Skip to main content
Log in

Hydrogen sulfide partly mediates abscisic acid-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Abscisic acid (ABA), a plant hormone, plays crucial roles in plant growth, development and response to environmental stress. Recently, hydrogen sulfide (H2S) also has emerged similar functions, but interaction between ABA and H2S in the acquisition of heat tolerance is not clear. In this study, pretreatment of tobacco suspension cultured cells with ABA improved the survival percentage and regrowth ability, alleviated a decrease in cell vitality, increase in malondialdehyde content and electrolyte leakage of cells under heat stress, suggesting that ABA pretreatment could improve the heat tolerance of tobacco cells. In addition, treatment with ABA induced the accumulation of endogenous H2S in both tobacco cells and culture medium, increased the activity of l-cysteine desulfhydrase, a key enzyme in H2S biosynthesis. Also, ABA-induced heat tolerance was enhanced by addition of NaHS, a H2S donor, but weakened by dl-propargylglycine (specific inhibitor of H2S biosynthesis) and hypotaurine (H2S scavenger) respectively. These results suggest that ABA pretreatment could improve the heat tolerance of tobacco suspension cultured cells, and H2S, at least partly, mediated the acquisition of heat tolerance induced by ABA.

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

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abbreviations

ABA:

Abscisic acid

APX:

Ascorbate peroxidase

ASC:

Ascorbic acid

CAT:

Catalase

FW:

Fresh weight

GR:

Glutathione reductase

GSH:

Glutathione

H2S:

Hydrogen sulfide

HT:

Hypotaurine

LCD:

l-Cysteine desulfhydrase

MDA:

Malondialdehyde

NO:

Nitric oxide

PAG:

dl-Propargylglycine

POD:

Guaiacol peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TTC:

Triphenyl tetrazolium chloride

References

  • Bruňáková K, Petijová L, Zámečník J, Turečková V, Čellárová E (2015) The role of ABA in the freezing injury avoidance in two Hypericum species differing in frost tolerance and potential to synthesize hypericins. Plant Cell, Tissue Organ Cult 122:45–56

    Article  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 

  • Chen J, Wang WH, Wu FH, You CY, Liu WT, Dong XK, He JX, Zheng H (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318

    Article  CAS  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  CAS  PubMed  PubMed Central  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 14:42

    Article  PubMed  PubMed Central  Google Scholar 

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

    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, Li YJ, Chen SZ (1998) Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. J Plant Physiol 153:488–496

    Article  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 

  • Ishikawa M, Robertson AJ, Gusta LV (1995) Comparison of viability tests for assessing cross-adaptation to freezing, heat and salt stresses induced by abscisic acid in bromegrass (Bromus inermis Leyss) suspension cultured cells. Plant Sci 107:83–93

    Article  CAS  Google Scholar 

  • Kumar S, Kausha N, Nayyar H, Gaur P (2012) Abscisic acid induces heat tolerance in chickpea (Cicer arietinum L.) seedlings by facilitated accumulation of osmoprotectants. Acta Physiol Plant 34:1651–1658

    Article  CAS  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, 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  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 H, Liu SS, Yi CY, Wang F, Zhou J, Xia XJ, Shi K, Zhou YH, Yu JQ (2014c) Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants. Plant, Cell Environ 37:2768–2780

    Article  CAS  Google Scholar 

  • Li ZG, Long WB, Yang SZ, Wang YC, Tang JH, Chen T (2015a) Involvement of sulfhydryl compounds and antioxidant enzymes in H2S-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension-cultured cells. In Vitro Cell Dev Biol Plant 51:428–437

    Article  CAS  Google Scholar 

  • Li ZG, Long WB, Yang SZ, Wang YC, Tang JH, Wen L, Zhu BY, Min X (2015b) Endogenous hydrogen sulfide regulated by calcium is involved in thermotolerance in tobacco Nicotiana tabacum L. suspension cell cultures. Acta Physiol Plant 37:219

