Investigate the physiological, biochemical, and productivity aspects of crops to cold stress
الموضوعات :
Roghiyeh Farzi Aminabad
1
,
Safar Nasrollahzadeh
2
1 - Department of Plant Ecophysiology, Faculty of Agriculture, University of Tabriz, Tabriz, Iran
2 - Department of Plant Ecophysiology, Faculty of Agriculture, University of Tabriz, Tabriz, Iran
الکلمات المفتاحية: Cold, Chilling, Freezing, ICE1, COR Genes,
ملخص المقالة :
Cold stress is one of the environmental stresses that affects the growth, development, and productivity of crops in various climates. Understanding the physiological and biochemical mechanisms by which plants respond to this stress can improve their growth and development. Cold stress can be categorized into two types: freezing stress and chilling stress. Freezing stress occurs when the temperature drops below 0 °C, while chilling stress occurs when the temperature ranges between 0 and 15 °C. Cold stress leads to the destruction or alteration of membrane proteins, causing a loss of membrane fluidity. This stress also increases the production of oxygen free radicals (ROS), which attack and destroy cell membranes. If cold stress persists, it can ultimately result in plant death. The ICE1-CBF-COR transcription cascade serves as a major signaling pathway activated in response to cold stress in plants. This cascade involves the induction of CBF genes, which encode transcription factors that bind to the promoter of COR genes, initiating their transcription. Enzymes such as SOD, APX, CAT, and GR exhibit increased activity in response to low temperatures. Additionally, the accumulation of MDA can serve as an indicator of oxidative stress sensitivity and cold tolerance. Cold stress has detrimental effects on crop yield formation. It initially impairs the reproductive phase of plants, ultimately leading to reduced final yields.
Achard, P., F. Gong, S. Cheminant, M. Alioua, P. Hedden and P. Genschik. 2008. The cold inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. The Plant Cell, 20: 2117-2129.
Ahmad, I., S. M. A. Basra and A. Wahid. 2014. Exogenous application of ascorbic acid, salicylic acid and hydrogen peroxide improves the productivity of hybrid maize under at low temperature stress. International Journal of Agricultural Biology, 16: 825-830.
Albertos, B., K. Wanger and B. Poppenberger. 2019. Cold stress signaling in female reproductive tissues. Plant Cell Environ, 42: 846-853.
An, D., J. Yang and P. Zhang. 2012. Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC genomics, 13: 1-25.
Arshad, M. S., Farooq, M., Asch, F., Krishna, J. S., Prasad, P. V., & Siddique, K. H. 2017. Thermal stress impacts reproductive development and grain yield in rice. Plant Physiology and Biochemistry, 115, 57-72.
Aroca, R., P. Vernieri, J. J. Irigoyen, M. Sánchez-Dıaz, F. Tognoni and A. Pardossi. 2003. Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Science, 165(3): 671-679.
Bibi, A., S. A. Majid, N. Azhar, M. Sh. Amjad1, S. Ashraf1, I. Ahmad, S. Sadia Mumtaz and Sh. Ijaz, 2020. Differential Changes in Growth and Enzyme Activities of Chilling Induced Wheat Seedlings by Nitric Oxide Priming. International journal of agriculture & biology, 23 (5): 919-926.
Chen, X., X. Shi, X. Cai, F. Yang, L. Li, J. Wu and S. Wang, 2021. Ice-binding proteins: a remarkable ice crystal regulator for frozen foods. Food Science and Nutrition, 61: 3436-3449.
Cheng, W. H., E. W. Taliercio and P. S. Chourey. 1996. The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. The Plant Cell, 8: 971-983.
Colebrook, E. H., S. G. Thomas, A. L. Phillips and P. Hedden, 2014. The role of gibberellin signaling in plant responses to abiotic stress. Journal of Experimental Biology, 217: 67-75.
Dalmannsdottir, S., M. Jørgensen, M. Rapacz, L. Østrem, A. Larsen, R. Rødven and O. A. Rognli. 2017. Cold acclimation in warmer extended autumns impairs freezing tolerance of perennial ryegrass (Lolium perenne L.) and timothy (Phleum pratense L.), Plant Physiology, 160: 266-281.
Devireddy, A. R., S. I. Zandalinas, Y. Fichman and R. Mittler, 2021. Integration of reactive oxygen species and hormone signaling during abiotic stress. The Plant Journal, 105: 459-476.
Ding, Y., J. Sheng, S. Li, Y. Nie, J. Zhao, Z. Zhu, Z. Wang and X. Tang, 2015. The role of gibberellins in the mitigation of chilling injury in cherry tomato (Solanum lycopersicum L.) fruit. Postharvest Biology and Technology, 101: 88-95.
Ding, Y., Y. Shi and S. Yang. 2019. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytologist, 222: 1690-1704.
Deng, X., J. Wang and Y. Li, 2018. Comparative transcriptome analysis reveals phytohormone signaling, heat shock module and ROS scavenger mediate the cold tolerance of rubber tree. Scientific Reports, 8: 4931.
Farooq, M., M. Hussain, A. Nawaz, D. J. Lee, S. S. Alghamdi and KH. M Siddique, 2017. Seed priming improves chilling tolerance in chickpea by modulating germination metabolism, trehalose accumulation and carbon assimilation. Plant Physiology Biochemistry, 111: 274-283.
Gass, T., A. Schori, A. Fossati, A. Soldati, and P. Stamp, 1996. Cold tolerance of soybean (Glycine max L.) during the reproductive phase. European Journal of Agronomy, 5: 71-88.
Hajihashemi, S., F. Noedoost, J. M. C. Geuns, I. Djalovic and KH. M. Siddique, 2018. Effect of Cold Stress on Photosynthetic Traits, Carbohydrates, Morphology, and Anatomy in Nine Cultivars of Stevia rebaudiana. Frontiers in Plant Science, 9: 1430.
Hassan, M. A., C. Xiang, M. Farooq, N. Muhammad, Z. Yan, X. Hui, K. Yuanyuan, A. K. Bruno, Z. Lele and L. Jincai, 2021. Cold stress in wheat: plant acclimation responses and management strategies. Frontiers in Plant Science 12: 676884.
Han, D., J. Han, G. Yang, S. Wang, T. Xu and W. Li, 2020. An ERF transcription factor gene from (Malus baccata L.) Borkh, MbERF11, affects cold and salt stress tolerance in Arabidopsis. Forests, 11: 514.
Han, D., J. Han, T. Xu, X. Li, C. Yao, T. Li, X. Sun, X. Wang and G. Yang, 2021. Overexpression of MbERF12, an ERF gene from (Malus baccata L.) Borkh, increases cold and salt tolerance in Arabidopsis thaliana associated with ROS scavenging through ethylene signal transduction. In Vitro Cell Developmental Biology- Plant, 57: 760-770.
Heidarvand, L and R. Maali-Amiri 2013. Physio-biochemical and proteome analysis of chickpea in early phases of cold stress. Journal of Plant Physiology, 170: 459-469.
