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Sulfur dioxide improves drought tolerance through activating Ca2+ signaling pathways in wheat seedlings

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Abstract

Sulfur dioxide (SO2) and drought are two important co-occurring abiotic stresses affecting the growth and productivity of plants. Here, we will investigate the role of Ca2+ in regulating antioxidant defense during drought or SO2/drought stress, and the effect of SO2 pretreatment on the physiological response of wheat seedlings to drought stress. The results showed that exogenous Ca2+ increased the activities of SOD, CAT and POD, and reduced the contents of H2O2 and MDA in drought-treated wheat seedlings, suggesting Ca2+ could improve drought tolerance by promoting antioxidant defense in plants. Moreover, exogenous Ca2+ up-regulated the expression of two stress-responsive transcription factor (TF) genes, ERF1 and MYB30, to cope with drought stress. Exposure of wheat seedlings to 10 mg m−3 SO2 significantly enhanced the activities of SOD, CAT and POD. The contents of H2O2 and MDA remained at control levels, showing that SO2 at this concentration led to an activation of the antioxidant defense system and did not cause oxidative damage to the seedlings. Furthermore, 10 mg m−3 SO2 pretreatment increased the expression of CCaMK and CPK10, enhanced the activities of SOD and POD, and reduced the accumulation of H2O2 and MDA in drought-treated wheat seedlings, showing a role of SO2 in protection of plants against drought stress. However, with removal of Ca2+ by spraying EGTA on the SO2-pretreated wheat seedlings, the expression of transcription factor genes and activities of antioxidant enzymes were decreased, and the contents of H2O2 and MDA enhanced to the level of drought treatment alone, suggesting a role of Ca2+ in the SO2-induced alleviation of drought stress. Together, these results indicated that exogenous Ca2+ increased defense-related gene expression and enzyme activity in response to drought stress, and that pre-exposure to appropriate levels of SO2 could improve drought tolerance through activation of Ca2+ signaling pathways in plants. This study would provide new strategy for enhancing plant resistance to environmental stress.

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References

  • Ahmad P, Abd Allah EF, Alyemeni MN, Wijaya L, Alam P, Bhardwaj R, Siddique KHM (2018) Exogenous application of calcium to 24-epibrassinosteroid pre-treated tomato seedlings mitigates NaCl toxicity by modifying ascorbate–glutathione cycle and secondary metabolites. Sci Rep 8:13515

    Article  CAS  Google Scholar 

  • Anwar K, Joshi R, Dhankher OP, Singla-Pareek SL, Pareek A (2021) Elucidating the response of crop plants towards individual, combined and sequentially occurring abiotic stresses. Int J Mol Sci 22:6119

    Article  CAS  Google Scholar 

  • Appalasamy M, Varghese B, Ismail R, Sershen (2017) Responses of Trichilia dregeana leaves to sulphur dioxide pollution: a comparison of morphological, physiological and biochemical biomarkers. Atmos Pollut Res 8:729–740

    Article  Google Scholar 

  • Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes 10:771

    Article  CAS  Google Scholar 

  • Chen Z, Ma Y, Yang R, Gu Z, Wang P (2019) Effects of exogenous Ca2+ on phenolic accumulation and physiological changes in germinated wheat (Triticum aestivum L.) under UV-B radiation. Food Chem 288:368–376

    Article  CAS  Google Scholar 

  • Cheng L, Han M, Yang LM, Yang L, Sun Z, Zhang T (2018) Changes in the physiological characteristics and baicalin biosynthesis metabolism of Scutellaria baicalensis Georgi under drought stress. Ind Crop. Prod 122:473–482

    CAS  Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    Article  CAS  Google Scholar 

  • Dudziak K, Sozoniuk M, Szczerba H, Kuzdralinski A, Kowalczyk K, Borner A, Nowak M (2020) Identification of stable reference genes for qPCR studies in common wheat (Triticum aestivum L.) seedlings under short-term drought stress. Plant Methods 16:58

    Article  CAS  Google Scholar 

  • Han Y, Yang H, Wu M, Yi H (2019) Enhanced drought tolerance of foxtail millet seedlings by sulfur dioxide fumigation. Ecotoxicol Environ Saf 178:9–16

    Article  CAS  Google Scholar 

  • Han Y, Yin Y, Yi H (2020) Decreased endogenous nitric oxide contributes to sulfur dioxide derivative-alleviated cadmium toxicity in foxtail millet roots. Environ Exp Bot 177:104144

    Article  CAS  Google Scholar 

  • Hofstra G, Beckerson DW (1981) Foliar responses of five plant species to ozone and a sulphur dioxide/ozone mixture after a sulphur dioxide pre-exposure. Atmos Environ 15:383–389.

