Skip to main content
SpringerLink
Log in

Cold stress modulates osmolytes and antioxidant system in Calendula officinalis

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Understanding the mechanism of adaptation to low-temperature stress is very crucial for developing cold-tolerant crop plants. The present study was used to investigate the response of Calendula officinalis (C. officinalis) to cold stress (CS). Seeds of C. officinalis were grown at normal temperature of 25 °C for 14 days and then shifted to a growth chamber set at 4 °C. The response of C. officinalis seedlings to cold stress was evaluated by estimating the relative growth changes, chlorophyll, electrolyte leakage (EL) and the content of malondialdehyde (MDA), proline, glycine betaine (GB), total soluble sugars, trehalose, total protein content and fatty acid profile. Enzymatic activity of antioxidants such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and glutathione reductase (GR) was also assessed. Moreover, transcript expression of cold-responsive genes [APX, CAT, dehydration-responsive element-binding protein (DREB1), GR and SOD] was also evaluated on homology basis. We measured and compared these indices of seedlings leaves under low temperature (4 °C) and normal temperature (25 °C) and observed that on exposure to CS, C. officinalis shows higher accumulation of osmoprotectants (proline, soluble sugars, glycine betaine and trehalose), phenolics and proteins, and increased antioxidant enzyme activity (APX, GR and SOD) except CAT activity, which declined in cold-stressed plants. Transcript expression of cold-responsive genes (SOD, CAT, APX, GR and DREB1) was found to be upregulated under cold stress. Overall, our study suggests that cold exposure/CS, besides eliciting various biochemical/physiological responses, triggers various pathways causing differential gene expression, consequently leading to differential protein expression. Further, this is the first report of C. officinalis under cold stress that may help us in exploring the mechanism of cold tolerance in future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abdallah MMS, Abdelgawad ZA, El-Bassiouny HMS (2016) Alleviation of the adverse effects of salinity stress using trehalose in two rice varieties. S Afr J Bot. https://doi.org/10.1016/j.sajb.2015.09.019

    Google Scholar 

  • Aghaee A, Moradi F, Zare-Maivan H, Zarinkamar F, Irandoost HP, Sharifi P (2011) Physiological responses of two rice (Oryza sativa L.) genotypes to chilling stress at seedling stage. Afr J Biotechnol 10:7617–7621

    Google Scholar 

  • Aono M, Saji H, Fujiyama K, Sugita M, Kondo N, Tanaka K (1995) Decrease in activity of glutathione reductase enhances paraquat sensitivity in transgenic Nicotiana tabacum. Plant Physiol 107:645–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apak R, Güçlü K, Özyürek M, Çelik SE (2008) Mechanism of antioxidant capacity assays and the CUPRAC (cupric ion reducing antioxidant capacity) assay. Microchim Acta 160:413–419

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Aras S, Eşitken A (2013) Effects of antifreeze proteins and glycine betaine on strawberry plants for resistance to cold temperature. ICABT 60:21 (IACSIT Press, Singapore)

    Google Scholar 

  • Arbona V, Manzi M, Zandalinas SI, Vives-Peris V, Pérez-Clemente RM, Gómez-Cadenas A (2017) Physiological, metabolic and molecular responses of plants to abiotic stress. In stress signaling in plants. Genom Proteom Perspect 2:1–35

    Article  Google Scholar 

  • Asif M (2015) Pharmacological activities and phytochemistry of various plant containing coumarin derivatives. Curr Sci Perspect 1:77–90

    Google Scholar 

  • Azymi S, Sofalian O, Jahanbakhsh GS, Khomari S (2012) Effect of chilling stress on soluble protein, sugar and proline accumulation in cotton (Gossypium hirsutum L.) genotypes. Int J Agric Crop Sci 4:825–830

    Google Scholar 

  • Bano S, Aslam M, Saleem M, Basra SMA, Aziz K (2015) Evaluation of maize accessions under low temperature stress at early growth stages. J Anim Plant Sci 25:392–400

