Skip to main content
SpringerLink
Log in

Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. under Ca(NO3)2 stress

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The effects of 0.1 μM 24-epibrassinolide (EBL) on plant growth (plant height, leaf area, fresh weight, and dry weight), chlorophyll content, photosynthetic characteristics, antioxidant enzymes, and chloroplast ultrastructure were investigated using cucumber seedlings (Cucumis sativus L. cv. Jinyou No. 4) with 80 mM Ca(NO3)2 to induce stress. The presence of Ca(NO3)2 caused significant reductions in net photosynthetic rate (P N), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr) of leaves. In addition, Ca(NO3)2 markedly reduced the chlorophyll content and inhibited photochemical activity, including the actual photochemical efficiency (ΦPSII). In contrast, EBL increased the chlorophyll content, especially chlorophyll b, and minimized the harmful effects on photosynthesis caused by the Ca(NO3)2. The application of EBL to the plants subjected to Ca(NO3)2-enhanced photochemical activity. EBL protected the photosynthetic membrane system from oxidative damage due to up-regulating the capacity of the antioxidant systems. Microscopic analyses revealed that Ca(NO3)2 affected the structure of the photosynthetic apparatus and membrane system and induced damage of granal thylakoid layers, while EBL recovered the typical shape of chloroplasts and promoted the formation of grana. Taken together, EBL compensated for damage/losses by Ca(NO3)2 due to the regulation of photosynthetic characteristics and the antioxidant system.

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

Abbreviations

APX:

Ascorbate peroxidase

BRs:

Brassinosteroids

CAT:

Catalase

Chl:

Chlorophyll

EBL:

24-Epibrassinolide

Fv/Fm:

Maximal quantum yield of PSII photochemistry

GPX:

Guaiacol peroxidase

LHC:

Light-harvesting complex

PSI:

Photosystem I

PSII:

Photosystem II

ΦPSII:

The actual efficiency of PSII

qN:

Non-photochemical quenching

qP:

Coefficient for photochemical quenching

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

References

  • Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126. doi:10.1016/S0076-6879(84)05016-3

    Article  CAS  Google Scholar 

  • Ali B, Hayat S, Fariduddin Q, Ahmad A (2008a) 24-Epibrassinolide protects against the stress generated by saline and nickel in Brassica juncea. Chemosphere 72:1387–1392. doi:10.1016/j.chemosphere.2008.04.012

    Article  PubMed  CAS  Google Scholar 

  • Ali Q, Athar HR, Ashraf M (2008b) Modulation of growth, photosynthetic capacity and water relations in salt stressed wheat plants by exogenously applied 24-epibrassinolide. Plant Growth Regul 56:107–116. doi:10.1007/s10725-008-9290-7

    Article  CAS  Google Scholar 

  • Ashraf M (1994) Breeding for salinity tolerance in plants. Crit Rev Plant Sci 13:17–42. doi:10.1080/07352689409701906

    Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrate formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  PubMed  CAS  Google Scholar 

  • FAO (2012) FAO land and plant nutrition management service. http://www.fao.org/ag/agl/agll/spush

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plantarum 92:696–717. doi:10.1111/j.1399-3054.1994.tb03042.x

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase in higher plants. Plant Physiol 59:309–314

    Article  PubMed  CAS  Google Scholar 

  • Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334. doi:10.1104/pp.011254

    Article  PubMed  CAS  Google Scholar 

  • Hayat S, Hasan SA, Yusuf M, Hayat Q, Ahmad A (2010) Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata. Environ Exp Bot 69:105–112. doi:10.1016/j.envexpbot.2010.03.004

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetic and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. doi:10.1016/0003-9861(68)90654-1

    Article  PubMed  CAS  Google Scholar 

  • Herzog V, Fahimi H (1973) Determination of the activity of peroxidase. Anal Biochem 55:554–562