    Article  CAS  Google Scholar 

  • Hu KD, Bai GS, Li WJ, Yan H, Hu LY, Li YH, Zhang H (2014) Sulfur dioxide promotes germination and plays an antioxidant role in cadmium-stressed wheat seeds. Plant Growth Regul 75:271–280

    Article  CAS  Google Scholar 

  • Iyer NJ, Tang Y, Mahalingam R (2013) Physiological, biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula. Plant Cell Environ 36:706–720

    Article  CAS  Google Scholar 

  • Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029

    Article  Google Scholar 

  • Khan A, Anwar Y, Hasan MM, Iqbal A, Ali M, Alharby HF, Hakeem KR, Hasanuzzaman M (2017) Attenuation of drought stress in Brassica seedlings with exogenous application of Ca2+ and H2O2. Plants 6:20

    Article  CAS  Google Scholar 

  • Khan MN, Siddiqui MH, AlSolami MA, Alamri S, Hu Y, Ali HM, Al-Amri AA, Alsubaie QD, Al-Munqedhi BM, Al-Ghamdi A (2020) Crosstalk of hydrogen sulfide and nitric oxide requires calcium to mitigate impaired photosynthesis under cadmium stress by activating defense mechanisms in Vigna radiata. Plant Physiol Biochem 156:278–290

    Article  CAS  Google Scholar 

  • Li L, Yi H (2012) Differential expression of Arabidopsis defense-related genes in response to sulfur dioxide. Chemosphere 87:718–724

    Article  CAS  Google Scholar 

  • Liu Y, Li Y, Li L, Zhu Y, Liu J, Li G, Hao L (2017) Attenuation of sulfur dioxide damage to wheat seedlings by co-exposure to nitric oxide. B Environ Contam Tox 99:1–6

    Article  CAS  Google Scholar 

  • Lucas PW (1990) The effects of prior exposure to sulphur dioxide and nitrogen dioxide on the water relations of timothy grass (Phleum pratense) under drought conditions. Environ Pollut 66:117–138

    Article  CAS  Google Scholar 

  • Martins V, Soares C, Spormann S, Fidalgo F, Gerós H (2021) Vineyard calcium sprays reduce the damage of postharvest grape berries by stimulating enzymatic antioxidant activity and pathogen defense genes, despite inhibiting phenolic synthesis. Plant Physiol Bioch 162:48–55

    Article  CAS  Google Scholar 

  • Mulaudzi T, Hendricks K, Mabiya T, Muthevhuli M, Ajayi RF, Mayedwa N, Gehring C, Iwuoha E (2020) Calcium improves germination and growth of Sorghum bicolor seedlings under salt stress. Plants 9:730

    Article  CAS  Google Scholar 

  • Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci USA 104:4730–4735

    Article  CAS  Google Scholar 

  • Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016) Calcium supplementation improves Na+/K+ ratio, antioxidant defense and glyoxalase systems in salt-stressed rice seedlings. Front Plant Sci 7:609

    Article  Google Scholar 

  • Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032

    Article  CAS  Google Scholar 

  • Roy PR, Tahjib-Ul-Arif M, Polash MAS, Hossen MZ, Hossain MA (2019) Physiological mechanisms of exogenous calcium on alleviating salinity-induced stress in rice (Oryza sativa L.). Physiol Mol Biol Plants 25:611–624

    Article  CAS  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Sakran AM, Basalah MO, Ali HM (2012) Effect of calcium and potassium on antioxidant system of Vicia faba L. under cadmium stress. Int J Mol Sci 13:6604–6619

    Article  CAS  Google Scholar 

  • Siddiqui MH, Alamri S, Nasir Khan M, Corpas FJ, Al-Amri AA, Alsubaie QD, Ali HM, Kalaji HM, Ahmad P (2020) Melatonin and calcium function synergistically to promote the resilience through ROS metabolism under arsenic-induced stress. J Hazard Mater 398:122882