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–208

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292

    Article  CAS  PubMed  Google Scholar 

  • Cansev A, Gulen H, Celik G, Eris A (2012) Alterations in total phenolic content and antioxidant capacity in response to low temperatures in olive (Olea europaea L. “Gemlik”). Plant Arch 12:489–494

    Google Scholar 

  • Cavalcanti FR, Oliveira JTA, M-Miranda AS, Viegas RA, Silveira JAG (2004) Superoxide dismutase, catalase and peroxidase activities do not confer protection against oxidative damage in salt-stressed cowpea leaves. New Phytol 163:563–571

    Article  CAS  Google Scholar 

  • Chakraborty A, Bhattacharjee S (2015) Differential competence of redox-regulatory mechanism under extremes of temperature determines growth performances and cross tolerance in two indica rice cultivars. J Plant Physiol 176:65–77

    Article  CAS  PubMed  Google Scholar 

  • Chassot A, Richner W (2002) Root characteristics and phosphorus uptake of maize seedlings in a bilayered soil. Agron J 94:118–127

    Article  Google Scholar 

  • Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, Varma A (2016) Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stresses. J Plant Growth Regul 35:276–300

    Article  CAS  Google Scholar 

  • Cyril J, Powell GL, Duncan RR, Baird WV (2002) Changes in membrane polar lipid fatty acids of Seashore Paspalum in response to low temperature exposure. Crop Sci 42:2031–2037

    Article  CAS  Google Scholar 

  • Dar GH, Malik AH, Khuroo AA (2014) A Contribution to the flora of Rajouri and Poonch districts in the Pir Panjal Himalaya (Jammu & Kashmir), India. Check List 10:317–328

    Article  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inz´e D, Van Breusegen D (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  CAS  PubMed  Google Scholar 

  • de Azevedo Neto AD, Prisco JT, Eneas-Filho J, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on anti-oxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94

    Article  Google Scholar 

  • de Carvalho MC (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165

    Article  Google Scholar 

  • Dey PM (1990) Oligosaccharides. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry, carbohydrates, vol 2. Academic Press, London, pp 189–218

    Chapter  Google Scholar 

  • Di Fenza M, Hogg B, Grant J, Barth S (2017) Transcriptomic response of maize primary roots to low temperatures at seedling emergence. Peer J 5:e2839

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding S, Lu Q, Zhang Y, Yang Z, Wen X, Zhang L, Lu C (2009) Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Mol Biol 69:577–592

    Article  CAS  PubMed  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multi-functional molecule. Glycobiology 13:17–27

    Article  Google Scholar 

  • Ershadi A, Karimi R, Mahdei KN (2016) Freezing tolerance and its relationship with soluble carbohydrates, proline and water content in 12 grapevine cultivars. Acta Physiol Plant 38:2

    Article  Google Scholar 

  • Fan J, Ren J, Zhu W, Amombo E, Fu J, Chen L (2014) Antioxidant responses and gene expression in Bermuda grass under cold stress. J Am Soc Hortic Sci 139:1–7

    Google Scholar 

  • Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furlan A, Bianucci E, Tordable M, Castro S, Dietz KJ (2013) Antioxidant enzyme activities and gene expression patterns in peanut nodules during a drought and rehydration cycle. Funct Plant Biol 41:704–713

    Article  Google Scholar 

  • Genard H, Le Saos J, Hillard J, Tremolieres A, Boucaud J (1991) Effect of salinity on lipid composition, glycine betaine content and photosynthetic activity in chloroplasts of Suaeda maritime. Plant Physiol Biochem 29:421–427

    CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Greive CM, Grattan SR (1983) Rapid assay for determination of water-soluble quaternary amino compounds. Plant Soil 70:303–307

    Article  Google Scholar 

  • Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    Article  CAS  PubMed  Google Scholar 

  • Haldimann P (1999) How do changes in temperature during growth affect leaf pigment composition and photosynthesis in Zea mays genotypes differing in sensitivity to low temperature? J Exp Bot 50:543–550

    Article  CAS  Google Scholar 

  • Halliwell B, Foyer CH (1978) Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. Planta 139:9–17