Huang, X., H. Shi, Z. Hu, A. Liu, E. Amombo, L. Chen and J. Fu, 2017. ABA is involved in regulation of cold stress response in bermudagrass. Frontiers in Plant Science, 8: 1613.
Hu, Y. R., Y. J. Jiang, X. Han, H. P. Wang, J. J. Pan and D. Q. Yu, 2017. Jasmonate regulates leaf senescence and tolerance to cold stress: Crosstalk with other phytohormones. Journal of Experimental Botany, 68: 13611369.
Hu, Y., L. Jiang, F. Wang and D. Yu, 2013. Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. The Plant Cell, 25: 2907-2924.
Hurry, V. M and N. P. Huner, 1992. Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiology, 100: 1283-1290.
Hussain, H. A., S. Hussain, A. Khaliq, U. Ashraf, S. A. Anjum, S. Men and L. Wang, 2018.Chilling and drought stresses in crop plants: implications, cross talk, and potential management opportunities. Frontiers in Plant Science, 9: 393.
Jan, N., U. Majeed, K. I. Andrabi and R. John, 2018. Cold stress modulates osmolytes and antioxidant system in Calendula officinalis. Acta physiologiae plantarum. 40: 1-16.
Jarzabek, M., P. M. Pukacki and K. Nuc, 2009. Cold-regulated proteins with potent antifreeze and cryoprotective activities in spruces (Picea spp.). Cryobiology, 58: 268-274.
Kidokoro, S., K. Hayashi, H. Haraguchi, T. Ishikawa, F. Soma, I. Konoura, S. Toda, J. Mizoi, T. Suzuki and K. Yamaguchi-Shinozaki, 2021. Posttranslational regulation of multiple clock-related transcription factors triggers cold-inducible gene expression in Arabidopsis. proceedings of the national academy of sciences, india section b. Biological Sciences, 118: e2021048118
Kosova, K., I. T. Prasil and P. Vitamvas, 2008. The relationship between vernalization and photo periodically-regulated genes and the development of frost tolerance in wheat and barley. Biologia Plantarum, 52: 601-615.
Krupa, Z., G. Oquist and P. Gustafsson. 1990. Photoinhibition and Recovery of Photosynthesis in psbA Gene Inactivated Strains of cyanobacterium Anacystis nidulans. Plant Physiology, 93: 1-6.
Lantzouni, O., A. Alkofer, P. Falter-Braun and C. Schwechheimer, 2020. Growth-regulating factors interact with DELLAs and regulate growth in cold stress. The Plant Cell, 32: 1018-1034.
Lei, Y. A. N., T. Shah, Y. Cheng, L. Ü. Yan, X. K. Zhang and X. L. Zou, 2019. Physiological and molecular responses to cold stress in rapeseed (Brassica napus L.). Journal of Integrative Agriculture, 18: 2742-2752.
Lenka, S. K., S. K. Muthusamy, V. Chinnusamy and K. C. Bansal, 2018. Ectopic expression of rice PYL3 enhances cold and drought tolerance in Arabidopsis thaliana. Molecular Biotechnology, 60: 350-361.
Liang, Y., H. Chen, M. J. Tang, P. F. Yang and S. H. Shen, 2007. Responses of Jatropha curcas seedlings to cold stress: Photosynthesis related proteins and chlorophyll fluorescence characteristics. Physiologia Plantarum, 131: 508-517.
Li, Y., Q. Zhang, L. Ou, D. Ji, T. Liu, R. Lan, X. Li and L. Jin, 2020. Response to the cold stress signaling of the tea plant (Camellia sinensis) elicited by chitosan oligosaccharide. Agronomy, 10: 915.
Li, Z., B. Wang, Z. Zhang, W. Luo, Y. Tang, Y. Niu, K. Chong and Y. Xu, 2021. OsGRF6 interacts with SLR1 to regulate OsGA2ox1 expression for coordinating chilling tolerance and growth in rice. Journal of Plant Physiology, 260: 153406.
Li, J., M. A. Muneer, A. Sun, Q. Guo, Y. Wang, Z. Huang, W. Li and C. Zheng, 2023. Magnesium application improves the morphology, nutrients uptake, photosynthetic traits, and quality of tobacco (Nicotiana tabacum L.) under cold stress. Frontiers in Plant Science, 14: 1078128.
Liu, W., H. Wang, Y. Chen, S. Q. Zhu, M. Chen, X. Z. Lan, G. P. Chen and Z. Liao, 2017. Cold stress improves the production of artemisinin depending on the increase in endogenous jasmonate. Biotechnology and Applied Biochemistry, 64: 305-314.
Liu, L., H. Ji, J. An, K. Shi, J. Ma, B. Liu, L. Tang, W. Cao and Y. Zhu, 2019. Response of biomass accumulation in wheat to low-temperature stress at jointing and booting stages. Environmental and Experimental Botany, 157: 46-57.
Liu, W., C. Zheng, J. Chen, J. Qiu, Z. Huang, Q. Wang and Y. Ye, 2018. Cold acclimation improves photosynthesis by regulating the ascorbate-glutathione cycle in chloroplasts of Kandelia obovata. Journal of Forestry Research, 30: 755-765.
Lidon, F. C., A. S. Loureiro, D. E. Vieira, E. A. Bilho, P. Nobre and R. Costa. 2001. Photoinhibition in chilling stressed wheat and maize. Photosynthetica, 39: 161-166.
Llanes, A., G. Devinar and V. Luna, 2015. Role of abscisic acid in legumes under abiotic stress. Legumes Under Environmental Stress: Yield, Improvement and Adaptations. John Wiley & Sons, pp: 145-160.
Lynch, D. V and P. L. Steponkus, 1987. Plasma Membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiology, 83: 761-767.
Marentes, E., M. Griffith, A. Mlynarz and R. Brush, 1993. Proteins accumulate in the apoplast of winter rye leaves during cold acclimation. Physiologia Plantarum, 87: 499-507.
Martino-Catt, S and D. R. Ort, 1992. Low temperature interrupts circadian regulation of transcriptional activity in chilling-sensitive plants. Proceedings of the National Academy of Sciences, 89: 3731-3735.
Miquel, M., D. James, H. Dooner and J. Browse, 1993. Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proceedings of the National Academy of Sciences, 90: 6208-6212.
Moieni-Korbekandi, Z., G. Karimzadeh and M. Sharifi, 2014. Cold-induced changes of proline, malondialdehyde and chlorophyll in spring canola cultivars. Journal of Plant Physiology and Breeding, 4: 1-11.
Mutlu, S., Ö. Karadağoğlu, Ö. Atici and B. Nalbantoğlu. 2013. Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. Biologia Plantarum, 57: 507-513.
Nandagopal, J. G. T and G. Shanmugam, 2022. Screening and differential oxidative stress responses of hot pepper (Capsicum annuum L.) genotypes under cold stress. South African Journal of Botany, 151: 591-599.
