Skip to main content
Log in

Endogenous hydrogen sulfide regulated by calcium is involved in thermotolerance in tobacco Nicotiana tabacum L. suspension cell cultures

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

Abstract

Calcium (Ca2+)/calmodulin (CaM), a core component of calcium messenger system, is a multiple second messenger that is involved in multiple stress tolerance including heat tolerance in plants, hydrogen sulfide (H2S) is fast emerging similar functions, but Ca2+ and H2S crosstalk in the acquisition of thermotolerance is not completely understood. In this article, Ca2+ and CaM activated the activity of cysteine desulfhydrase (L-DES), followed by inducing endogenous H2S accumulation in tobacco suspension cultured cells, while treatment with Ca2+ chelator ethylene glycol-bis(b-aminoethylether)-N,N,N′,N′-tetraacetic acid and CaM antagonists chlorpromazine lowered L-DES activity and H2S accumulation. Interestingly, Ca2+- and CaM-activated L-DES activity and endogenous H2S accumulation were eliminated by H2S synthesis inhibitors DL-propargylglycine (PAG), aminooxy acetic acid (AOA), potassium pyruvate (PP) and hydroxylamine (HA), and the H2S scavenger hypotaurine (HT), indicating that Ca2+ and CaM regulated endogenous H2S generation via activating L-DES activity in tobacco cells. Furthermore, H2S donor NaHS, Ca2+ and CaM treatment alone significantly improved the thermotolerance of tobacco cells, and heat tolerance induced by Ca2+ and CaM was enhanced by exogenous NaHS, while weakened by PAG, AOA, PP, HA or HT. All above-mentioned results suggest that endogenous H2S generated by L-DES was involved, at least partly, in the thermotolerance induced by Ca2+ and CaM in tobacco suspension cell cultures.

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AOA:

Aminooxy acetic acid

CaM:

Calmodulin

CPZ:

Chlorpromazine

CS:

Cysteine synthase

L-DES:

L-cysteine desulfhydrase

ECS:

Extracellular calcium stores

EGTA:

Ethylene glycol-bis(b-aminoethylether)-N,N,N′,N′-tetraacetic acid

HA:

Hydroxylamine

H2S:

Hydrogen sulfide

HT:

Hypotaurine

ICS:

Intracellular calcium stores

NaHS:

Sodium hydrosulfide

PAG:

DL-propargylglycine

PP:

Potassium pyruvate

References

  • Batistic O, Kim KN, Kleist T, Kudla J, Luan S (2011) The CBL–CIPK network for decoding calcium signals in plants. In: Luan S (ed) Coding and decoding of calcium signals in plants. Springer, Berlin, pp 235–258

    Chapter  Google Scholar 

  • Calderwood A, Kopriva S (2014) Hydrogen sulfide in plants: from dissipation of excess sulfur to signalling molecule. Nitric Oxide 41:72–78

    Article  CAS  PubMed  Google Scholar 

  • Christou A, Manganaris GA, Papadopoulos I, Fotopouls V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64:1953–1966

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Christou A, Filippou P, Manganaris GA, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 149:42

    Article  Google Scholar 

  • Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:4.1–4.28

    Article  Google Scholar 

  • Dubrovina AS, Kiselev KV, Khristenko VS (2013) Expression of calcium-dependent protein kinase (CDPK) genes under abiotic stress conditions in wild-growing grapevine Vitis amurensis. J Plant Physiol 170:1491–1500

    Article  CAS  PubMed  Google Scholar 

  • Fang T, Cao ZY, Li JL, Shen WB, Huang LQ (2014a) Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol Biochem 76:44–51

    Article  CAS  PubMed  Google Scholar 

  • Fang HH, Jing T, Liu ZQ, Zhang LP, Jin ZP, Pei YX (2014b) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481

    Article  CAS  PubMed  Google Scholar 

  • Fu PN, Wang WJ, Hou LX, Liu X (2013) Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Soc Bot Pol 82:295–302

    Article  CAS  Google Scholar 

  • García-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 

  • Gong M, Chen SN, Song YQ, Li ZG (1997) Effect of calcium and calmodulin on intrinsic heat tolerance in relation to antioxidant systems in maize seedlings. Aust J Plant Physiol 24:371–379

    Article  CAS  Google Scholar 

  • Gong M, van der Luit AH, Knight MR, Trewavas AJ (1998) Heat shock-induced changes of intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116:429–437

    Article  PubMed Central  CAS  Google Scholar 

  • Hancock JT, Whiteman M (2014) Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol Biochem 78:37–42

    Article  CAS  PubMed  Google Scholar 

  • Knight H (2000) Calcium signaling during abiotic stress in plants. Inter Rev Cytol 195:269–324