    Article  CAS  PubMed  Google Scholar 

  • Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS, Chen SY (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313

    Article  CAS  PubMed  Google Scholar 

  • Harb A, Awad D, Samarah N (2015) Gene expression and activity of antioxidant enzymes in barley (Hordeum vulgare L.) under controlled severe drought. J Plant Interact 10:109–116

    Article  CAS  Google Scholar 

  • Hayashi H, Mustardy L, Deshnium P, Ida M, Murata N (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycine betaine and enhanced tolerance to salt and cold stress. Plant J 12:133–142

    Article  CAS  PubMed  Google Scholar 

  • Hossain M, Mostofa M, Fujita M (2013) Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol Plant Breed 4:50–70

    Google Scholar 

  • Hsiao TC, Xu LK (2000) Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport. J Exp Bot 51:1595–1616

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA, Selvaraj G (2000) Genetic engineering of glycine betaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol 122:747–756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hund A, Fracheboud Y, Soldati A, Frascaroli E, Salvi S, Stamp P (2004) QTL controlling root and shoot traits of maize seedlings under cold stress. Theor Appl Genet 109:618–629

    Article  CAS  PubMed  Google Scholar 

  • Hund A, Richner W, Soldati A, Fracheboud Y, Stamp P (2007) Root morphology and photosynthetic performance of maize inbred lines at low temperature. Eur J Agron 27:52–61

    Article  Google Scholar 

  • Jan N, John R (2017) Calendula officinalis-an important medicinal plant with potential biological properties. Proc Indian Nat Sci Acad 83(4):769–787

    Google Scholar 

  • Jan N, Hussain M, Andrabi KI (2009) Cold resistance in plants: a mystery unresolved. Electron J Biotechnol 12:15

    Article  Google Scholar 

  • Janmohammadi M (2012) Metabolomic analysis of low temperature responses in plants. Curr Opin Agric 1:1

    Google Scholar 

  • Janska A, Marsik P, Zelenkova S, Ovesna J (2010) Cold stress and acclimation: what is important for metabolic adjustment? Plant Biol 12:395–405

    Article  CAS  PubMed  Google Scholar 

  • John R, Anjum NA, Sopory SK, Akram NA, Ashraf M (2016) Some key physiological and molecular processes of cold acclimation. Biol Plant 60:603–618

    Article  CAS  Google Scholar 

  • John R, Raja V, Ahmad M, Jan N, Majeed U, Ahmad S, Yaqoob U, Kaul T (2017) Trehalose: metabolism and role in stress signaling in plants. In: Sarwat M et al (eds) Stress signaling in plants: genomics and proteomics perspective, vol 2. https://doi.org/10.1007/978-3-319-42183-4-11

  • Karabudak T, Bor M, Özdemir F, Türkan İ (2014) Glycine betaine protects tomato (Solanum lycopersicum) plants at low temperature by inducing fatty acid desaturase 7 and lipoxygenase gene expression. Mol Biol Rep 41:1401–1410

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  CAS  PubMed  Google Scholar 

  • Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants—gene regulatory mechanisms. Biochim Biophys Acta 1819:137–148

    Article  CAS  PubMed  Google Scholar 

  • Kidokoro S, Yoneda K, Takasaki H, Takahashi F, Shinozaki K, Yamaguchi-Shinozaki K (2017) Different cold-signaling pathways function in the responses to rapid and gradual decreases in temperature. Plant Cell 29 (4):760–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koc E, Islek C, Ustun AS (2010) Effect of cold on protein, proline, phenolic compounds and chlorophyll content of two pepper (Capsicum annuum L.) varieties. GU J Sci 23:1–6

    Google Scholar 

  • Król A, Amarowicz R, Weidner S (2015) The effects of cold stress on the phenolic compounds and antioxidant capacity of grapevine (Vitis vinifera L.) leaves. J Plant Physiol 189:97–104

    Article  PubMed  Google Scholar 

  • Lalrinzuali K, Vabeiryureilai M, Jagetia GC (2016) The analysis of antioxidant activity and phenolic contents of selected medicinal plants of Mizoram. Genom Appl Biol 28:6