Noctor, G and CH. Foyer 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Biology, 49: 249-279.
Pareek, A., A. Khurana, A. Sharma and R. Kumar, 2017. An overview of signaling regulons during cold stress tolerance in plants. Current Genomics, 18: 498-511.
Perez-Llorca, M., P. Munoz, M. Müller, Munn´ and S. e-Bosch, 2019. Biosynthesis, metabolism and function of auxin, salicylic acid and melatonin in climacteric and non-climacteric fruits. Frontiers in Plant Science, 10: 136.
Repkina, N., A. Ignatenko, E. Holoptseva, Z. MiszalskI, P. Kaszycki and V. Talanova, 2021. Exogenous Methyl Jasmonate Improves Cold Tolerance with Parallel Induction of Two Cold-Regulated (COR) Genes Expression in (Triticum aestivum L.)’. Plants, 10: 1421.
Ruelland, E and A. Zachowski, 2010. How plants sense temperature. Environmental and Experimental Botany, 69: 225-232.
Simova-Stoilova, L., K. Demirevska, T. Petrova, N. Tsenov and U. Feller, 2008. Antioxidative protection in wheat varieties under severe recoverable drought at seedling stage. Plant Soil Environ, 54: 529-536.
Singh, R. K., S. Singh, S. Anandhan, L. M. Shannon, F. R. Quiroz-Figueroa and E. Ruiz-May, 2017. First insights into the biochemical and molecular response to cold stress in Cicer micro phylum, a crop wild relative of chickpea (Cicer arietinum L.). Russian Journal of Plant Physiology, 64: 758-765.
Shi, Y., Y. Ding and S. Yang, 2015. Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant and Cell Physiology, 56: 7-15.
Song, Y., X. Zhang, M. Li, H. Yang, D. Fu, J. Lv, Y. Ding, Z. Gong, Y. Shi and S. Yang, 2021. The direct targets of CBFs: in cold stress response and beyond. Journal of Integrative Plant Biology, 63: 1874-1887.
Strand, A., V. Hurry, P. Gustafsson and P. Gardeström, 1997. Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plants, 12: 605-614.
Subedi, K. D., P. J. Gregory, R. J. Summerfield and M. J. Gooding 1998. Cold temperatures and boron deficiency caused grain set failure in spring wheat (Triticum aestivum L.). Field Crops Research, 57: 277-288.
Takahashi, R and E. Shimosaka, 1997. cDNA sequence analysis and expression of two cold-regulated genes in soybean. Plant Science, 123: 93-104.
Thomashow, M. F. 1999. Plant cold acclimation: Freezing Tolerance Genes and Regulatory Mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology, 50: 571-599.
Theocharis, A., C. Clément and E. A. Barka, 2012. Physiological and molecular changes in plants grown at low temperatures. Planta, 235: 1091–1105.
Wan, S. B., L. Tian, R. R. Tian, Q. H. Pan, J. C. Zhan, P. F. Wen ... and W. D. Huang, 2009. Involvement of phospholipase D in the low temperature acclimation-induced thermotolerance in grape berry. Plant Physiology and Biochemistry, 47: 504-510.
Wang, X., Z. Mao, J. Zhang, M. Hemat M. Huang, J. Cai, Q. Zhou, T. Dai and D. Jiang 2019. Osmolyte accumulation plays important roles in the drought priming induced tolerance to post-anthesis drought stress in winter wheat (Triticum aestivum L.). Environmental and Experimental Botany, 166: 103804.
Wang, M., J. Hao, X. Chen and X. Zhang, 2020. SlMYB102 expression enhances low temperature stress resistance in tomato plants. Peer J., 8: e10059.
Wellensiek, S. J. 1964. Dividing cells as prerequisite for vernalization. Plant Physiology, 39: 832.
Wu, J., M. Nadeem, L. Galagedara, R. Thomas and M. Cheema 2022. Effects of Chilling Stress on Morphological, Physiological and Biochemical Attributes of Silage Corn Genotypes During Seedling Establishment. Plants, 11: 1217.
Yan, L., T. Shah, Y. Cheng, Y. Lu, X. Zhang, K. Zou and X. ling. 2019. Physiological and molecular responses to cold stress in rapeseed (Brassica napus L.). Journal of Integrative Agriculture, 18: 2742-2752.
Yuan, S and H. H. Lin, 2008. Mini review: Role of salicylic acid in plant abiotic stress. Zeitschrift für Naturforschung C, 63: 313-320.
Yu, J., J. Cang, Q. W. Lu, B. Fan, Q. H. Xu, W.N. Li and X. T. Wang, 2020. ABA enhanced cold tolerance of wheat ‘dn1’ via increasing ROS scavenging system. Plant Signaling & Behavior, 15: 1780403.
Yang, S. 2022. Cold responses in rice: ‘from physiology to molecular biology. Journal of Plant Physiology, 269: 153602.
Yamasaki, T., T. Yamakawa, Y. Yamane, H. Koike, K. Satoh and S. Katoh, 2002. Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat. Plant Physiology, 128: 1087-1097.
Yousefi, S., A. Marchese, S. A. Salami, J. Benny. A. Giovino A. Perrone, T. Caruso, M. Gholami, H. Sarikhani, M. Buti and F. Martinelli, 2022. Identifying conserved genes involved in crop tolerance to cold stress. Functional Plant Biology, 49: 861-873.
Zhang, W., J. Wang, Z. Huang, L. Mi, K. Xu, J. Wu, Y. Fan, S. Ma and D. Jiang, 2019. Effects of low temperature at booting stage on sucrose metabolism and endogenous hormone contents in winter wheat spikelet. Frontiers in Plant Science, 10: 498.
Yang, J. C and J. Zhang, 2006. Grain filling of cereals under soil drying. New Phytologist, 169: 223-236.
Zhang, K. G., W. Z. Xun, X. K. Fei and S. G. Chou, 2007. Protection of ultrastructure in chilling stressed banana leaves by salicylic acid. Journal of Zhejiang University Science B, 8: 277-282.
Zhang, Q., J. Z. Zhang, W. S. Chow, L. L. Sun, J. W. Chen, Y. J. Chen and C. L. Peng, 2011. The influence of low temperature on photosynthesis and antioxidant enzymes in sensitive banana and tolerant plantain (Musa sp.) cultivars. Photosynthetica, 49: 201-208.
Zhou, X., I. Muhammad, H. Lan and C. Xia, 2022. Recent advances in the analysis of cold tolerance in maize. Frontiers in Plant Science, 13: 866034.
