Skip to main content
SpringerLink
Log in

Hydrogen sulfide donor sodium hydrosulfide-induced accumulation of betaine is involved in the acquisition of heat tolerance in maize seedlings

  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Hydrogen sulfide (H2S) which is involved in plant growth, development, and the acquisition of stress tolerance including heat tolerance, is considered as the third signal molecule after nitric oxide and reactive oxygen species, while betaine is an important osmolyte with multiple physiological functions, but interaction between H2S and betaine in the acquisition of heat tolerance in plants is not clear. In this study, pretreatment with H2S donor sodium hydrosulfide (NaHS), as comparison to the control seedlings without NaHS treatment, significantly improved the activity of betaine aldehyde dehydrogenase (BADH), a key enzyme in the biosynthesis of betaine, which in turn induced the accumulation of endogenous betaine, eventually enhanced the survival percentage of maize seedlings under heat stress. In contrast, these effects induced by NaHS were eliminated by application of H2S scavenger hypotaurine and inhibitor of BADH disulfiram, respectively, indicating that H2S-improved heat tolerance of maize seedlings may be closely associated with the accumulation of endogenous betaine by activating the activity of BADH. In addition, exogenous betaine treatment enhanced the content of endogenous betaine, followed by improved the survival percentage of maize seedlings compared with the control without betaine treatment. All of the above-mentioned results showed that NaHS pretreatment could induce the accumulation of endogenous betaine by increasing BADH activity, and this accumulation may be involved in the acquisition of heat tolerance of maize seedlings, bridging a gap between H2S and betaine in the acquisition of heat tolerance in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Christou A, Filippou P, Manganaris GA, Fotopouls 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 Central  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 

  • Fan W, Zhang M, Zhang H, Zhang P (2012) Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PLoS One 7:e37344

    Article  PubMed Central  CAS  PubMed  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 

  • Fitzgerald TL, Waters DLE, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol 11:119–130

    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 (2010) Hydrogen sulfide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984

    Article  PubMed  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 201:66–73

    Article  PubMed  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 

  • Hanumappa M, Nguyen HT (2010) Genetic approaches toward improving heat tolerance in plants. In: Jenks MA, Wood AJ (eds) Genes for plant abiotic stress. Wiley-Blackwell, Oxford, pp 221–260

    Google Scholar 

  • Jin ZP, Xue SW, Luo YN, Tian BH, Fang HH, Li H, Pei YX (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 

  • Königshofer H, Tromballa HW, Loppert HG (2008) Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant Cell Environ 31:1771–1780

    Article  PubMed  Google Scholar 

  • Leipner J, Stamp P (2009) Chilling stress in maize seedlings. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its biology. Springer, New York, pp 291–344

    Chapter  Google Scholar 

  • Li ZG, Gong M (2011) Mechanical stimulation-induced cross-adaptation in plants: an overview. J Plant Biol 54:358–364

    Article  Google Scholar 

  • Li SF, Li F, Wang JW, Zhang W, Meng QW, Chen THH, Murata N, Yang XH (2011a) Glycine betaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings. Plant Cell Environ 34:1931–1943

    Article  CAS  PubMed  Google Scholar 

  • Li L, Rose P, Moore PK (2011b) 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 185:185–189

    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, 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 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, Yuan LX, Wang QL, Ding ZL, Dong CY (2013c) Combined action of antioxidant defense system and osmolytes in chilling shock-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol Plant 35:2127–2136

    Article  CAS  Google Scholar 

  • Li MF, Guo SJ, Xu Y, Meng QW, Li G, Yang XH (2014a) Glycine betaine-mediated potentiation of HSP gene expression involves calcium signaling pathways in tobacco exposed to NaCl stress. Physiol Plant 150:63–75

    Article  CAS  PubMed  Google Scholar 

  • Li MF, Li ZM, Li SF, Guo SJ, Meng QM, Li G, Yang XH (2014b) Genetic engineering of glycine betaine biosynthesis reduces heat-enhanced photoinhibition by enhancing antioxidative defense and alleviating lipid peroxidation in tomato. Plant Mol Biol Rep 32:42–51

