Skip to main content
Log in

Salicylic acid and cold priming induce late-spring freezing tolerance by maintaining cellular redox homeostasis and protecting photosynthetic apparatus in wheat

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

An increasing number of studies provide evidence that priming (pre-exposure of plants to moderate stress or chemical stimulus) can confer plant tolerance to a later occurring severe stress. The main objective of this study was to explore and compare the physiological mechanisms of salicylic acid (SA) and cold priming to enhance freezing tolerance. Wheat plants were firstly primed with SA (100 μM) or cold temperature (day/night temperature of 6 °C/2 °C), and then grown without any treatment for 8 days, and subsequently subjected to a freezing stress (day/night temperature of 2 °C/0 °C on the first day and − 2 °C/− 4 °C on the second day) at the jointing stage. The results showed that primed plants up-regulated the expression level of WRKY gene (WRKY19), heat shock transcription factor (HSF3), mitochondrial alternative oxidase (AOX1a), and heat shock protein (HSP70) under freezing stress, which contribute to increase of antioxidant capacity and protection of photosystem in parallel with lower malonaldehyde content, superoxide radical production and higher photochemistry efficiency of photosystem II under freezing stress as compared with non-primed plants. Furthermore, primed plants had a better photosynthesis performance and higher biomass production during the recovery period, and higher grain yield at maturity as compared with non-primed plants. Collectively, these results indicated that SA and cold priming effectively upregulated the expression of cold-responsive genes under freezing stress, resulting in increased antioxidant activity and cyanide-resistant respiration capacity and molecular chaperones level, maintaining cellular redox homeostasis and protecting photosynthetic apparatus, thereby conferring tolerance to freezing stress in wheat plants.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aravind P, Prasad MNV (2005) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate–glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43:107–116

    Article  CAS  PubMed  Google Scholar 

  • Arfan M, Athar HR, Ashraf M (2007) Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? J Plant Physiol 164:685–694

    Article  CAS  PubMed  Google Scholar 

  • Bidinger F, Musgrave RB, Fischer RA (1977) Contribution of stored pre-anthesis assimilate to grain yield in wheat and barley. Nature 270:431–433

    Article  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 

  • Buer JV, Cvetkovic J, Baier M (2016) Cold regulation of plastid ascorbate peroxidases serves as a priming hub controlling ROS signaling in Arabidopsis thaliana. BMC Plant Biol 16:1–20

    Article  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  PubMed  Google Scholar 

  • Ding ZS, Tian SP, Zheng XL, Zhou ZW, Xu Y (2007) Responses of reactive oxygen metabolism and quality in mango fruit to exogenous oxalic acid or salicylic acid under chilling temperature stress. Physiol Plant 130:112–121

    Article  CAS  Google Scholar 

  • Dinler BS, Antoniou C, Fotopoulos V (2014) Interplay between GST and nitric oxide in the early response of soybean (Glycine max L.) plants to salinity stress. J Plant Physiol 171:1740–1747

    Article  CAS  PubMed  Google Scholar 

  • Dong CJ, Li L, Shang QM, Liu XY, Zhang ZG (2014) Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings. Planta 240:687–700

    Article  CAS  PubMed  Google Scholar 

  • Duan YH, Guo J, Ding K, Wang SJ, Zhang H, Dai XW, Chen YY, Govers F, Huang LL, Kang ZS (2011) Characterization of a wheat HSP70 gene and its expression in response to stripe rust infection and abiotic stresses. Mol Biol Rep 38:301–307

    Article  CAS  PubMed  Google Scholar 

  • Ehlert B, Hincha DK (2008) Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves. Plant Methods 4:1–7

    Article  CAS  Google Scholar 

  • Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756

    Article  CAS  PubMed  Google Scholar 

  • Ganeshan S, Vitamvas P, Fowler DB, Chibbar RN (2008) Quantitative expression analysis of selected COR genes reveals their differential expression in leaf and crown tissues of wheat (Triticum aestivum L.) during an extended low temperature acclimation regimen. J Exp Bot 59:2393–2402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grabelnych OI, Pobezhimova TP, Korzun AM, Voznenko SA (2011) The participation of cyanide-resistant respiration in heat generation and antioxidative defense of cell in winter wheat shoots under cold influence. J Stress Physiol Biochem 42:300–306

    Google Scholar 

  • Hahn A, Bublak D, Schleiff E, Scharf K-D (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23:741–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han QX, Kang GZ, Guo TC (2013) Proteomic analysis of spring freeze-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.). Plant Physiol Biochem 63:236–244