    Article  PubMed  CAS  Google Scholar 

  • Horn R, Grundmann G, Paulsen H (2007) Consecutive binding of chlorophylls a and b during the assembly in vitro of light-harvesting chlorophyll-a/b protein (LHCII b). J Mol Biol 366:1045–1054. doi:10.1016/j.jmb.2006.11.069

    Article  PubMed  CAS  Google Scholar 

  • Houimli SM, Denden M, El Hadj SB (2008) Induction of salt tolerance in pepper (Capsicum annuum) by 24-epibrassinolide. Eur Asia J Bio Sci 2:83–90

    Google Scholar 

  • Hu WH, Wu Y, Zeng JZ, He L, Zeng QM (2010) Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. Photosynthetica 48(4):537–544. doi:10.1007/s11099-101-0071-y

    Article  CAS  Google Scholar 

  • Ioannidis NE, Kotzabasis K (2007) Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. Biochim Biophys Acta 1767:1372–1382. doi:10.1016/j.bbabio.2007.10.002

    Article  PubMed  CAS  Google Scholar 

  • Janeczko A, Gullner G, Skoczowski A, Dubert F, Barna B (2007) Effect of brassinosteroid infiltration prior to cold treatment on ion leakage and pigment contents in rape leaves. Biol Plant 51:355–358. doi:10.1007/s10535-007-0072-2

    Article  CAS  Google Scholar 

  • Jin CY, Sun J, Guo SR (2010) Effects of exogenous spermidine on growth and active oxygen metabolism in cucumber seedlings under Ca(NO3)2 stress. Acta Bot Boreal 30(8):1627–1633

    CAS  Google Scholar 

  • Kooten O, Snel J (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150. doi:10.1007/BF00033156

    Article  Google Scholar 

  • Lambers H, Chapin FS, Pons TL (2008) Plant water relations. In: Lambers H, Chapin FS, Pons TL (eds) Plant physiological ecology. Springer, New York, pp 163–223. doi:10.1007/978-0-387-78341-3_5

  • Li DP, Wu ZJ, Liang CH, Chen LJ (2004) Characteristics and regulation of greenhouse soil environment. Chin J Ecol 23:192–197

    CAS  Google Scholar 

  • Liang YC, Si J, Nikolic M, Peng Y, Chen W, Jiang Y (2005) Organic manure stimulates biological activity and barley growth in soil subject to secondary salinization. Soil Biol Biochem 37:1185–1195. doi:10.1016/j.soilbio.2004.11.017

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. doi:10.1016/S1360-1385(02)02312-9

    Article  PubMed  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:679–690

    Google Scholar 

  • Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Yu JQ, Nogues S (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57. doi:10.1007/s00344-007-9030-7

    Article  CAS  Google Scholar 

  • Parida AK, Das AB, Mittra B (2003) Effects of NaCl stress on the structure, pigment complex composition, and photosynthetic activity of mangrove Bruguiera parvifolra chloroplasts. Photosynthetica 41:191–200. doi:10.1023/B:PHOT.0000011951.37231.69

    Article  CAS  Google Scholar 

  • Patterson BD, Macrae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plants extracts using titanium (IV). Ann Biochem 139(2):487–492. doi:10.1016/0003-2697(84)90039-3

    Article  CAS  Google Scholar 

  • Qayyum B, Shahbaz M, Akram NA (2007) Interactive effect of foliar application of 24-epibrassinolide and root zone salinity on morpho-physiological attributes of wheat (Triticum aestivum L.). Int J Agric Biol 9:584–589

    CAS  Google Scholar 

  • Sam O, Ramírez C, Coronado MJ, Testillano PS, Risueño MC (2003) Changes in tomato leaves induced by NaCl stress: leaf organization and cell ultrastructure. Biol Plantarum 47:361–366. doi:10.1023/B:BIOP.0000023878.58899.88

    Article  Google Scholar 

  • Strain HH, Svec WA (1966) Extraction, separation, estimation and isolation of the chlorophylls. In: Vernon LP, Seeley GR (eds) The chlorophylls. Academic Press, New York, pp 21–66