Review |
Investigate the physiological, biochemical, and productivity aspects of crops to cold stress
Roghiyeh Farzi Aminabad* and Safar Nasrollahzadeh
Department of Plant Ecophysiology, Faculty of Agriculture, University of Tabriz, Tabriz, Iran ________________________________________________________________________________
Abstract
Cold stress is one of the environmental factors that affects the growth, development, and productivity of crops in various climates. Understanding the physiological and biochemical mechanisms by which plants respond to this stress can help improve their growth and development. Cold stress can be categorized into two types: freezing stress and chilling stress. Freezing stress occurs when the temperature drops below 0 °C, while chilling stress occurs when the temperature ranges between 0 and 15 °C. Cold stress leads to the destruction or alteration of membrane lipids and proteins, causing a loss of membrane fluidity. This stress also increases the production of reactive oxygen species (ROS), which attack and destroy cell membranes. If cold stress persists, it can ultimately result in plant death. The ICE1-CBF-COR transcription cascade serves as a major signaling pathway activated in response to cold stress in plants. This cascade involves the induction of CBF (C-repeat binding factor) genes, which encode transcription factors that bind to the promoter of cold-responsive (COR) genes, initiating their transcription. Enzymes such as superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), and glutathione reductase (GR) exhibit increased activity in response to low temperatures. Additionally, the accumulation of malondialdehyde (MDA) can serve as an indicator of oxidative stress sensitivity and cold tolerance. Cold stress has detrimental effects on crop yield formation. It initially impairs the reproductive phase of plants, ultimately leading to reduced final yields.
Keywords: Cold, Chilling, Freezing, ICE1, COR Genes
Farzi Aminabad, R. and S. Nasrollahzadeh, 2024. Investigate the physiological, biochemical, and productivity aspects of crops to cold stress. Iranian Journal of Plant Physiology 14 (3), 5141-5153.
|
____________________________________ * Corresponding Author E-mail Address : roghiyehfarzi374@gmail.com Received: December, 2023 Accepted: April, 2024
|
The role of phytohormones in gene regulation to cold tolerance
Cold stress significantly alters several physio-biochemical processes in plants. For instance, exposure to cold stress (4°C for 7 days) in wheat (Triticum aestivum L.) has been shown to decrease photosynthetic efficiency, transpiration, and stomatal conductance, while increasing levels of reactive oxygen species (ROS) and malondialdehyde (MDA). Consequently, these changes lead to a reduction in both root and shoot growth (Repkina et al., 2021). The photosynthetic apparatus is highly susceptible to the effects of cold stress, resulting in a decrease in photosynthetic activity and chlorophyll synthesis (Liu et al., 2019). To counteract the detrimental effects of low temperatures, plants employ defense mechanisms such as osmotic regulation and antioxidant enzymes. Osmotic adjustments facilitate the accumulation of compatible solutes (osmo-protectants), which help protect cell structure and maintain turgor pressure (Wang et al., 2019). This accumulation of osmolytes and antioxidants aids in enhancing the plants' tolerance to cold stress (Jan et al., 2018).
When exposed to low temperatures, plants exhibit various responses, including changes in cell membrane fluidity, disruption of protein structures, decreased activity of antioxidant enzymes, increased production of ROS, alterations in photosynthesis, damage to cell membranes, and electrolyte leakage. Additionally, cold stress influences gene expression patterns and protein synthesis (Ding et al., 2019). Superoxide dismutase (SOD) is the first line of defense against ROS. The inactivation of ROS is carried out by the SOD enzyme. The activity of this enzyme increases in cold-tolerant species and decreases in cold-sensitive chickpea species (Heidarvand and Maali-Amiri, 2013). Following exposure to low temperatures, there is an increasing trend in ascorbate peroxidase (APX), catalase (CAT), SOD, and glutathione reductase (GR) activity, along with proline accumulation in chickpea (Cicer arietinum L.) and Lygodium microphyllum L. (Singh et al., 2017). The accumulation of MDA is higher in cold-sensitive rapeseed cultivars compared to tolerant cultivars (Yan et al., 2019). A similar trend has also been reported in spring canola. Lipid peroxidation occurs less in tolerant cultivars than in cold-sensitive cultivars, resulting in lower levels of MDA in tolerant cultivars. MDA serves as an important indicator for oxidative stress sensitivity analysis and is a reliable measure of plant cold tolerance in plant breeding (Moieni-Korbekandi et al., 2014).
Nandagopal and Shanmugam (2022) observed that glutathione peroxidase (GPX) activity is correlated with CAT, and both enzyme activities significantly increase in all genotypes of pepper (Capsicum annuum L.) under cold stress conditions. At the molecular level, cold stress affects membrane fluidity and subsequently alters membrane permeability. Plants respond to cold stress by inducing physiological and molecular changes, including alterations in the plant metabolic profile. These changes may play a beneficial role in protecting cells during cold stress or before freezing temperatures occur (Thomashow, 1999).
Lipid composition changes and lipid metabolism during cold stress are crucial in determining the extent of cold damage in plants and other species. Increased levels of unsaturated fatty acids in the plasma membrane of acclimated plants enhance membrane fluidity and stability. Studies using fatty acid desaturase (fad2) mutants have demonstrated that polyunsaturated lipids are necessary for survival at cold temperatures in Arabidopsis (Miquel et al., 1993). In cold-acclimated rye (Secale cereale L.), the levels of di-unsaturated molecular species such as phosphatidylcholine and phosphatidylethanolamine were found to increase in the plasma membrane (Lynch and Steponkus, 1987). Similar findings have been reported in tea (Camellia sinensis) (Li et al., 2020) and banana plants (Musa spp.) (Zhang et al., 2011). Interference in the sucrose mechanism under cold stress may cause developmental aberrations in plants, leading to a decrease in the activity of the cell wall invertase enzyme. This results in sucrose accumulation and, consequently, prevents cell division in the endosperm (Cheng et al., 1996).
In conclusion, cold stress has significant effects on various physio-biochemical processes in plants. Exposure to low temperatures can lead to decreased photosynthetic efficiency, transpiration, and stomatal conductance, as well as increased levels of ROS and MDA. These changes ultimately result in reduced root and shoot growth. However, plants have defense mechanisms such as osmotic regulation and antioxidant enzymes to counteract the detrimental effects of cold stress. Osmotic adjustments and the accumulation of osmo-protectants and antioxidants help protect cell structure and maintain turgor, enhancing plant tolerance to cold stress. Cold stress also influences gene expression patterns, protein synthesis, and lipid composition, affecting membrane fluidity and permeability. The activity of enzymes like SOD, APX, CAT, and GR increases in response to low temperatures, while the accumulation of MDA serves as an indicator of oxidative stress sensitivity and cold tolerance. Furthermore, interference in the sucrose mechanism under cold stress can lead to developmental aberrations in plants. Overall, understanding the physiological and molecular changes induced by cold stress is crucial for developing strategies to enhance plant cold tolerance and mitigate the negative impacts of low temperatures.