    Article  CAS  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kump LR, Pavlov A, Arthur MA (2005) Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia. Geology 33:397–400

    Article  CAS  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:628–695

    Article  Google Scholar 

  • Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269

    Article  CAS  PubMed  Google Scholar 

  • Lee SW, Hu YS, Hu LF, Lu Q, Dawe GS, Moore PK, Wong PTH, Bian JS (2006) Hydrogen sulphide regulates calcium homeostasis in microglial cells. Glia 54:116–124

    Article  PubMed  Google Scholar 

  • Li ZG (2013) Hydrogen sulfide: a multifunctional gaseous molecule in plants. Russ J Plant Physiol 60:733–740

    Article  CAS  Google Scholar 

  • Li ZG (2015a) Analysis of some enzymes activities of hydrogen sulfide metabolism in plants. Methods Enzymol 555:253–269

    Article  PubMed  Google Scholar 

  • Li ZG (2015b) Quantification of hydrogen sulfide concentration using methylene blue and 5,5′-dithiobis(2-nitrobenzoic acid) methods in Plants. Methods Enzymol 554:101–110

    Article  PubMed  Google Scholar 

  • Li ZG, Gong M (2009) Involvement of calcium and calmodulin in mechanical stimulation-induced heat tolerance in tobacco (Nicotiana Tabacum L.) suspension cultured cells. Plant Physiol J 45:363–366

    Google Scholar 

  • Li ZG, Zhu LP (2015) Hydrogen sulfide donor sodium hydrosulfide-induced accumulation of betaine is involved in the acquisition of heat tolerance in maize seedlings. Br J Bot 38:31–38

    Article  Google Scholar 

  • Li ZG, Du CK, Gong M (2005) Involvement of Ca2+ and calmodulin in the regulation of H2O2-induced heat tolerance in maize seedlings. J Plant Physiol Mol Biol 31:515–519

    CAS  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 ZG, Gong M, Liu P (2012a) 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 (2012b) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185(186):185–189

    Article  PubMed  Google Scholar 

  • Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013a) Hydrogen sulfide 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 

  • Li ZG, Ding XJ, Du PF (2013b) 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, Luo LJ, Zhu LP (2014a) Involvement of trehalose in hydrogen sulfide donor sodium hydrosulfide-induced the acquisition of heat tolerance in maize (Zea mays L.) seedlings. Bot Stud 55:20

    Article  Google Scholar 

  • Li ZG, Yi XY, Li YT (2014b) Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings. Biologia 69:1001–1009

    CAS  Google Scholar 

  • Li ZG, Xie LR, Li XJ (2015) Hydrogen sulfide acts as a downstream signal molecule in salicylic acid-induced heat tolerance in maize (Zea mays L.) seedlings. J Plant Physiol 177:121–127

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935

    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 

  • McAinsh RM, Pittman JK (2009) Shaping the calcium signature. N Phytol 181:275–294

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–479

    Article  CAS  Google Scholar 

  • Nagain Y, Tsugane M, Oka JI, Kimura H (2004) Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18:557–559

    Google Scholar 

  • Reddy ASN (2001) Calcium: silver bullet in signaling. Plant Sci 160:381–404

    Article  CAS  PubMed  Google Scholar 

  • Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:62010–62032

    Article  Google Scholar 

  • Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327

    Article  CAS  PubMed  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 (2014) 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 (2015) Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J Int Plant Biol 57:628–640

    Article  CAS  Google Scholar 

  • Takahashi Y, Ito T (2011) Structure and function of CDPK: a sensor responder of calcium. In: Luan S (ed) Coding and decoding of calcium signals in plants. Springer, Berlin, pp 129–146

    Chapter  Google Scholar 

  • Yang GD, Wu LY, Jiang B, Yang W, Qi JS, Cao K, Meng QH, Mustafa AK, Mu WD, Zhang SM, Snyder SH, Wang R (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase. Science 322:587–590

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang H, Hua SL, Zhang ZJ, Hua LY, Jiang CX, Wei ZJ, Liu L, Wang HL, Jiang ST (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharv Biol Technol 60:251–257

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by National Natural Science Foundation of China (31360057 to Zhong-Guang Li).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhong-Guang Li.

Additional information

Communicated by H. Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, ZG., Long, WB., Yang, SZ. et al. Endogenous hydrogen sulfide regulated by calcium is involved in thermotolerance in tobacco Nicotiana tabacum L. suspension cell cultures. Acta Physiol Plant 37, 219 (2015). https://doi.org/10.1007/s11738-015-1971-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-015-1971-z

Keywords

Navigation