Skip to main content
Log in

Effects of 28-homobrassinoloid on key physiological attributes of Solanum lycopersicum seedlings under cadmium stress: Photosynthesis and nitrogen metabolism

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

Abstract

Heavy metal accumulation due to environmental pollution, especially in agricultural ecosystem can cause serious deterioration of crop yield and quality. In present study we assessed the effect of exogenous 28-homobrassinoloid (HBL; 10−8 M) on growth, photosynthesis, indices of chlorophyll a fluorescence and nitrogen metabolism in Solanum lycopersicum seedlings grown under two doses (Cd1: 3 mg kg−1 sand and Cd2: 9 mg kg−1 sand) of cadmium. Accumulation of Cd in root tissues was considerably higher than shoot hence, Cd declined the growth, pigment contents, and photosynthetic O2 yield in its concentration dependent manner. Chlorophyll a fluorescence due to Cd stress was negatively affected as shown by decreased QA reoxidation kinetics: φP0, ψ0, φE0 and PI_ABS and increased energy flux parameters: ABS/RC, TR0/RC, ET0/RC and DI0/RC. HBL application under Cd stress improved the photochemistry of photosystem II (PS II) by affecting these parameters positively. Treatment of Cd in test seedlings resulted into significant decrease in nitrate reductase, nitrite reductase, glutamine synthetase and glutamate synthase activities, and induced enhancing effect on ammonium content and glutamate dehydrogenase activity. Exogenous HBL treatment alleviated the negative effect of Cd on growth, photosynthesis, contents of protein, carbohydrate and inorganic nitrogen and nitrogen assimilating enzymes. The data indicate that exogenous HBL protects the test seedlings during the early growth phase against Cd phytotoxicity by regulating Cd accumulation in tissues and two key metabolic processes; photosynthesis and nitrogen metabolism.

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

Similar content being viewed by others

Abbreviations

ABS/RC:

Energy fluxes for absorption of photon per active reaction centre

DI0/RC:

Energy dissipation flux per active reaction centre

ET0/RC:

Electron transport flux per active reaction centre

Fv/F0 :

Size and number of active reaction centres in photosynthetic apparatus

F0/Fv :

Efficiency of water splitting complex

Fv/Fm (φP0):

Maximum quantum efficiency of PS II photochemistry

GS:

Glutamine synthatase

GOGAT:

Glutamate synthase

GDH:

Glutamate dehydrogenase

NR:

Nitrate reductase

NiR:

Nitrite reductase

Psi_0 or Ψ0 :

Yield of electron transport per trapped exciton

Phi_E0 or φE0 :

Quantum yield of electron transport

RC:

Reaction centre

TR0/RC:

Trapped energy flux per active reaction centre

References

  • Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013) Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213

    Article  CAS  PubMed  Google Scholar 

  • Ahammed G, Xia X, Li X, Shi K, Yu J, Zhou Y (2014) Role of brassinosteroid in plant adaptation to abiotic stresses and its interplay with other hormones. Curr Protein Pept Sci 16:462–473

    Article  Google Scholar 

  • Ali B, Hayat S, Fariduddin Q, Ahmad A (2008) 24-Epibrassinolide Protects against the stress generated by salinity and nickel in Brassica juncea. Chemosphere 72:1387–1392

    Article  CAS  PubMed  Google Scholar 

  • Allen SE, Grimshaw HM, Rowland AP (1986) Chemical analysis. In: Moore PD, Chapman SB (eds), Methods Plant Ecol. Blackwell Scientific Publication, Oxford, 285–344

    Google Scholar 

  • Balakumar T, Paliwal K (1998) Action sites of UV-B radiation in the nitrate assimilation pathway of crop plants. In: Biologic effects of light. Springer, Kluwer Academic Publishers, Berlin, pp 57–59

    Google Scholar 

  • Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect of cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Funct Plant Biol 30:57–64

    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 

  • Britto D, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

    Article  CAS  Google Scholar 

  • Cao FB, Cai Y, Liu L, Zhang M, He XY, Zhang GP, Wu FB (2015) Differences in photosynthesis, yield and grain cadmium accumulation as affected by exogenous cadmium and glutathione in the two rice genotypes. Plant Growth Regul 75:715–723

