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CDPKs enhance Cd tolerance through intensifying H2S signal in Arabidopsis thaliana

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Abstract

Background and aims

Hydrogen sulfide (H2S) acting as the third gasotransmitter following NO and CO has important physiological functions in both animals and plants. In plants, H2S plays a critical role in alleviating toxicity of Cd stresses. It is well known that Calcium-Dependent Protein Kinases (CDPKs) can regulate cell recognition and signal transduction through reversible protein phosphorylation, but how CDPKs regulate H2S signal remains unclear.

Methods

The genetic and pharmacological method together with spectrophotometry and LC-MS/MS were used in this study.

Results

Our results indicated that Arabidopsis pretreated with H2S exhibited enhanced tolerance to Cd. After treatment by trifluoroperazine (TFP), the toxicity of Cd was exacerbated. Meanwhile, the activity of L-cysteine desulfhydrase (LCD) was reduced and the content of endogenous H2S decreased. In vitro experiments demonstrated that CDPK3 could raise LCD activity. Interestingly, expressions of Cd associated genes could not normally respond to Cd stress in cdpk3 whereas increased when this mutant was pretreated with H2S. S-sulfhydration results revealed that the content of glutathione persulfide (GSSH) was significantly lower in lcd and cdpk3 mutants. The results indicated that the decrease in GSSH content was mainly due to the reduction in H2S, which further caused the increased sensitivity to Cd.

Conclusions

CDPKs can enhance the tolerance to Cd in Arabidopsis through the way of intensifying H2S signal.

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References

  • Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aroca A, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a new post-translational modification in plant systems. Plant Physiol. doi:10.1104/pp. 15.00009

    PubMed  PubMed Central  Google Scholar 

  • Becana M, Aparicio-Tejo P, Irigoyen JJ, Sanchez-Diaz M (1986) Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of medicago sativa. Plant Physiol 82:1169–1171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605

    CAS  PubMed  Google Scholar 

  • Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5:663–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawood M, Cao F, Jahangir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209–210:121–128

    Article  PubMed  Google Scholar 

  • Dooley FD, Nair SP, Ward PD (2013) Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One 8, e62048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang H, Jing T, Liu Z, Zhang L, Jin Z, Pei Y (2014) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481

    Article  CAS  PubMed  Google Scholar 

  • Finkel T (2012) From sulfenylation to sulfhydration: what a thiolate needs to tolerate. Sci Signal 5:pe10

    Article  PubMed  Google Scholar 

  • Garcia-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201–202:66–73

    Article  PubMed  Google Scholar 

  • Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 57:715S–724S, discussion 724S-725S

    CAS  PubMed  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486

    Article  CAS  PubMed  Google Scholar 

  • Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46

    Article  CAS  PubMed  Google Scholar 

  • Krishnan N, Fu C, Pappin DJ, Tonks NK (2011) H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal 4:ra86

    Article  PubMed  PubMed Central  Google Scholar 

  • Krussel L, Junemann J, Wirtz M, Birke H, Thornton JD, Browning LW, Poschet G, Hell R, Balk J, Braun HP, Hildebrandt TM (2014) The mitochondrial sulfur dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 is required for amino acid catabolism during carbohydrate starvation and embryo development in Arabidopsis. Plant Physiol 165:92–104

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51:169–187

    Article  CAS  PubMed  Google Scholar 

  • Li L, Wang Y, Shen W (2012a) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Gong M, Xie H, Yang L, Li J (2012b) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L) suspension cultured cells and involvement of Ca(2+) and calmodulin. Plant Sci 185–186:185–189

    Article  PubMed  Google Scholar 

  • Li ZG, Ding XJ, Du PF (2013a) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013b) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564–1572

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36:1607–1616

    Article  CAS  PubMed  Google Scholar 

  • Lu C, Kavalier A, Lukyanov E, Gross SS (2013) S-sulfhydration/desulfhydration and S-nitrosylation/denitrosylation: a common paradigm for gasotransmitter signaling by H2S and NO. Methods 62:177–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol 4, e327