    Google Scholar 

  • Lee E, Staebler M, Tollenaar M (2002) Genetic variation in physiological discriminators for cold tolerance-early autotrophic phase of maize development. Crop Sci 42:1919–1929

    Article  Google Scholar 

  • Leshem YY (1992) Plant membranes: a biophysical approach to structure, development and senescence. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stress—chilling, freezing and high temperature stresses, vol 1. Academic Press, New York

    Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Transact 603:591–592

    Article  Google Scholar 

  • Liu SQ, Chen CM, Chen GJ, Cao BH, Chen QH, Lei JJ (2012) RNA sequencing tag profiling of the placenta and pericarp of pungent pepper provides robust candidates contributing to capsaicinoid biosynthesis. Plant Cell Tissue Organ Cult 110:111–121

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔC(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu P, Sang WG, Ma KP (2008) Differential responses of the activities of antioxidant enzymes to thermal stresses between two invasive Eupatorium species in China. J Integr Plant Biol. https://doi.org/10.1111/j.1744-7909.2007.00583.x

    Google Scholar 

  • Malamy J (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77

    Article  CAS  PubMed  Google Scholar 

  • Martin RJ, Deo B (2000) Effect of plant population on calendula (Calendula officinalis L.) flower production. N Z J Crop Hortic Sci 28:37–44

    Article  Google Scholar 

  • Maysa M, Mallah E, Mohamed A (2015) Hepatoprotective effect of Calendula officinalis Linn (Asteraceae) flowers against CCl4-induced hepatotoxicity in rats. World Appl Sci J 33:949–1959

    Google Scholar 

  • Mc Neil SD, Rhodes D, Russell BL, Nuccio ML, Shachar-Hill Y, Andrew D, Hanson AD (2000) Metabolic model identifies key constraints on an engineered glycine betaine synthetic pathway in tobacco. Plant Physiol 12:153–162

    Article  Google Scholar 

  • Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115:875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu X, Xiong F, Liu J, Sui Y, Zeng Z, Lu BR, Liu Y (2014) Co-expression of ApGSMT and ApDMT promotes biosynthesis of glycine betaine in rice (Oryza sativa L.) and enhances salt and cold tolerance. Environ Exp Bot 104:16–25

    Article  CAS  Google Scholar 

  • Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150:1368–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker MR, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn AFM, Pronk A et al (2007) Specific root length as an indicator of environmental change. Plant Biosyst 141:426–442

    Article  Google Scholar 

  • Pan Y, Wu LJ, Yu ZL (2006) Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycorhiza uralensis Fisch). J Plant Growth Regul 49:157–165

    Article  CAS  Google Scholar 

  • Posmyk MM, Bailly C, Szafran´ska K, Jasan KM, Corbineau F (2005) Antioxidant enzymes and isoflavonoids in chilled soybean (Glycine max L. Merr.) seedlings. J Plant Physiol 162:403–412

    Article  CAS  PubMed  Google Scholar 

  • Presterl T, Ouzunova M, Schmidt W, Möller EM, Röber FK, Knaak C, Ernst K, Westhoff P, Geiger HH (2007) Quantitative trait loci for early plant vigour of maize grown in chilly environments. Theor Appl Genet 114:1059–1070

    Article  PubMed  Google Scholar 

  • Rahimi A, Jahanbin Sh, Salehi A, Farajee H (2016) Changes in content of chlorophyll, carotenoids, phosphorus and relative water content of medicinal plant of Borage (Borago officinalis L.) under the influence of mycorrhizal fungi and water stress. J Biol Sci 17:28–34

    Article  Google Scholar 

  • Raja V, Majeed U, Kang H, Andrabi KI, John R (2017) Abiotic stress: interplay between ROS, hormones and MAPKs. Environ Exp Bot 137:142–157

    Article  CAS  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genom 12:30–43