    Article  CAS  Google Scholar 

  • Singh PK, Srivastava D, Tiwari P, Tiwari M, Verma G, Chakrabarty D (2019) Drought tolerance in plants: molecular mechanism and regulation of signaling molecules. In: Plant Signaling Molecules. Woodhead Publishing,105–123

  • Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43

    Article  Google Scholar 

  • Wang D, Chen Q, Chen W, Guo Q, Xia Y, Wang S, Jing D, Liang G (2021) Physiological and transcription analyses reveal the regulatory mechanism of melatonin in inducing drought resistance in loquat (Eriobotrya japonica Lindl.) seedlings. Environ Exp Bot 181:104291

    Article  CAS  Google Scholar 

  • Wang SS, Zhang YX, Yang F, Huang ZQ, Tang J, Hu KD, Zhang H (2017) Sulfur dioxide alleviates programmed cell death in barley aleurone by acting as an antioxidant. PLoS ONE 12:e0188289

    Article  CAS  Google Scholar 

  • Wei W, Liang D, Bian X, Shen M, Xiao J, Zhang W, Ma B, Lin Q, Lv J, Chen X, Chen S, Zhang J (2019) GmWRKY54 improves drought tolerance through activating genes in abscisic acid and Ca2+ signaling pathways in transgenic soybean. Plant J 100:384–398

    Article  CAS  Google Scholar 

  • Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC, Zhao YX, Lu Y, Ni ZY, Liu L, Qiu ZG, Ma YZ (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732

    Article  CAS  Google Scholar 

  • Yoo JH, Park CY, Kim JC, Heo WD, Cheong MS, Park HC, Kim MC, Moon BC, Choi MS, Kang YH, Lee JH, Kim HS, Lee SM, Yoon HW, Lim CO, Yun DJ, Lee SY, Chung WS, Cho MJ (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J Biol Chem 280:3697–3706

    Article  CAS  Google Scholar 

  • Zandalinas SI, Fritschi FB, Mittler R (2020) Signal transduction networks during stress combination. J Exp Bot 71:1734–1741

    Article  CAS  Google Scholar 

  • Zandalinas SI, Fritschi FB, Mittler R (2021a) Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends Plant Sci 26:588–599

    Article  CAS  Google Scholar 

  • Zandalinas SI, Sengupta S, Fritschi FB, Azad RK, Nechushtai R, Mittler R (2021b) The impact of multifactorial stress combination on plant growth and survival. New Phytol 230:1034–1048

    Article  CAS  Google Scholar 

  • Zhang H, Sonnewald U (2017) Differences and commonalities of plant responses to single and combined stresses. Plant J 90:839–855

    Article  CAS  Google Scholar 

  • Zhang L, Zhao G, Xia C, Jia J, Liu X, Kong X (2012) A wheat R2R3-MYB gene, TaMYB30-B, improves drought stress tolerance in transgenic Arabidopsis. J Exp Bot 63:5873–5885

    Article  CAS  Google Scholar 

  • Zhang X, Lei L, Lai J, Song W (2018) Effects of drought stress and water recovery on physiological responses and gene expression in maize seedlings. BMC Plant Biol 18:68

    Article  CAS  Google Scholar 

  • Zhu DB, Hu KD, Guo XK, Liu Y, Hu LY, Li YH, Wang SH, Zhang H (2015) Sulfur dioxide enhances endogenous hydrogen sulfide accumulation and alleviates oxidative stress induced by aluminum stress in germinating wheat seeds. Oxid Med Cell Longev 2015:612363

    Article  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  Google Scholar 

Download references

Funding

This research was supported by the Natural Science Foundation of Shanxi Province (201901D111301); Doctoral Startup and Research Fund of Jinzhong University (1000107); and Program for “1331 Project” Maker Team of Jinzhong University (Jzxycktd2019031).

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LL conceived and designed the experiments, and wrote the paper. HL and LW performed the experiments and analyzed the data. HQ conceived of the experiments and led the study design. All authors read and approved the final manuscript.

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Correspondence to Hongxue Qi.

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Li, L., Li, H., Wu, L. et al. Sulfur dioxide improves drought tolerance through activating Ca2+ signaling pathways in wheat seedlings. Ecotoxicology 31, 852–859 (2022). https://doi.org/10.1007/s10646-022-02547-1

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