    Article  CAS  PubMed  Google Scholar 

  • Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biochem 42:657–662

    Article  CAS  PubMed  Google Scholar 

  • Herman EM, Rotter K, Premakumar R, Elwinger G, Bae R, Ehler-King L, Chen S, Livingston DP, Bae H (2006) Additional freeze hardiness in wheat acquired by exposure to −3 °C is associated with extensive physiological, morphological, and molecular changes. J Exp Bot 57:3601–3618

    Article  CAS  PubMed  Google Scholar 

  • Hilker M, Schwachtje J, Baier M, Balazadeh S, Bäurle I, Geiselhardt S, Hincha DK, Kunze R, Mueller-Roeber B, Rillig MC (2015) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev 1:393–406

    Google Scholar 

  • Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hu WH, Yan XH, Yu JQ (2016) Importance of the mitochondrial alternative oxidase (AOX) pathway in alleviating photoinhibition in cucumber leaves under chilling injury and subsequent recovery when leaves are subjected to high light intensity. J Hortic Sci Biotechnol 92:31–38

    Article  CAS  Google Scholar 

  • Janda T, Szalai G, Lesko KL, Yordanova R, Apostol S, Popova LP (2007) Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. Phytochemistry 68:1674–1682

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang JH (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  CAS  PubMed  Google Scholar 

  • Kovacs V, Gondor OK, Szalai G, Eva Darko IM, Janda T, Pál M (2014) Synthesis and role of salicylic acid in wheat varieties with different levels of cadmium tolerance. J Hazard Mater 280:12–19

    Article  CAS  PubMed  Google Scholar 

  • Lee B, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA, Fryer M (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138:451–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei T, Feng H, Sun X, Dai QL, Zhang F, Liang HG, Lin H-H (2010) The alternative pathway in cucumber seedlings under low temperature stress was enhanced by salicylic acid. Plant Growth Regul 60:35–42

    Article  CAS  Google Scholar 

  • Li CY, Jiang D, Wollenweber B, Li Y, Dai TB, Cao WX (2011) Waterlogging pretreatment during vegetative growth improves tolerance to waterlogging after anthesis in wheat. Plant Sci 180:672–678

    Article  CAS  PubMed  Google Scholar 

  • Li XN, Cai J, Liu FL, Dai TB, Cao WX, Jiang D (2014) Cold priming drives the sub-cellular antioxidant systems to protect photosynthetic electron transport against subsequent low temperature stress in winter wheat. Plant Physiol Biochem 82:34–43

    Article  CAS  PubMed  Google Scholar 

  • Li XN, Pu HC, Liu FL, Zhou Q, Cai J, Dai TB, Cao WX, Jiang D (2015) Winter wheat photosynthesis and grain yield responses to spring freeze. Agrono J 107:1002–1010

    Article  Google Scholar 

  • Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CM, Pozo MJ, Ton J, Dam NM, Conrath U (2016) Recognizing plant defense priming. Trends Plant Sci 21:818–822

    Article  CAS  PubMed  Google Scholar 

  • Min K, Showman L, Perera A, Arora R (2018) Salicylic acid-induced freezing tolerance in spinach (Spinacia oleracea L.) leaves explored through metabolite profiling. Environ Exp Bot 156:214–227

    Article  CAS  Google Scholar 

  • Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:1

    Article  Google Scholar 

  • Niu CF, Wei W, Zhou QY, Tian AG, Hao YJ, Zhang WK, Biao MA, Lin Q, Zhang ZB, Zhang JS (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Environ 35:1156–1170

    Article  CAS  PubMed  Google Scholar 

  • Öquist G (1983) Effects of low temperature on photosynthesis. Plant Cell Environ 6:281–300

    Google Scholar 

  • Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2013) Primed plants do not forget. Environ Exp Bot 94:46–56

    Article  CAS  Google Scholar 

  • Patra HK, Kar M, Mishra D (1978) Catalase activity in leaves and cotyledons during plant development and senescence. Biochem Physiol Pflanz 172:385–390

    Article  CAS  Google Scholar 

  • Rhoads DM, Mclntosh L (1992) Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell 4:1131–1139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruellan E, Vaultier M, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150

    Article  CAS  Google Scholar 

  • Sanmartin M, Drogoudi PD, Lyons T, Pateraki I, Barnes J, Kanellis AK (2003) Over-expression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216:918–928

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Ding Y, Yang S (2018) Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci 23:623–637

    Article  CAS  PubMed  Google Scholar 

  • Shin H, Min K, Arora R (2018) Exogenous salicylic acid improves freezing tolerance of spinach (Spinacia oleracea L.) leaves. Cryobiology 81:192–200