    Google Scholar 

  • Sun YD, Luo WR, Li XZ, Qi AG (2009) Effects of Ca(NO3)2 stress on the growth and physiological indexes of cucumber seedlings. Environ Sci Info Appl Technol 268–271. doi:10.1109/ESIAT.2009.110

  • Tong YW, Chen DF (1991) Study on the cause and control of secondary saline soils in greenhouse. Acta Hortic Sin 18:159–162

    Google Scholar 

  • Wu XG (2001) Causes and preventive measures of salt accumulation on face soil in vegetable greenhouse. J Zhejiang Wanli Univ 14:19–21

    Google Scholar 

  • Xia XJ, Huang YY, Wang L, Huang LF, Yu YL, Zhou YH, Yu JQ (2006) Pesticides-induced depression of photosynthesis was alleviated by 24-epibrassinolide pretreatment in Cucumis sativus L. Pest Biochem Phys 86:42–48. doi:10.1016/j.pestbp.2006.01.005

    Article  CAS  Google Scholar 

  • Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen ZX, Yu JQ (2009) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230:1185–1196. doi:10.1007/s00425-009-1016-1

    Article  PubMed  CAS  Google Scholar 

  • Yabuta Y, Motoki T, Yoshimura K, Takeda T, Ishikawa T, Shigeoka S (2002) Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photo-oxidative stress. Plant J 32:915–925. doi:10.1046/j.1365-313X.2002.01476.x

    Article  PubMed  CAS  Google Scholar 

  • Yamane K, Kawasaki M, Taniguchi M, Miyake H (2003) Differential effect of NaCl and polyethylene glycol on the ultrastructure of chloroplasts in rice seedlings. J Plant Physiol 160:573–575. doi:10.1078/0176-1617-00948

    Article  PubMed  CAS  Google Scholar 

  • Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogués S (2004) A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. J Exp Bot 55:1135–1143. doi:10.1093/jxb/erh124

    Article  PubMed  CAS  Google Scholar 

  • Yu HY, Li TX, Zhou JM (2005) Secondary salinization of greenhouse soil and its effects on soil properties. Soils 37(6):581–586

    CAS  Google Scholar 

  • Zhang GW, Liu ZL, Zhou JG, Zhu YL (2008) Effects of Ca(NO3)2 stress on oxidative damage, antioxidant enzymes activities and polyamine contents in roots of grafted and non-grafted tomato plants. Plant Growth Regul 56:7–19. doi:10.1007/s10725-008-9281-8

    Article  CAS  Google Scholar 

  • Zhang RH, Li J, Guo SR, Tezuka T (2009) Effects of exogenous putrescine on gas-exchange characteristics and chlorophyll fluorescence of NaCl-stressed cucumber seedlings. Photosynth Res 100:155–162. doi:10.1007/s11120-009-9441-3

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by National Basic Research Program of China (973 334 Program, No. 2009CB119000), National Natural Science Foundation of China (No. 30900995; No. 335 31071831), and the Priority Academic Program Development of Jiangsu Higher Education Institutions 336 (PAPD), and supported by the China Earmarked Fund for Modern Agro-industry 337 Technology Research System (CARS-25-C-03).

Author information

Authors and Affiliations

  1. Key Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Lingyun Yuan, Sheng Shu, Jin Sun & Shirong Guo

  2. Division of Complex System Science, Graduate School of Information Science, Nagoya University, Nagoya, 464-8601, Japan

    Takafumi Tezuka

Authors
  1. Lingyun Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sheng Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shirong Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takafumi Tezuka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shirong Guo.

Additional information

Lingyun Yuan and Sheng Shu contributed equally to this paper.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yuan, L., Shu, S., Sun, J. et al. Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. under Ca(NO3)2 stress. Photosynth Res 112, 205–214 (2012). https://doi.org/10.1007/s11120-012-9774-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-012-9774-1

Keywords

Search

Navigation