    Article  CAS  Google Scholar 

  • Li ZG, Luo LJ, Zhu LP (2014c) Involvement of trehalose in hydrogen sulfide donor sodium hydrosulfide-induced the acquisition of heat tolerance in maize (Zea mays L.) seedlings. Bot Stu 55:20

    Article  Google Scholar 

  • Li ZG, Yi XY, Li YT (2014d) 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 

  • 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 

  • Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125

    Article  CAS  PubMed  Google Scholar 

  • Nakamura M, Kuramata M, Kasugai I, Abe M, Youssefian S (2009) Increased thiol biosynthesis of transgenic poplar expressing a wheat O-acetylserine(thiol) lyase enhances resistance to hydrogen sulfide and sulfur dioxide toxicity. Plant Cell Rep 28:313–323

    Article  CAS  PubMed  Google Scholar 

  • Oukarroum A, Madidi SE, Strasser RJ (2012) Exogenous glycine betaine and proline play a protective role in heat-stressed barley leaves (Hordeum vulgare L.): a chlorophyll a fluorescence study. Plant Biosyst 146:1037–1043

    Article  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vog 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 9:582–588

    Article  CAS  PubMed  Google Scholar 

  • Saidi Y, Finka A, Goloubinoff P (2011) Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol 190:556–565

    Article  CAS  PubMed  Google Scholar 

  • Shan C, Liu H, Zhao L, Wang X (2014) Effects of exogenous hydrogen sulfide on the redox states of ascorbate and glutathione in maize leaves under salt stress. Biol Plant 58:169–173

    Article  CAS  Google Scholar 

  • Strable J, Scanlon MJ (2009) Maize (Zea Mays): A model organism for basic and applied research in plant biology. Cold Spring Harb Protoc 10 (2009), pdb.emo132

  • Szabados L, Savoure A (2010) Proline: A multifunctional amino acid. Trends Plant Sci 15:89–97

  • Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

  • Velasco-García R, Chacón-Aguilar VM, Hervert-Hernández D, Muñoz-Clares RA (2003) Inactivation of betaine aldehyde dehydrogenase from Pseudomonas aeruginosa and Amaranthus hypochondriacus L. leaves by disulfiram. Chem Biol Int 143/144:149–158

    Article  Google Scholar 

  • 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 GP, Zhang XY, Li F, Luo Y, Wang W (2010) Overaccumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis. Photosynthetica 48:117–126

    Article  CAS  Google Scholar 

  • Wu HC, Luo DL, Vignols F, Jinn TL (2012) Heat shock-induced biphasic Ca2+ signature and OsCaM1-1 nuclear localization mediate downstream signalling in acquisition of thermotolerance in rice (Oryza sativa L.). Plant Cell Environ 35:1543–1557

    Article  CAS  PubMed  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 Normal Univ 33:29–35

    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 WP, 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 51:1084–1092

    Google Scholar 

  • Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250

    Article  CAS  Google Scholar 

  • Zhang H, Wang MF, Hua LY, Wang SH, Hua KD, Bao LJ, Luo JP (2010) Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ J Plant Physiol 57:532–539

    Article  CAS  Google Scholar 

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

    Article  CAS  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 information

Authors and Affiliations

  1. School of Life Sciences, Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Normal University, Kunming, Yunnan, 650092, People’s Republic of China

    Z.-G. Li & L.-P. Zhu

Authors
  1. Z.-G. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L.-P. Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Z.-G. Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, ZG., Zhu, LP. Hydrogen sulfide donor sodium hydrosulfide-induced accumulation of betaine is involved in the acquisition of heat tolerance in maize seedlings. Braz. J. Bot 38, 31–38 (2015). https://doi.org/10.1007/s40415-014-0106-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-014-0106-x

Keywords

Search

Navigation