    Article  CAS  PubMed  Google Scholar 

  • Sugie A, Naydenov N, Mizuno N, Nakamura C, Takumi AS (2006) Overexpression of wheat alternative oxidase gene Waox1a alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes Genet Syst 81:349–354

    Article  CAS  PubMed  Google Scholar 

  • Sun LY, Li XN, Wang ZS, Sun ZW, Zhu XC, Liu SQ, Song FB, Liu FL, Wang YJ (2018) Cold priming induced tolerance to subsequent low temperature stress is enhanced by melatonin application during recovery in wheat. Molecules 23:1091

    Article  PubMed Central  CAS  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 

  • Tasgin E, Atici O, Nalbantoglu B (2003) Effects of salicylic acid and cold on freezing tolerance in winter wheat leaves. Plant Growth Regul 41:231–236

    Article  CAS  Google Scholar 

  • Tsvetanov S, Ohno R, Tsuda K, Takumi S, Mori N, Atanassov A, Nakamura C (2000) A cold-responsive wheat (Triticum aestivum L.) gene wcor14 identified in a winter-hardy cultivar ‘Mironovska 808’. Genes Genet Syst 75:49–57

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Cai J, Liu FL, Dai TB, Cao WX, Wollenweber B, Jiang D (2014) Multiple heat priming enhances thermo-tolerance to a later high temperature stress via improving subcellular antioxidant activities in wheat seedlings. Plant Physiol Biochem 74:185–192

    Article  CAS  PubMed  Google Scholar 

  • Wang WL, Wang X, Huang M, Cai J, Zhou Q et al (2018a) Hydrogen peroxide and abscisic acid mediate salicylic acid-induced freezing tolerance in wheat. Front Plant Sci 9:1137

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, Zhang XX, Chen J, Cai J, Zhou Q, Dai TB, Cao WX, Jiang D (2018b) Parental drought-priming enhances tolerance to post-anthesis drought in offspring of wheat. Front Plant Sci 9:261

    Article  PubMed  PubMed Central  Google Scholar 

  • Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771

    Article  CAS  PubMed  Google Scholar 

  • Wisniewski M, Webb R, Balsamo R, Close TJ, Yu XM, Griffith M (2010) Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol Plant 105:600–608

    Article  Google Scholar 

  • Xia XJ, Wang YJ, Zhou YH, Yuan T, Mao WH, Shi K, Asami T, Chen ZX, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Z, Zhang ZL, Hanzlik S, Cook E, Shen QJ (2007) Salicylic acid inhibits gibberellin-induced alpha-amylase expression and seed germination via a pathway involving an abscisic-acid-inducible WRKYgene. Plant Mol Biol 64:293–303

    Article  CAS  PubMed  Google Scholar 

  • Xie Q, Mayes S, Sparkes DL (2016) Preanthesis biomass accumulation of plant and plant organs defines yield components in wheat. Eur J Agron 81:15–26

    Article  Google Scholar 

  • 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 5:484–496

    Article  CAS  Google Scholar 

  • Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Yamane H, Shimono M, Sugano S, Takatsuji H (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64:5085–5097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang LT, Zhang ZS, Gao HY, Meng XL, Yang C, Liu JG, Meng QW (2012) The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biol 12:40

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang J, Shi Y, Zhang XZ, Dub HM, Xu B, Huang BR (2017) Melatonin suppression of heat-induced leaf senescence involves changes in abscisic acid and cytokinin biosynthesis and signaling pathways in perennial ryegrass (Lolium perenne L.). Environ Exp Bot 138:36–45

    Article  CAS  Google Scholar 

  • Zhong X, Mei X, Li Y, Yoshida H, Zhao P, Wang X, Han L, Hu X, Huang S, Huang J (2008) Changes in frost resistance of wheat young ears with development during jointing stage. J Agron Crop Sci 194:343–349

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Key Research and Development Program of China (2016YFD0300107), the National Natural Science Foundation of China (31401326, 31325020, and 31771693), the China Agriculture Research System (CARS-03), Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP), and Postgraduate Research & Practice Innovation Program of Jiangsu Province. We also thank Prof. Shui-zhang Fei (Iowa State University, USA) for providing language help.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xiao Wang or Dong Jiang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 120 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, W., Wang, X., Zhang, J. et al. Salicylic acid and cold priming induce late-spring freezing tolerance by maintaining cellular redox homeostasis and protecting photosynthetic apparatus in wheat. Plant Growth Regul 90, 109–121 (2020). https://doi.org/10.1007/s10725-019-00553-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-019-00553-8

Keywords

Navigation