The role of phytohormones in gene regulation to cold tolerance
Phytohormones, such as abscisic acid (ABA), auxins (IAA), gibberellins (GAs), cytokinins (CKs), salicylic acid (SA), ethylene (ET), brassinosteroids (BRs), and jasmonic acid (JA), play a crucial role in mediating cold stress signaling and regulating the transcription of certain cold-regulated (COR) genes (Deng et al., 2018). When plants experience cold stress, the levels of ABA and JA in the leaves increase, while ET, CKs, and GA decrease. After exposure to cold stress, the concentration of JA increased by up-regulating the expression of JA biosynthetic genes, which positively impacted cold stress tolerance in Artemisia annua (Liu et al., 2017). The exogenous application of JA significantly improved plant freezing tolerance in Arabidopsis, while blocking endogenous JA biosynthesis and signaling decreased plant freezing stress tolerance. Correspondingly, the production of endogenous JA increased after exposure to cold stress (Hu et al., 2013). In addition, several JAZ proteins, repressors of the JA signaling pathway, physically interact with ICE1 and ICE2 and repress their transcriptional functions. Overexpression of JAZ1 and JAZ4 repressed freezing stress responses in Arabidopsis (Hu et al., 2013). GAs have various functions in regulating plant growth processes (Colebrook et al., 2014). Besides growth regulation, GAs can also coordinate plant growth and stress responses to contribute to cold resistance by reducing GA levels and signaling after exposure to cold stress (Colebrook et al., 2014). Overexpression of OsSLR1, which encodes a rice DELLA protein, enhanced chilling tolerance by mediating SLR1 physically interacting with OsGRF6 to increase OsGA2ox1 expression and decrease GA content (Li et al., 2021). Low temperature-induced CBF1 expression results in an increase in DELLA protein accumulation by decreasing GA content. CBF1 enhances freezing tolerance through the synergistic DELLA-dependent and COR-dependent pathways (Achard et al., 2008). Additionally, DELLA proteins act as repressors of the GA hormone signalling pathway, and GRF modulation contributes to cold stress-responsive gene expression (Lantzouni et al., 2020). Phytohormones also have a significant impact on starch and glucose metabolism and the inhibition of ROS (An et al., 2012). The role of SA in plants can vary depending on the level and severity of abiotic stress.
At moderate and severe levels of abiotic stress, SA has been attributed to redox regulation in plant cells (Yuan and Lin, 2008) and the protection of cell structures under cold stress (Zhang et al., 2007). SA plays crucial roles in response to external stimuli and activates the defense system in plants. The activation of phospholipase D is an early response to low temperatures and is involved in the accumulation of free SA, as well as the development of thermotolerance induced by low-temperature acclimation in grape berries (Vitis vinifera) (Wan et al., 2009). SA in plants promotes growth, ripening, and tolerance to abiotic stresses (Perez-Llorca et al., 2019). Various studies have demonstrated that foliar application of salicylic acid on different plants enhances cold stress tolerance. For instance, in Solanum lycopersicum, applying 0.2 mM salicylic acid during the fruit formation stage increased the levels of antioxidant enzymes, malondialdehyde, and proline contents, thereby enhancing cold tolerance (Ding et al., 2015). The response factors of ethylene primarily participate in the plant's response to biotic and abiotic stress. Han et al. (2020) isolated an ERF gene (MbERF11) from Siberian crabapple (Malus baccata Borkh.). When transformed into transgenic Arabidopsis, MbERF11 enhanced cold and salt tolerance by increasing the activities of antioxidant enzymes such as CAT, POD, and SOD, as well as the levels of photosynthesis pigments such as chlorophylls and proline contents. Additionally, it decreased the MDA content and scavenged ROS (Han et al., 2021). ABA plays a pivotal role as a hormone in regulating cold stress responses in plants. In Cynodon dactylon, the application of exogenous ABA has been shown to enhance cold tolerance by preserving cell membrane stability and modulating the expression of ABA and cold-related genes such as ABF1, CBF1, and LEA (Huang et al., 2017). Moreover, the ectopic overexpression of the ABA receptor OSPYL3 in Arabidopsis has been demonstrated to improve cold tolerance (Lenka et al., 2018). Low temperatures reduce water availability in plant cells, leading to osmotic stress and the stimulation of ABA biosynthesis (Chen et al., 2021). Endogenous abscisic acid is then transferred from the roots to the shoots, where it accumulates in the guard cells, causing water to escape and resulting in stomatal closure. Consequently, transcription and cell growth are reduced (Llanes et al., 2015). In Triticum aestivum, the application of exogenous ABA has been found to enhance cold tolerance by increasing the activities of various antioxidant enzymes. These enzymes include CAT, SOD, POD, APX, GR, dehydroascorbate reductase (DHAR), and monodehydroascorbate reductase (MDHAR) (Yu et al., 2020).
Fig. I. An overview of some phytohormones involved in regulating stress responses and altering external and internal responses under cold stress
Fig. II. Genome mapping of cold stress-modulated genes of key categories involved in abiotic stress responses in common in tolerant and sensitive genotypes |
Cold tolerant genes
Cold stress activates multiple downstream signaling pathways in plant cells, most notably the ICE1-CBF-COR (inducer of CBF expression-C-repeat-binding factors-cold-regulated genes) transcription cascade (Shi et al., 2015; Ding et al., 2015; Yang, 2022). This cascade induces the formation of complexes, such as CBFs/DREBs, that bind to the promoters of COR genes, initiating their transcription (Fig. 2). These signaling pathways lead to the activation of multigene families associated with transcription factors (TFs) like MYB, WRKY, NAC, bZIP, and APETALA2/ethylene-responsive element binding factor (AP2/ERF), which are crucial for stress responses (Wang et al., 2020; KidokoroH et al., 2021; Song et al., 2021).
During cold acclimation, low molecular mass polypeptides (15 to 32 kDa) accumulate in the leaf apoplast of plants such as winter rye and spruce (Marentes et al., 1993; Jarzabek et al., 2009). These polypeptides likely enhance cold tolerance by lowering the freezing point in the apoplastic space during cold stress. Being sessile, plants exhibit a broad range of gene expression patterns to tolerate cold stress and adapt to changing environmental conditions. The severity of cold stress decreases over time as plants undergo physiological, biochemical, and molecular changes (Dalmannsdottir et al., 2017).
In two of four analyzed datasets (rice 1 and rice 2; Oryza sativa L.), genes related to cell walls were upregulated in both cold-sensitive and one cold-tolerant genotype (Sorghum bicolor L.). Genes linked to secondary metabolism were upregulated in cold-sensitive Vigna unguiculata subsp. Sesquipedalis and cold-tolerant sorghum. Conversely, genes related to protein synthesis were downregulated in tolerant rice 1, rice 2, beans, and sorghum, and also in sensitive rice 1, rice 2, and sorghum. No other common gene categories were modulated by cold stress across the datasets (Fig. II).
The ICE1-CBF-COR transcription cascade is a key signaling pathway triggered by cold stress. This cascade initiates the expression of CBF genes, which encode transcription factors that activate COR gene transcription. These responses are regulated by several TF families, including MYB, WRKY, NAC, bZIP, and AP2/ERF. Additionally, cold acclimation leads to the accumulation of low molecular weight polypeptides in the leaf apoplast, which may lower the freezing point, contributing to enhanced cold tolerance. Ultimately, plants exhibit a wide range of gene expression adjustments in response to cold stress, gradually reducing its severity through physiological, biochemical, and molecular changes. Differential gene expression patterns related to cell wall composition, secondary metabolism, and protein synthesis vary depending on the plant species and genotype in response to cold stress.
