerance in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 16668407PubMed |

Płażek A, Rapacz M, Hura K (2004) Relationship between quantum efficiency of PSII and cold-induced plant resistance to fungal pathogens. Acta Physiologiae Plantarum 26, 141–148.
Relationship between quantum efficiency of PSII and cold-induced plant resistance to fungal pathogens.Crossref | GoogleScholarGoogle Scholar |

Rapacz M (2002) Regulation of frost resistance during cold de-acclimation and re-acclimation in oilseed rape. A possible role of PSII redox state. Physiologia Plantarum 115, 236–243.
Regulation of frost resistance during cold de-acclimation and re-acclimation in oilseed rape. A possible role of PSII redox state.Crossref | GoogleScholarGoogle Scholar | 12060241PubMed |

Rapacz M, Hura K (2002) The pattern of changes in photosynthetic apparatus in response to cold acclimation and de-acclimation in two contrasting cultivars of oilseed rape. Photosynthetica 40, 63–69.
The pattern of changes in photosynthetic apparatus in response to cold acclimation and de-acclimation in two contrasting cultivars of oilseed rape.Crossref | GoogleScholarGoogle Scholar |

Rapacz M, Janowiak F (1999) Relationship between prehardening, photosynthesis activity at cold acclimation temperatures and frost tolerance in winter rape (Brassica napus var. oleifera). The consequences for the reliability of frost resistance estimation under controlled conditions. Journal Agronomy & Crop Science 182, 57–63.
Relationship between prehardening, photosynthesis activity at cold acclimation temperatures and frost tolerance in winter rape (Brassica napus var. oleifera). The consequences for the reliability of frost resistance estimation under controlled conditions.Crossref | GoogleScholarGoogle Scholar |

Rapacz R, Tokarz K, Janowiak F (2001) 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 Science 161, 221–230.
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.Crossref | GoogleScholarGoogle Scholar |

Rivero RM, Ruiz JM, Garcia PC, Lopez-Lefebre LR, Sanchez E, Romera L (2002) Response of oxidative metabolism in watermelon plants subjected to cold stress. Functional Plant Biology 29, 643–648.
Response of oxidative metabolism in watermelon plants subjected to cold stress.Crossref | GoogleScholarGoogle Scholar |

Rorat T, Havaux M, Irzykowski W, Cuine S, Becuwe N, Rey P (2001) PSIIS gene expression, photosynthetic activity and abundance of plastid thioredoxin-related and lipid-associated proteins during chilling stress in Solanum species differing in freezing resistance. Physiologia Plantarum 113, 72–78.
PSIIS gene expression, photosynthetic activity and abundance of plastid thioredoxin-related and lipid-associated proteins during chilling stress in Solanum species differing in freezing resistance.Crossref | GoogleScholarGoogle Scholar |

Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: Mechanism and effectiveness in protecting plant from photodamage. Plant Physiology 170, 1903–1916.
Nonphotochemical chlorophyll fluorescence quenching: Mechanism and effectiveness in protecting plant from photodamage.Crossref | GoogleScholarGoogle Scholar | 26864015PubMed |

Sairam RK, Deshmukh PS, Shukla DS (1997) Tolerance to drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. Journal Agronomy & Crop Science 178, 171–178.
Tolerance to drought and temperature stress in relation to increased antioxidant enzyme activity in wheat.Crossref | GoogleScholarGoogle Scholar |

Samach A, Wigge PA (2005) Ambient temperature perception in plants. Current Opinion in Plant Biology 8, 483–486.
Ambient temperature perception in plants.Crossref | GoogleScholarGoogle Scholar | 16054430PubMed |

Savitch LV, Leonardos ED, Krol M, Jansson S, Grodzinski B, Huner NPA, Öquist G (2002) Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation. Plant, Cell & Environment 25, 761–771.
Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation.Crossref | GoogleScholarGoogle Scholar |

Sayed OH (2003) Chlorophyll fluorescence as a tool in cereal crop research. Photosynthetica 41, 321–330.
Chlorophyll fluorescence as a tool in cereal crop research.Crossref | GoogleScholarGoogle Scholar |

Schreiber U, Schliw U, Bilger W (1986) Continuous recording of photochemical and non- photochemical fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10, 51–62.
Continuous recording of photochemical and non- photochemical fluorescence quenching with a new type of modulation fluorometer.Crossref | GoogleScholarGoogle Scholar | 24435276PubMed |

Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In ‘Ecological studies. Vol. 110. Ecophysiology of photosynthesis’. (Eds ED Schulze, MM Caldwell) pp. 49–70. (Springer-Verlag: Berlin)

Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. The Plant Cell 11, 377–391.