    Article  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  Google Scholar 

  • Pei ZM, Murata N, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  Google Scholar 

  • Robertson AJ, Ishikawa M, Gusta LV, MacKenzie SL (1994) Abscisic acid-induced heat tolerance in Bromus inermis Leyss cell-suspension cultures: heat-stable, abscisic acid-responsive polypeptides in combination with sucrose confer enhanced thermostability. Plant Physiol 105:181–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rock CD, Sakata Y, Quatrano RSA (2010) Stress signaling I: The role of abscisic acid (ABA). In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Springer, New York, pp 33–73

    Google Scholar 

  • Saeed B, Das M, Khurana P (2015) Overexpression of β-carotene hydroxylase1 (BCH1) in Indian mulberry, Morus indica cv. K2, confers tolerance against UV, high temperature and high irradiance stress induced oxidative damage. Plant Cell, Tissue Organ Cult 120:1003–1014

    Article  CAS  Google Scholar 

  • Song L, Ding W, Shen J, Zhang Z, Bi Y, Zhang L (2008) Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress. Plant Sci 175:826–832

    Article  CAS  Google Scholar 

  • Vidhyasekaran P (ed) (2015) Plant hormone signaling systems. In: Plant innate immunity. Springer, New York

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  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 J, Chen J, Pan K (2013) Effect of exogenous abscisic acid on the level of antioxidants in Atractylodes macrocephala Koidz under lead stress. Environ Sci Pollut Res 20:1441–1449

    Article  CAS  Google Scholar 

  • Wang L, Ma X, Che Y, Hou L, Liu X, Zhang W (2015) Extracellular ATP mediates H2S-regulated stomatal movements and guard cell K+ current in a H2O2-dependent manner in Arabidopsis. Sci Bull 60:419–427

    Article  CAS  Google Scholar 

  • Wu DH, Li YL, Xia X, Pu ZP, Liao JM, Huang K, Li ZG (2013) Hydrogen sulfide donor sodium hydrosulfide pretreatment improved multiple resistance abilities of wheat to high temperature and drought stress. J Yunnan Norm Univ 33:29–35

    Google Scholar 

  • Zhang DP (2014) Abscisic acid: Metabolism, transport and signaling. Springer, Dordrecht

    Google Scholar 

  • Zhang H, Hua SL, Zhang ZJ, Hua LY, Jiang CX, Wei ZJ, Liu J, 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 

  • Zheng YL, Li WQ, Sun WB (2015) Effects of acclimation and pretreatment with abscisic acid or salicylic acid on tolerance of Trigonobalanus doichangensis to extreme temperatures. Biol Plant 59:382–388

    Article  CAS  Google Scholar 

  • Zhou L, Wang N, Kong L, Gong S, Li Y, Li X (2014) Molecular characterization of 26 cotton WRKY genes that are expressed differentially in tissues and are induced in seedlings under high salinity and osmotic stress. Plant Cell, Tissue Organ Cult 119:141–156

    Article  CAS  Google Scholar 

  • Zhu L, Wang W, Shi J, Zhang W, Shen Y, Du H, Wu S (2014) Hydrogen sulfide extends the postharvest life and enhances antioxidant activity of kiwifruit during storage. J Sci Food Agric 94:2699–2704

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research is supported by National Natural Science Foundation of China (31360057). We appreciate the reviewers and editors for their exceptionally helpful comments about the manuscript.

Author’s contribution

Zhong-Guang Li implemented assumption, excogitation and wrote the paper, Jia-Zheng Jin carried through research and analysis of data. All authors read and approved the final manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhong-Guang Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, ZG., Jin, JZ. Hydrogen sulfide partly mediates abscisic acid-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells. Plant Cell Tiss Organ Cult 125, 207–214 (2016). https://doi.org/10.1007/s11240-015-0939-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-015-0939-4

Keywords

Navigation