Skip to main content
Log in

The exogenous application of spermidine alleviates photosynthetic inhibition and membrane lipid peroxidation under low-light stress in tomato (Lycopersicon esculentum Mill.) seedlings

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The effects of three concentrations (0.001, 0.01, and 0.1 mg/L) of exogenous spermidine (Spd) on the O ·−2 production rate, malondialdehyde (MDA) content, antioxidant enzyme activities, leaf photosynthesis, chlorophyll content, chlorophyll fluorescence, and light response curve parameters were investigated in the seedlings of two tomato cultivars: low-light-stress-tolerant ‘Zhongza 9’ and sensitive ‘Zhongshu 6’. Low-light stress of 150 μmol m−2 s−1 resulted in an increase in the O ·−2 production rate, MDA content, and peroxidase activity, whereas the superoxide dismutase and catalase activities decreased. Exogenous Spd effectively ameliorated these effects. The net photosynthetic rate (Pn), maximal photochemical quantum efficiency of photosystem II (Fv/Fm), light saturation point, net photosynthetic rate at light saturation point (Amax), and dark respiration rate (Rd) simultaneously decreased under low light, but the chlorophyll content, particularly the chlorophyll b (chlb) content, markedly increased when compared to the normal-light (control) plants. Exogenous Spd diminished the decrease in leaf Pn and Fv/Fm and induced a further increase in the chlb content and decrease in Rd and chla/chlb under low-light stress. These results suggested that exogenous Spd could improve plant tolerance by alleviating the membrane lipid peroxidation and photosynthetic inhibition resulting from low light. However, the optimal Spd concentration generally differed in the two cultivars.

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

Similar content being viewed by others

Abbreviations

IVF:

Institute of Vegetables and Flowers

CAAS:

Chinese Academy of Agricultural Sciences

Spd:

Spermidine (Spd1, 0.1 mg/L Spd; Spd2, 0.01 mg/L Spd; Spd 3, 0.001 mg/L Spd)

References

  • Ai XZ, Guo YK, Ma XZ, Xing YX (2004) Photosynthetic characteristics and ultrastructure of chloroplast of cucumber under low light intensity in solar greenhouse. Sci Agric Sin 37:268–273

    Google Scholar 

  • Anderson JM, Goodchild DJ, Boardman NK (1973) Composition of the photosystems and chloroplast structure in extreme shade plants. BBA Bioenerg 325:573–585

    Article  CAS  Google Scholar 

  • Anjum MA (2009) Effect of exogenously applied Spd on growth and physiology of citrus rootstock Troyer citrange under saline conditions. Turk J Agric For 2011:43–53

    Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Chen SY (1989) Membrane-lipid peroxidation and plant stress. Chin Bull Bot 6:211–217

    Google Scholar 

  • Cheng L, Zou YJ, Ding SL, Zhang JJ, Yu XL, Cao JS, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Sun RR, Wang FY, Peng Z, Kong FL, Wu J, Cao JS, Lu G (2012) Spermidine affects the transcriptome responses to high temperature stress in ripening tomato fruit. J Zhejiang Univ Sci B 13:283–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus—the protective role of polyamines. Biochim Biophys Acta Bioenerg 1767:272–280

    Article  CAS  Google Scholar 

  • Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defence against lipid peroxidation. J Exp Bot 32:79–91

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Duan JJ, Li J, Guo SR, Kang YY (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635

    Article  CAS  PubMed  Google Scholar 

  • Groppa MD, Benavides MP, Tomaro ML (2003) Polyamine metabolism in sunf lower and wheat leaf discs under cadmium or copper stress. Plant Sci 164:293–299

    Article  CAS  Google Scholar 

  • Hu LP, Xiang LX, Zhang L, Zhou XT, Zou ZR, Hu XH (2014) The photoprotective role of spermidine in tomato seedlings under salinity-alkalinity stress. PLoS ONE. doi:10.1371/journal.pone.0110855

    Google Scholar 

  • Huang WD, Wu LK, Zhan JC (2002) Effect of low light on the peroxidation of membrane-lipid of cherry leaves. Acta Bot Sin 8:920–924

    Google Scholar 

  • Huang WD, Wu LK, Zhan JC (2004) Growth and photosynthesis adaptation of dwarf-type Chinese cherry (Prunus pseudocerasus L. cv. Laiyang) leaves to weak light stress. Sci Agric Sin 37:1981–1985

    Google Scholar 

  • Jiménez-Bremont JF, Ruiz OA, Rodríguez-Kessler M (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821

    Article  PubMed  Google Scholar 

  • Kochba J, Lavee S, Spiegel-Roy P (1977) Differences in peroxidase activity and isoenzymes in embryogenic ane non-embryogenic ‘Shamouti’ orange ovular callus lines. Plant Cell Physiol 18:463–467

    CAS  Google Scholar 

  • Kooten O, Snel JH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  PubMed  Google Scholar 