    Article  CAS  Google Scholar 

  • Shan T, Jin P, Zhang Y, Huang Y, Wang X, Zheng Y (2016) Exogenous glycine betaine treatment enhances chilling tolerance of peach fruit during cold storage. Postharvest Biol Technol 114:104–110

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543–584

    Article  CAS  Google Scholar 

  • Subba P, Barua P, Kumar R, Datta A, Soni KK, Chakraborty S, Chakraborty N (2013) Phosphoproteomic dynamics of chickpea (Cicer arietinum L.) reveals shared and distinct components of dehydration response. J Proteome Res 12:5025–5047

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

    Article  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Tahmasebi A, Pakniyat H (2015) Comparative analysis of some biochemical responses of winter and spring wheat cultivars under low temperature. Int J Agric Agric 7:14–22

    Google Scholar 

  • Trivedi D, Gill SS, Yadav S, Tuteja N (2013) Genome-wide analysis of glutathione reductase (GR) genes from rice and Arabidopsis. Plant Signal Behav 8:1

    Article  Google Scholar 

  • Tuteja N, Gill SS (2016) Abiotic stress response in plants. Wiley, New York

    Book  Google Scholar 

  • Wang L, Fan XW, Pan JL, Huang ZB, Li YZ (2015) Physiological characterization of maize tolerance to low dose of aluminum, highlighted by promoted leaf growth. Planta 242:1391–1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wijewardana C, Henry WB, Hock MW, Reddy KR (2016) Growth and physiological trait variation among corn hybrids for cold tolerance. Can J Plant Sci 96:639–656

    Article  CAS  Google Scholar 

  • Wu FZ, Wang BC, Yang CP (2014) Proteomic analysis of the cold stress response in the leaves of birch (Betula platyphylla Suk). Plant Omics J 7:195–204

    Google Scholar 

  • Xiong Y, Fei SZ (2006) Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.). Planta 224:878–888

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Gill R, Anjum NA (2014) Target osmoprotectants for abiotic stress tolerance in crop plants-glycine betaine and proline. In: Plant adaptation to environmental change: significance of amino acids and their derivatives, vol 10, pp 97–108

  • Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteom 3:484–496

    Article  Google Scholar 

  • Yue C, Cao H, Wang L et al (2015) Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. Plant Mol Biol 88:591–608

    Article  CAS  PubMed  Google Scholar 

  • Zhang HY, Jiang YN, He ZY, Ma M (2005) Cadmium accumulation and oxidative burst in garlic (Allium sativum). J Plant Physiol 162:977–984

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Zhao X, Wang W, Pan Y, Huang L, Liu X, Zong Y, Zhu L, Yang D, Fu B (2012) Comparative transcriptome profiling of chilling stress responsiveness in two contrasting rice genotypes. PLoS ONE 7:e43274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YP, E ZG, Jiang H, Wang L et al (2015) A comparative study of stress-related gene expression under single stress and intercross stress in rice. Genet Mol Res 14:3702–3717

    Article  CAS  PubMed  Google Scholar 

  • Zuther E, Juszczak I, Lee YP, Baier M, Hincha DK (2015) Time-dependent deacclimation after cold acclimation in Arabidopsis thaliana accessions. Sci Rep. https://doi.org/10.1038/srep12199

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Authors acknowledge the financial support by Department of Biotechnology (DBT) and Science and Engineering Research Board (SERB). NJ also acknowledges the grant by Department of Science and Technology (DST) under Women Scientist Scheme (WOS).

Author information

Authors and Affiliations

  1. University of Kashmir, Srinagar, India

    Nelofer Jan, Umer Majeed, Khurshid Iqbal Andrabi & Riffat John

Authors
  1. Nelofer Jan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Umer Majeed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Khurshid Iqbal Andrabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Riffat John
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Riffat John.

Additional information

Communicated by J. Gao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jan, N., Majeed, U., Andrabi, K.I. et al. Cold stress modulates osmolytes and antioxidant system in Calendula officinalis. Acta Physiol Plant 40, 73 (2018). https://doi.org/10.1007/s11738-018-2649-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-018-2649-0

Keywords

Search

Navigation