Plant growth and productivity
Table 1 The effect of cold stress on some physiological, biochemical and yield of different crops
|
Furthermore, cold stress severely damages crop yield formation, starting with reproductive phase impairments characterized by sterile pollen, aborted ovules, and undersized grains, ultimately reducing final yields (Arshad et al., 2017; Zhang et al., 2019). This cold sensitivity can cause yield losses of 30-40% in rice and up to 78% in wheat, primarily due to reproductive disturbances and later grain development issues at temperatures below 10°C (Subedi et al., 1998). During the reproductive stage, low temperatures may result in flower drop, pollen sterility, and reduced fruit formation, which further decreases plant yield (Albertos et al., 2019).
Cold stress can lead to irregular distribution of pods and grains along the stem, with reduced pod formation occurring when night temperatures drop below 8°C (Gass et al., 1996). The response to cold stress and pod formation varies among different soybean cultivars, with gene expression regulation playing a crucial role in cold tolerance (Takahashi and Shimosaka, 1997). Additionally, low temperatures can induce early flowering through vernalization, a process that affects active and dividing cells beyond the meristem regions (Wellensiek, 1964). Vernalization is a phenological response to cold, delaying the transition from the relatively cold-tolerant vegetative stage to the more sensitive reproductive stage until milder temperatures are encountered (Kosova et al., 2008).
In wheat, cold temperatures affect phenology and grain filling, prolonging the vegetative phase before flowering (Subedi et al., 1998). The deposition of reserve nutrients during grain filling is also influenced by fluctuating environmental conditions, which can significantly impact both the quantity and quality of yield (Yang and Zhang, 2006).
In conclusion, cold stress has a direct impact on the photosynthetic apparatus, reducing photosynthetic efficiency and increasing the production of reactive oxygen species (ROS). Proteins involved in photosynthesis may be either up-regulated or down-regulated in response to cold stress. Additionally, cold stress negatively affects crop yield formation, starting with reproductive impairments and ultimately leading to reduced final yields. Rice and wheat, in particular, are highly sensitive to cold stress, with substantial yield losses reported.
Cold stress also causes irregular pod and grain distribution along the stem, and the effects on phenology and grain filling further exacerbate the decline in yield. Lastly, vernalization triggered by cold temperatures delays the transition from vegetative to reproductive stages, allowing plants to avoid entering sensitive phases until temperatures are more favorable.
Conclusion and Future Prospects
In recent years, significant advancements have been made in understanding how plants respond to cold stress, encompassing physiological, biochemical, and molecular aspects. Cold stress is a major climatic challenge that negatively impacts crop productivity and food security. However, the precise mechanisms by which plants sense and respond to cold signals remain elusive.
When exposed to low temperatures, plants activate cold responses through both CBF-dependent and CBF-independent pathways. The CBF1 transcription factor enhances freezing tolerance through synergistic DELLA-dependent and COR-dependent pathways. While considerable progress has been made in understanding these cold signaling pathways, the molecular mechanisms underlying cold signal perception and transduction still require further investigation.
Cold stress can decrease the photosynthetic rate, transpiration rate, total chlorophyll content, and water use efficiency. These changes can lead to reduced grain yield and productivity. Additionally, cold stress increases the levels of soluble sugars, proline, lipid peroxidation, and enzyme activities such as catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD), as well as the content of gibberellic acid (GA) and abscisic acid (ABA) in crops (Table 1).
Plant hormones, including salicylic acid (SA), jasmonic acid (JA), ABA, and gibberellic acid (GA), play a crucial role in enhancing cold resistance. They do so by increasing soluble sugars, soluble proteins, and proline, scavenging reactive oxygen species (ROS), and activating the antioxidant defense system.
One proposed mechanism for cold signal perception involves the plasma membrane. It is hypothesized that changes in membrane fluidity and ion channel activity may be involved in sensing and transmitting cold signals within the plant. However, further research is necessary to fully elucidate these processes.
Acknowledgement
We are propitiated to Tabriz University for their generous support and assistance throughout the research process.
References
Achard, P., F. Gong, S. Cheminant, M. Alioua, P. Hedden and P. Genschik. 2008. The cold inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. The Plant Cell, 20: 2117-2129.
Albertos, B., K. Wanger and B. Poppenberger. 2019. Cold stress signaling in female reproductive tissues. Plant Cell Environ, 42: 846-853.
An, D., J. Yang and P. Zhang. 2012. Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC genomics, 13: 1-25.
Arshad, M. S., Farooq, M., Asch, F., Krishna, J. S., Prasad, P. V., & Siddique, K. H. 2017. Thermal stress impacts reproductive development and grain yield in rice. Plant Physiology and Biochemistry, 115, 57-72.
Aroca, R., P. Vernieri, J. J. Irigoyen, M. Sánchez-Dıaz, F. Tognoni and A. Pardossi. 2003. Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Science, 165(3): 671-679.
Bibi, A., S. A. Majid, N. Azhar, M. Sh. Amjad1, S. Ashraf1, I. Ahmad, S. Sadia Mumtaz and Sh. Ijaz, 2020. Differential Changes in Growth and Enzyme Activities of Chilling Induced Wheat Seedlings by Nitric Oxide Priming. International journal of agriculture & biology, 23 (5): 919-926.
Chen, X., X. Shi, X. Cai, F. Yang, L. Li, J. Wu and S. Wang, 2021. Ice-binding proteins: a remarkable ice crystal regulator for frozen foods. Food Science and Nutrition, 61: 3436-3449.
Cheng, W. H., E. W. Taliercio and P. S. Chourey. 1996. The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. The Plant Cell, 8: 971-983.
Colebrook, E. H., S. G. Thomas, A. L. Phillips and P. Hedden, 2014. The role of gibberellin signaling in plant responses to abiotic stress. Journal of Experimental Biology, 217: 67-75.
Dalmannsdottir, S., M. Jørgensen, M. Rapacz, L. Østrem, A. Larsen, R. Rødven and O. A. Rognli. 2017. Cold acclimation in warmer extended autumns impairs freezing tolerance of perennial ryegrass (Lolium perenne L.) and timothy (Phleum pratense L.), Plant Physiology, 160: 266-281.
Devireddy, A. R., S. I. Zandalinas, Y. Fichman and R. Mittler, 2021. Integration of reactive oxygen species and hormone signaling during abiotic stress. The Plant Journal, 105: 459-476.
Ding, Y., J. Sheng, S. Li, Y. Nie, J. Zhao, Z. Zhu, Z. Wang and X. Tang, 2015. The role of gibberellins in the mitigation of chilling injury in cherry tomato (Solanum lycopersicum L.) fruit. Postharvest Biology and Technology, 101: 88-95.