Sgherri CLM, Loggini B, Puliga S, Navari-Izzo F (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochemistry 35, 561–565.
Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration.Crossref | GoogleScholarGoogle Scholar |

Smallwood M, Bowles DJ (2002) Plants in a cold climate. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 357, 831–847.
Plants in a cold climate.Crossref | GoogleScholarGoogle Scholar | 12171647PubMed |

Strand A, Foyer CH, Gustafsson P, Hurry V (2003) Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant, Cell & Environment 26, 523–535.
Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance.Crossref | GoogleScholarGoogle Scholar |

Streb P, Shang W, Feierabend J (1999) Resistance to cold-hardened winter rye leaves (Secale cereale L.) to photo-oxidative stress. Plant, Cell & Environment 22, 1211–1223.
Resistance to cold-hardened winter rye leaves (Secale cereale L.) to photo-oxidative stress.Crossref | GoogleScholarGoogle Scholar |

Sun Y, Geng Q, Du Y, Yang X, Zhai H (2017) Induction of cyclic electron flow around photosystem I during heat stress in grape leaves. Plant Science 256, 65–71.
Induction of cyclic electron flow around photosystem I during heat stress in grape leaves.Crossref | GoogleScholarGoogle Scholar | 28167040PubMed |

Takagi T, Nakamura M, Hayashi H, Inatsugi R, Yano R, Nishida I (2003) The leaf-order-dependent enhancement of freezing tolerance in cold acclimated Arabidopsis rosettes is not correlated with the transcript levels of the cold-inducible transcription factors of CBF/DREB1. Plant & Cell Physiology 44, 922–931.
The leaf-order-dependent enhancement of freezing tolerance in cold acclimated Arabidopsis rosettes is not correlated with the transcript levels of the cold-inducible transcription factors of CBF/DREB1.Crossref | GoogleScholarGoogle Scholar |

Tao DL, Öqüist G, Wingsle G (1998) Active oxygen scavengers during cold acclimation of Scots pine seedlings in relation to freezing tolerance. Cryobiology 37, 38–45.
Active oxygen scavengers during cold acclimation of Scots pine seedlings in relation to freezing tolerance.Crossref | GoogleScholarGoogle Scholar | 9698428PubMed |

Tarkowski LP, Van der Ende W (2015) Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. Frontiers in Plant Science 6, 1–7.
Cold tolerance triggered by soluble sugars: a multifaceted countermeasure.Crossref | GoogleScholarGoogle Scholar |

Thomas H, Ougham H, Hörtensteiner S (2001) Recent advances in the cell biology of chlorophyll catabolism. Advances in Botanical Research 35, 1–52.
Recent advances in the cell biology of chlorophyll catabolism.Crossref | GoogleScholarGoogle Scholar |

Travert S, Valerio V, Fouraste I, Boudet AM, Teulieres C (1997) Enrichment in specific soluble sugars of two eucalyptus cell-suspension cultures by various treatments enhances their frost tolerance via a non-colligative mechanism. Plant Physiology 114, 1433–1442.
Enrichment in specific soluble sugars of two eucalyptus cell-suspension cultures by various treatments enhances their frost tolerance via a non-colligative mechanism.Crossref | GoogleScholarGoogle Scholar | 12223781PubMed |

Turan Ö, Ekmekçi Y (2011) Activities of photosystem II and antioxidant enzymes in chickpea (Cicer arietinum L.) cultivars exposed to chilling temperatures. Acta Physiologiae Plantarum 33, 67–78.
Activities of photosystem II and antioxidant enzymes in chickpea (Cicer arietinum L.) cultivars exposed to chilling temperatures.Crossref | GoogleScholarGoogle Scholar |