  • Kubiś J (2006) Exogenous spermidine alters in different way membrane permeability and lipid peroxidation in water stressed barley leaves. Acta Physiol Plant 28:27–33

    Article  Google Scholar 

  • Kumar SV, Sharma ML, Rajam MV (2006) Polyamine biosynthetic pathway as a novel target for potential applications in plant biotechnology. Physiol Mol Biol Plants 12:13–18

    CAS  Google Scholar 

  • Li H (2000) Principles and techniques of plant physiological biochemical experiment. Higher Education Press, Beijing

    Google Scholar 

  • Li ZG, Gong M (2005) Improvement of measurement method for superoxide anion radical in plant. Acta Bot Yunnanica 27:211–216 (in Chinese)

    CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Nayyar H, Kaur S, Singh S, Kumar S, Singh KJ, Dhir KK (2005) Involvement of polyamines in the contrasting sensitivity of chickpea (Cicer arietinum L.) and soybean (Glycine max (L.) Merrill.) to water deficit stress. Bot Bull Acad Sin 46:333–338

    CAS  Google Scholar 

  • Rider JE, Hacker A, Mackintosh CA, Pegg AE, Woster PM, Casero RA Jr (2007) Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33:231–240

    Article  CAS  PubMed  Google Scholar 

  • Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168:317–328

    Article  CAS  PubMed  Google Scholar 

  • Send SS, Wang Q, Zhang YE, Li CH, Liu TX, Zhao LF, Liu HP (2012) Effects of exogenous spermidine on physiological regulatory of maize after waterlogging stress. Acta Agron Sin 6:1042–1050

    Google Scholar 

  • Sfakianaki M, Sfichi L, Kotzabasis K (2006) The involvement of LHCII associated polyamines in the response of the photosynthetic apparatus to low temperature. J Photochem Photobiol B Biol 84:181–188

    Article  CAS  Google Scholar 

  • Sfichi L, Ioannidis N, Kotzabasis K (2004) Thylakoid-associated polyamines adjust the UV-B sensitivity of the photosynthetic apparatus by means of light-harvesting complex II changes. Photochem Photobiol 80:499–506

    Article  CAS  PubMed  Google Scholar 

  • Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sui XL, Jiang JZ, Wang ZY, Zhu YJ (1999) Effect of low light intensity on photosynthetic characteristics of different sweet pepper cultivars. Acta Hortic Sin 26:314–318

    Google Scholar 

  • Sui XL, Zhang BX, Zhang ZX, Mao SL, Wang LH (2005) Differences of photosynthetic characteristics and low light-tolerance in seedlings of four pepper cultivars. Acta Hortic Sin 32:222–227

    CAS  Google Scholar 

  • Unal D, Tuney I, Sukatar A (2008) The role of external polyamines on photosynthetic responses, lipid peroxidation, protein and chlorophyll a content under the UV-A (352 nm) stress in Physcia semipinnata. J Photochem Photobiol B Biol 90:64–68

    Article  CAS  Google Scholar 

  • Wang LJ, Zhang P, Gu QH, Zheng DH (2002) Study on changes of tomato ecology and biology characteristics under decreasing-light conditions. Tianjin Agric Sci 1:18–22

    Google Scholar 

  • Wang M, Jiang WJ, Yu HJ (2010) Effects of exogenous epibrassinolide on photosynthetic characteristics in tomato (Lycopersicon esculentum Mill) seedlings under weak light stress. J Agric Food Chem 58:3642–3645

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi KJ, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J, Liu K, Wang Z, Liu L (2007) Involvement of polyamines in the drought resistance of rice. J Exp Bot 58:1545–1555

    Article  CAS  PubMed  Google Scholar 

  • Zhang WP, Jiang B, Li WG, Song H, Yu YS, Chen JF (2009) Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Sci Hortic 122:200–208

    Article  CAS  Google Scholar 

  • Zhao HZ, Yang H (2008) Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis Rehd. Sci Hortic 116:442–447

    Article  CAS  Google Scholar 

  • Zhu YS, Gao SS, Feng H (2005) Effects of low light on leaf Pn and chlorophyll content in tomato seedlings of different genotypes. Liaoning Agric Sci 1:17–18

    Google Scholar 

Download references

Acknowledgments

This work was supported by the earmarked fund for China Agricultural Research System (CARS-25-C-09) and Science-Tech of Agri-industry Project (201203095, 20120301) Ministry of Agriculture, P. R. China; and national key project (2011BAD12B01), the National Key Basic R&D Program (2009CB19001), Ministry of Sciences & Technology, P. R. China.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Weijie Jiang.

Additional information

Hongjun Yu, Wenchao Zhao and Ming Wang have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, H., Zhao, W., Wang, M. et al. The exogenous application of spermidine alleviates photosynthetic inhibition and membrane lipid peroxidation under low-light stress in tomato (Lycopersicon esculentum Mill.) seedlings. Plant Growth Regul 78, 413–420 (2016). https://doi.org/10.1007/s10725-015-0102-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-015-0102-6

Keywords

Navigation