Ding, Y., Y. Shi and S. Yang. 2019. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytologist, 222: 1690-1704.
Deng, X., J. Wang and Y. Li, 2018. Comparative transcriptome analysis reveals phytohormone signaling, heat shock module and ROS scavenger mediate the cold tolerance of rubber tree. Scientific Reports, 8: 4931.
Gass, T., A. Schori, A. Fossati, A. Soldati, and P. Stamp, 1996. Cold tolerance of soybean (Glycine max L.) during the reproductive phase. European Journal of Agronomy, 5: 71-88.
Hajihashemi, S., F. Noedoost, J. M. C. Geuns, I. Djalovic and KH. M. Siddique, 2018. Effect of Cold Stress on Photosynthetic Traits, Carbohydrates, Morphology, and Anatomy in Nine Cultivars of Stevia rebaudiana. Frontiers in Plant Science, 9: 1430.
Han, D., J. Han, G. Yang, S. Wang, T. Xu and W. Li, 2020. An ERF transcription factor gene from (Malus baccata L.) Borkh, MbERF11, affects cold and salt stress tolerance in Arabidopsis. Forests, 11: 514.
Han, D., J. Han, T. Xu, X. Li, C. Yao, T. Li, X. Sun, X. Wang and G. Yang, 2021. Overexpression of MbERF12, an ERF gene from (Malus baccata L.) Borkh, increases cold and salt tolerance in Arabidopsis thaliana associated with ROS scavenging through ethylene signal transduction. In Vitro Cell Developmental Biology- Plant, 57: 760-770.
Heidarvand, L and R. Maali-Amiri 2013. Physio-biochemical and proteome analysis of chickpea in early phases of cold stress. Journal of Plant Physiology, 170: 459-469.
Huang, X., H. Shi, Z. Hu, A. Liu, E. Amombo, L. Chen and J. Fu, 2017. ABA is involved in regulation of cold stress response in bermudagrass. Frontiers in Plant Science, 8: 1613.
Hu, Y. R., Y. J. Jiang, X. Han, H. P. Wang, J. J. Pan and D. Q. Yu, 2017. Jasmonate regulates leaf senescence and tolerance to cold stress: Crosstalk with other phytohormones. Journal of Experimental Botany, 68: 13611369.
Hu, Y., L. Jiang, F. Wang and D. Yu, 2013. Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. The Plant Cell, 25: 2907-2924.
Hurry, V. M and N. P. Huner, 1992. Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiology, 100: 1283-1290.
Hussain, H. A., S. Hussain, A. Khaliq, U. Ashraf, S. A. Anjum, S. Men and L. Wang, 2018.Chilling and drought stresses in crop plants: implications, cross talk, and potential management opportunities. Frontiers in Plant Science, 9: 393.
Jan, N., U. Majeed, K. I. Andrabi and R. John, 2018. Cold stress modulates osmolytes and antioxidant system in Calendula officinalis. Acta physiologiae plantarum. 40: 1-16.
Jarzabek, M., P. M. Pukacki and K. Nuc, 2009. Cold-regulated proteins with potent antifreeze and cryoprotective activities in spruces (Picea spp.). Cryobiology, 58: 268-274.
Kidokoro, S., K. Hayashi, H. Haraguchi, T. Ishikawa, F. Soma, I. Konoura, S. Toda, J. Mizoi, T. Suzuki and K. Yamaguchi-Shinozaki, 2021. Posttranslational regulation of multiple clock-related transcription factors triggers cold-inducible gene expression in Arabidopsis. proceedings of the national academy of sciences, india section b. Biological Sciences, 118: e2021048118
Kosova, K., I. T. Prasil and P. Vitamvas, 2008. The relationship between vernalization and photo periodically-regulated genes and the development of frost tolerance in wheat and barley. Biologia Plantarum, 52: 601-615.
Krupa, Z., G. Oquist and P. Gustafsson. 1990. Photoinhibition and Recovery of Photosynthesis in psbA Gene Inactivated Strains of cyanobacterium Anacystis nidulans. Plant Physiology, 93: 1-6.
Lantzouni, O., A. Alkofer, P. Falter-Braun and C. Schwechheimer, 2020. Growth-regulating factors interact with DELLAs and regulate growth in cold stress. The Plant Cell, 32: 1018-1034.
Lei, Y. A. N., T. Shah, Y. Cheng, L. Ü. Yan, X. K. Zhang and X. L. Zou, 2019. Physiological and molecular responses to cold stress in rapeseed (Brassica napus L.). Journal of Integrative Agriculture, 18: 2742-2752.
Lenka, S. K., S. K. Muthusamy, V. Chinnusamy and K. C. Bansal, 2018. Ectopic expression of rice PYL3 enhances cold and drought tolerance in Arabidopsis thaliana. Molecular Biotechnology, 60: 350-361.
Liang, Y., H. Chen, M. J. Tang, P. F. Yang and S. H. Shen, 2007. Responses of Jatropha curcas seedlings to cold stress: Photosynthesis related proteins and chlorophyll fluorescence characteristics. Physiologia Plantarum, 131: 508-517.
Li, Y., Q. Zhang, L. Ou, D. Ji, T. Liu, R. Lan, X. Li and L. Jin, 2020. Response to the cold stress signaling of the tea plant (Camellia sinensis) elicited by chitosan oligosaccharide. Agronomy, 10: 915.
Li, Z., B. Wang, Z. Zhang, W. Luo, Y. Tang, Y. Niu, K. Chong and Y. Xu, 2021. OsGRF6 interacts with SLR1 to regulate OsGA2ox1 expression for coordinating chilling tolerance and growth in rice. Journal of Plant Physiology, 260: 153406.
Li, J., M. A. Muneer, A. Sun, Q. Guo, Y. Wang, Z. Huang, W. Li and C. Zheng, 2023. Magnesium application improves the morphology, nutrients uptake, photosynthetic traits, and quality of tobacco (Nicotiana tabacum L.) under cold stress. Frontiers in Plant Science, 14: 1078128.
Liu, W., H. Wang, Y. Chen, S. Q. Zhu, M. Chen, X. Z. Lan, G. P. Chen and Z. Liao, 2017. Cold stress improves the production of artemisinin depending on the increase in endogenous jasmonate. Biotechnology and Applied Biochemistry, 64: 305-314.
Liu, L., H. Ji, J. An, K. Shi, J. Ma, B. Liu, L. Tang, W. Cao and Y. Zhu, 2019. Response of biomass accumulation in wheat to low-temperature stress at jointing and booting stages. Environmental and Experimental Botany, 157: 46-57.
Liu, W., C. Zheng, J. Chen, J. Qiu, Z. Huang, Q. Wang and Y. Ye, 2018. Cold acclimation improves photosynthesis by regulating the ascorbate-glutathione cycle in chloroplasts of Kandelia obovata. Journal of Forestry Research, 30: 755-765.