Valluru R, Lammens W, Claupein W, Van den Ende W (2008) Freezing tolerance by vesicle-mediated fructan transport. Trends in Plant Science 13, 409–414.
Freezing tolerance by vesicle-mediated fructan transport.Crossref | GoogleScholarGoogle Scholar | 18619894PubMed |

Verhoeven A, Garcia-Plazaola JI, Marin BF (2018) Shared mechanism of photoprotection in photosynthetic organisms tolerant to desiccation or to low temperature. Environmental and Experimental Botany 154, 66–79.
Shared mechanism of photoprotection in photosynthetic organisms tolerant to desiccation or to low temperature.Crossref | GoogleScholarGoogle Scholar |

Wang SY, Jiao H, Faust M (1991) Changes in ascorbate, glutathione and related enzyme activity during thidiazuron-induced bud break of apple. Plant Physiology 82, 231–236.
Changes in ascorbate, glutathione and related enzyme activity during thidiazuron-induced bud break of apple.Crossref | GoogleScholarGoogle Scholar |

Wang L, Yao L, Hao X, Li N, Wang Y, Ding C, Lei L, Qian W, Zeng J, Yang Y, Wang W (2019) Transcriptional and physiological analysis reveal the association of ROS metabolism with cold tolerance in tea plants. Environmental and Experimental Botany 160, 45–58.
Transcriptional and physiological analysis reveal the association of ROS metabolism with cold tolerance in tea plants.Crossref | GoogleScholarGoogle Scholar |

Wani MA, Qazi HA, Yaqoob U, Lone SA, John R (2017) Response of radish genotypes to short term cold stress in relation to biochemical changes and antioxidant activity. International Journal of Current Agricultural Sciences 7, 222–228.

Wanner LA, Juntilla O (1999) Cold induced freezing tolerance in Arabidopsis. Plant Physiology 120, 391–400.
Cold induced freezing tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 10364390PubMed |

Widomska J, Welc R, Gruszecki WI (2019) The effect of carotenoids on the concentration of singlet oxygen in lipid membranes. Biochimica et Biophysica Acta. Biomembranes 1861, 845–851.
The effect of carotenoids on the concentration of singlet oxygen in lipid membranes.Crossref | GoogleScholarGoogle Scholar | 30689980PubMed |

Xiaochuang C, Chu Z, Lianfeng Z, Junhua Z, Hussain S, Lianghuan W, Qianyu J (2017) Glycine increases cold tolerance in rice via the regulation of N uptake, physiological characteristics, and photosynthesis. Plant Physiology and Biochemistry 112, 251–260.
Glycine increases cold tolerance in rice via the regulation of N uptake, physiological characteristics, and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 28107733PubMed |

Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperature. Plant, Cell & Environment 23, 893–902.
Cold comfort farm: the acclimation of plants to freezing temperature.Crossref | GoogleScholarGoogle Scholar |

Xu CC, Jeon YA, Lee CH (1999) Relative contribution of photochemical and non-photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature. Physiologia Plantarum 107, 447–453.
Relative contribution of photochemical and non-photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature.Crossref | GoogleScholarGoogle Scholar |

Yoon YE, Kuppusamy S, Cho KM, Kim PJ, Kwack YB, Lee YB (2017) Influence of cold stress on contents of soluble sugars, vitamin C and free amino acids including gamma-aminobutyric acid (GABA) in spinach (Spinacia oleracea). Food Chemistry 215, 185–192.
Influence of cold stress on contents of soluble sugars, vitamin C and free amino acids including gamma-aminobutyric acid (GABA) in spinach (Spinacia oleracea).Crossref | GoogleScholarGoogle Scholar | 27542466PubMed |

Zhang Y, Yu H, Yang X, Li Q, Ling J, Wang H, Gu X, Huang S, Jiang W (2016) CsWRKY46, a WRKY transcription factor from cucumber, confers cold resistance in transgenic-plant by regulating a set of cold-stress responsive genes in an ABA-dependent manner. Plant Physiology and Biochemistry 108, 478–487.
CsWRKY46, a WRKY transcription factor from cucumber, confers cold resistance in transgenic-plant by regulating a set of cold-stress responsive genes in an ABA-dependent manner.Crossref | GoogleScholarGoogle Scholar | 27592172PubMed |