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H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis

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Abstract

Background and aims

In plants, salicylic acid (SA) acting as one of the signaling molecules can regulate and respond to cadmium (Cd) stress. It is well known that hydrogen sulfide (H2S) could alleviate toxicity of Cd stress but the crosstalk between SA and H2S in regulating Cd stress still remains unclear.

Methods

We studied on it through the physiological and biochemical method together with the microstructure synthesis.

Results

Our results indicated that the plants exhibited enhanced tolerance to Cd when pretreated with SA, which included weakening oxidative damage and intensifying photosynthesis as well as boosting L-cysteine desulfhydrase (LCD) activity and raising the content of endogenous H2S. In parallel, the plants pretreated with NaHS, a donor of H2S, showed a stronger ability to tolerate Cd stress, SA- pretreated plants presented normal growth and meanwhile the content of chlorophyll and the microstructure of roots were significantly different compared to those treated with Cd only. By contrast, with the same treatments, the positive function and effect of SA on the LCD-knockout mutants, lcd was not observed. Pharmacological experiments further testified these results.

Conclusions

All of the results suggest that H2S may be a downstream signal molecule in SA-induced Cd tolerance of Arabidopsis.

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Abbreviations

AOA:

Aminooxyacetic acid

Cd:

Cadmium

LCD:

L-cysteine desulfhydrase

HA:

Hydroxylamine

H2S:

Hydrogen sulfide

HT:

Hypotaurine

MDA:

Malondialdehyde

ROS:

Reactive oxygen species

SA:

Salicylic acid

PP:

Potassium pyruvate

References

  • Agami RA, Mohamed GF (2013) Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicol Environ Saf 94:164–171

    Article  CAS  PubMed  Google Scholar 

  • 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 Central  PubMed  Google Scholar 

  • Burandt P, Schmidt A, Papenbrock J (2002) Three OAS-TL isoenzymes from Arabidopsis catalyze cysteine synthesis and cysteine desulfuration at different pH values. J Plant Physiol 159:111–119

    Article  CAS  Google Scholar 

  • Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1886

    Article  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 Central  PubMed  Google Scholar 

  • Cui W, Chen H, Zhu K, Jin Q, Xie Y, Cui J, Xia Y, Zhang J, Shen W (2014) Cadmium-induced hydrogen sulfide synthesis is involved in cadmium tolerance in Medicago sativa by reestablishment of reduced (Homo)glutathione and reactive oxygen species homeostases. PLoS One 9, e109669

    Article  PubMed Central  PubMed  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 Central  PubMed  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 

  • 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 

  • Hao L, Zhao Y, Jin D, Zhang L, Bi XH, Chen HX, Xu Q, Ma CY, Li GZ (2012) Salicylic acid-altering Arabidopsis mutants response to salt stress. Plant Soil 354:81–95

    Article  CAS  Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25

    Article  CAS  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 

  • Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931

    Article  CAS  PubMed  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 Z, Gong M, Liu P (2012b) Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha Curcas. Acta Physiol Plant 34:2207–2213

    Article  CAS  Google Scholar 

  • Li ZG, Gong M, Xie H, Yang L, Li J (2012c) 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 

  • Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281

    Article  CAS  PubMed Central  PubMed  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 

  • 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 

  • Sajitha Rajan S, Murugan K (2010) Purification and kinetic characterization of the liverwort Pallavicinia lyelli (Hook.) S. Gray. cytosolic ascorbate peroxidase. Plant Physiol Biochem 48:758–763

    Article  CAS  PubMed  Google Scholar 

  • Schutzendubel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127:887–898

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shalata A, Tal M (1998) The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol Plant 104:167–174

    Article  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 74:99–107

    Article  CAS  PubMed  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. doi:10.1111/jipb.12302

    Google Scholar 

  • Tao SY, Sun LH, Ma CY, Li LL, Li GZ, Hao L (2013) Reducing basal salicylic acid enhances Arabidopsis tolerance to lead or cadmium. Plant Soil 372:309–318

    Article  CAS  Google Scholar 

  • Taylor MD (1997) Accumulation of cadmium derived from fertilisers in New Zealand soils. Sci Total Environ 208:123–126

    Article  CAS  PubMed  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 

  • Wang C, Zhang S, Wang P, Hou J, Qian J, Ao Y, Lu J, Li L (2011) Salicylic acid involved in the regulation of nutrient elements uptake and oxidative stress in Vallisneria natans (Lour.) Hara under Pb stress. Chemosphere 84:136–142

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Chen W (2011) Role of salicylic acid in alleviating photochemical damage and autophagic cell death induction of cadmium stress in Arabidopsis thaliana. Photochem Photobiol Sci 10:947–955

    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 

Download references

Acknowledgments

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

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    Authors and Affiliations

    1. School of Life Science, Shanxi University, Taiyuan, 030006, China

      Zengjie Qiao, Zhiqiang Liu, Liping Zhang, Zhuping Jin, Danmei Liu & Yanxi Pei

    2. Department of chemistry and biochemistry, Ohio University, Athens, OH, 45701, USA

      Tao Jing

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    1. Zengjie Qiao
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    2. Tao Jing
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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

    LCD transcriptional level (a) and the content of H2S (b) in the WT, lcd and OE-LCD plants. lcd is a T-DNA inserted knockout mutant (SAIL_793_C08/CS835466). Its gene expression at the transcriptional level and the content of H2S are dramatically down regulated compared to WT. OE-LCD is an overexpression mutant. Its LCD expression and the content of H2S are sharply up regulated (GIF 3 kb)

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    Qiao, Z., Jing, T., Liu, Z. et al. H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis . Plant Soil 393, 137–146 (2015). https://doi.org/10.1007/s11104-015-2475-8

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