Llanes, A., G. Devinar and V. Luna, 2015. Role of abscisic acid in legumes under abiotic stress. Legumes Under Environmental Stress: Yield, Improvement and Adaptations. John Wiley & Sons, pp: 145-160.
Lynch, D. V and P. L. Steponkus, 1987. Plasma Membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiology, 83: 761-767.
Marentes, E., M. Griffith, A. Mlynarz and R. Brush, 1993. Proteins accumulate in the apoplast of winter rye leaves during cold acclimation. Physiologia Plantarum, 87: 499-507.
Martino-Catt, S and D. R. Ort, 1992. Low temperature interrupts circadian regulation of transcriptional activity in chilling-sensitive plants. Proceedings of the National Academy of Sciences, 89: 3731-3735.
Moieni-Korbekandi, Z., G. Karimzadeh and M. Sharifi, 2014. Cold-induced changes of proline, malondialdehyde and chlorophyll in spring canola cultivars. Journal of Plant Physiology and Breeding, 4: 1-11.
Mutlu, S., Ö. Karadağoğlu, Ö. Atici and B. Nalbantoğlu. 2013. Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. Biologia Plantarum, 57: 507-513.
Nandagopal, J. G. T and G. Shanmugam, 2022. Screening and differential oxidative stress responses of hot pepper (Capsicum annuum L.) genotypes under cold stress. South African Journal of Botany, 151: 591-599.
Noctor, G and CH. Foyer 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Biology, 49: 249-279.
Pareek, A., A. Khurana, A. Sharma and R. Kumar, 2017. An overview of signaling regulons during cold stress tolerance in plants. Current Genomics, 18: 498-511.
Perez-Llorca, M., P. Munoz, M. Müller, Munn´ and S. e-Bosch, 2019. Biosynthesis, metabolism and function of auxin, salicylic acid and melatonin in climacteric and non-climacteric fruits. Frontiers in Plant Science, 10: 136.
Repkina, N., A. Ignatenko, E. Holoptseva, Z. MiszalskI, P. Kaszycki and V. Talanova, 2021. Exogenous Methyl Jasmonate Improves Cold Tolerance with Parallel Induction of Two Cold-Regulated (COR) Genes Expression in (Triticum aestivum L.)’. Plants, 10: 1421.
Simova-Stoilova, L., K. Demirevska, T. Petrova, N. Tsenov and U. Feller, 2008. Antioxidative protection in wheat varieties under severe recoverable drought at seedling stage. Plant Soil Environ, 54: 529-536.
Singh, R. K., S. Singh, S. Anandhan, L. M. Shannon, F. R. Quiroz-Figueroa and E. Ruiz-May, 2017. First insights into the biochemical and molecular response to cold stress in Cicer micro phylum, a crop wild relative of chickpea (Cicer arietinum L.). Russian Journal of Plant Physiology, 64: 758-765.
Shi, Y., Y. Ding and S. Yang, 2015. Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant and Cell Physiology, 56: 7-15.
Song, Y., X. Zhang, M. Li, H. Yang, D. Fu, J. Lv, Y. Ding, Z. Gong, Y. Shi and S. Yang, 2021. The direct targets of CBFs: in cold stress response and beyond. Journal of Integrative Plant Biology, 63: 1874-1887.
Subedi, K. D., P. J. Gregory, R. J. Summerfield and M. J. Gooding 1998. Cold temperatures and boron deficiency caused grain set failure in spring wheat (Triticum aestivum L.). Field Crops Research, 57: 277-288.
Takahashi, R and E. Shimosaka, 1997. cDNA sequence analysis and expression of two cold-regulated genes in soybean. Plant Science, 123: 93-104.
Theocharis, A., C. Clément and E. A. Barka, 2012. Physiological and molecular changes in plants grown at low temperatures. Planta, 235: 1091–1105.
Wang, X., Z. Mao, J. Zhang, M. Hemat M. Huang, J. Cai, Q. Zhou, T. Dai and D. Jiang 2019. Osmolyte accumulation plays important roles in the drought priming induced tolerance to post-anthesis drought stress in winter wheat (Triticum aestivum L.). Environmental and Experimental Botany, 166: 103804.
Wang, M., J. Hao, X. Chen and X. Zhang, 2020. SlMYB102 expression enhances low temperature stress resistance in tomato plants. Peer J., 8: e10059.
Wellensiek, S. J. 1964. Dividing cells as prerequisite for vernalization. Plant Physiology, 39: 832.
Wu, J., M. Nadeem, L. Galagedara, R. Thomas and M. Cheema 2022. Effects of Chilling Stress on Morphological, Physiological and Biochemical Attributes of Silage Corn Genotypes During Seedling Establishment. Plants, 11: 1217.
Yan, L., T. Shah, Y. Cheng, Y. Lu, X. Zhang, K. Zou and X. ling. 2019. Physiological and molecular responses to cold stress in rapeseed (Brassica napus L.). Journal of Integrative Agriculture, 18: 2742-2752.
Yuan, S and H. H. Lin, 2008. Mini review: Role of salicylic acid in plant abiotic stress. Zeitschrift für Naturforschung C, 63: 313-320.
Yu, J., J. Cang, Q. W. Lu, B. Fan, Q. H. Xu, W.N. Li and X. T. Wang, 2020. ABA enhanced cold tolerance of wheat ‘dn1’ via increasing ROS scavenging system. Plant Signaling & Behavior, 15: 1780403.
Yang, S. 2022. Cold responses in rice: ‘from physiology to molecular biology. Journal of Plant Physiology, 269: 153602.
Yousefi, S., A. Marchese, S. A. Salami, J. Benny. A. Giovino A. Perrone, T. Caruso, M. Gholami, H. Sarikhani, M. Buti and F. Martinelli, 2022. Identifying conserved genes involved in crop tolerance to cold stress. Functional Plant Biology, 49: 861-873.
Zhang, W., J. Wang, Z. Huang, L. Mi, K. Xu, J. Wu, Y. Fan, S. Ma and D. Jiang, 2019. Effects of low temperature at booting stage on sucrose metabolism and endogenous hormone contents in winter wheat spikelet. Frontiers in Plant Science, 10: 498.
Yang, J. C and J. Zhang, 2006. Grain filling of cereals under soil drying. New Phytologist, 169: 223-236.
Zhang, K. G., W. Z. Xun, X. K. Fei and S. G. Chou, 2007. Protection of ultrastructure in chilling stressed banana leaves by salicylic acid. Journal of Zhejiang University Science B, 8: 277-282.
Zhang, Q., J. Z. Zhang, W. S. Chow, L. L. Sun, J. W. Chen, Y. J. Chen and C. L. Peng, 2011. The influence of low temperature on photosynthesis and antioxidant enzymes in sensitive banana and tolerant plantain (Musa sp.) cultivars. Photosynthetica, 49: 201-208.
Zhou, X., I. Muhammad, H. Lan and C. Xia, 2022. Recent advances in the analysis of cold tolerance in maize. Frontiers in Plant Science, 13: 866034.