    Article  PubMed  PubMed Central  Google Scholar 

  • Munaron L, Avanzato D, Moccia F, Mancardi D (2013) Hydrogen sulfide as a regulator of calcium channels. Cell Calcium 53:77–84

    Article  CAS  PubMed  Google Scholar 

  • Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W, Gazi SK, Barrow RK, Yang G, Wang R, Snyder SH (2009) H2S signals through protein S-sulfhydration. Sci Signal 2:ra72

    PubMed  PubMed Central  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants - from the field to the test tube and back. Plant Biol (Stuttg) 9:582–588

    Article  CAS  Google Scholar 

  • Paul BD, Snyder SH (2012) H2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13:499–507

    Article  CAS  PubMed  Google Scholar 

  • Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548

    Article  CAS  PubMed  Google Scholar 

  • Qiao Z, Jing T, Liu Z, Zhang L, Jin Z, Liu D, Pei Y (2015) H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis. Plant Soil 393:137–146

    Article  CAS  Google Scholar 

  • Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005) Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. Febs J 272:1291–1304

    Article  CAS  PubMed  Google Scholar 

  • Romeroa LC, Ángeles Arocaa M, Sernab A, Gotora C (2013) Proteomic analysis of endogenous S-sulfhydration in Arabidopsis thaliana. Nitric Oxide 31:S23

    Article  Google Scholar 

  • Sambrook J, Manistis T (1987) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schaedle M (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sen N, Paul BD, Gadalla MM, Mustafa AK, Sen T, Xu R, Kim S, Snyder SH (2012) Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions. Mol Cell 45:13–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Ye T, Chan Z (2013) Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 71:226–234

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Ye T, Chan Z (2014a) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74C:99–107

    Article  Google Scholar 

  • Shi H, Ye T, Han N, Bian H, Liu X, Chan Z (2014b) Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J Integr Plant Biol 57:628–640

    Article  Google Scholar 

  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signal Behav 2:79–85

    Article  PubMed  PubMed Central  Google Scholar 

  • Vandiver MS, Paul BD, Xu R, Karuppagounder S, Rao F, Snowman AM, Ko HS, Lee YI, Dawson VL, Dawson TM, Sen N, Snyder SH (2013) Sulfhydration mediates neuroprotective actions of parkin. Nat Commun 4:1626

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Zhao K, Ju Y, Mani S, Cao Q, Puukila S, Khaper N, Wu L, Wang R (2013) Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal 18:1906–1919

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Ye Y, Wang S, Luo J, Tang J, Ma D (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250

    Article  CAS  Google Scholar 

  • Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567

    Article  CAS  PubMed  Google Scholar 

  • Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (31400237 to Zhuping Jin; 31372085 to Yanxi Pei and 31300236 to Zhiqiang Liu).

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Correspondence to Yanxi Pei.

Additional information

Responsible Editor: Juan Barcelo.

Zengjie Qiao and Tao Jing contributed equally to this work.

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Fig. S1

Expressions of LCD and CDPK3 induced by Cd. Total RNA was extracted from 14 day-old plants treated with CdCl2 for 0, 1, 3, 6, 12 and 24 h. The expression level of each gene was detected by RT-PCR, with ACTIN as an internal control. (JPEG 10 kb)

High resolution image (TIFF 156 kb)

Fig. S2

The expressions of ETHEI and STR1. The mRNAs were isolated from 14-day-old seedlings at 0, 1, 3, 6, 12, and 24 h of 100 μM Cd treatment. The expression level of each gene was detected by qRT-PCR. (JPEG 24 kb)

High resolution image (TIFF 934 kb)

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Qiao, Z., Jing, T., Jin, Z. et al. CDPKs enhance Cd tolerance through intensifying H2S signal in Arabidopsis thaliana . Plant Soil 398, 99–110 (2016). https://doi.org/10.1007/s11104-015-2643-x

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