    Article  CAS  Google Scholar 

  • Cataldo DA, Haroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Anal 6:71–80

    Article  CAS  Google Scholar 

  • Chan PK, Gresshoff PM (2009) Roles of plant hormones in legume nodulation. In: Horst W, Doelle Edgar J, DaSilva (eds) Encyclopedia of Life Support Systems (EOLSS): biotechnology. EOLSS Publishers, Oxford

    Google Scholar 

  • Debouba M, Gouia H, Suzuki A, Ghorbel MH (2006) NaCl stress effects on enzymes involved in nitrogen assimilation pathway in tomato Lycopersicon esculentum seedlings. J Plant Physiol 163:1247–1258

    Article  CAS  PubMed  Google Scholar 

  • Divi UK, Rahman T, Krishna P (2016) Gene expression and functional analyses in brassinosteroid-mediated stress tolerance. Plant Biotechnol J 14:419–432

    Article  CAS  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Durand TC, Sergeant K, Planchon S, Carpin S, Label P, Morabito D, Hausman JF, Renaut J (2010) Acute metal stress in Populus tremula xP. alba (717–1B4 genotype): leaf and cambial proteome changes induced by Cd2+. Proteomics 10:349–368

    Article  CAS  PubMed  Google Scholar 

  • Gajewska E, Sklodowska M (2009) Nickel-induced changes in nitrogen metabolism in wheat shoots. J Plant Physiol 166:1034–1044

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Khan NA, Anjum NA, Tuteja N (2011) Amelioration of cadmium stress in crop plants by nutrients management: morphological, physiological and biochemical aspects. In: Anjum NA, Lopez–Lauri F (ed) Plant nutrition and abiotic stress tolerance III. Plant Stress 5:1–23

  • Govindjee (1995) Sixty–three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160

    Article  CAS  Google Scholar 

  • Gupta S, Nayek S, Saha RN, Satpati S (2008) Assessment of heavy metal accumulation in macrophyte, agricultural soil and crop plants adjacent to discharge zone of sponge iron factory. Environ Geol 55:731–739

    Article  CAS  Google Scholar 

  • Hasan SA, Hayat S, Ahmad A (2011) Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 84:1446–1451

    Article  CAS  PubMed  Google Scholar 

  • Hayat S, Ali B, Hasan SA, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ Exp Bot 60:33–41

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif Agric Exp Stn Circ 347: 1–39

    Google Scholar 

  • Hodges M (2002) Enzyme redundancy and importance of 2-oxoglutarate in plant ammonium assimilation. J Exp Bot 53:905–916

    Article  CAS  PubMed  Google Scholar 

  • Krause GH, Weiss E (1991) Chlorophyll fluorescence and photosynthesis: the basic. Annu Rev Plant Physiol 42:313–349

    Article  CAS  Google Scholar 

  • Kumar S, Joshi UN (2008) Nitrogen metabolism as affected by hexavalent chromium in sorghum (Sorghum bicolor L.). Environ Exp Bot 64:135–144

    Article  CAS  Google Scholar 

  • Kurra-Hotta M, Satoh K, Katoh S (1987) Relationship between photosynthesis and Chl content during leaf senescence of rice seedlings. Plant Cell Physiol 28:1321–1329

    Google Scholar 

  • Li S, Yang W, Yang T, Chen Y, Nia W (2015) Effects of cadmium stress on leaf chlorophyll fluorescence and photosynthesis of Elsholtzia argyi: a cadmium accumulating plant. Int J Phytoremed 17:85–92

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lillo C (1984) Diurnal variations of nitrite reductase, glutamine synthetase, glutamate synthase, alanine amino transferase and aspartate amino transferase in barley leaves. Physiol Plant 61:214–218

    Article  CAS  Google Scholar 

  • Lu Y, Duan B, Zhang X (2009) Differences in growth and physiological traits of Populus cathayana populations as affected by enhanced UV-B radiation and exogenous ABA. Environ Exp Bot 66:100–109

    Article  CAS  Google Scholar 

  • Masclaux-Daubresse C, Reisdorf-Cren M, Pageau K, Lelandias M, Grandjean J, Valadier MH, Feraud M, Jouglet T, Suzuki A (2006) Glutamine synthetase, glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink source nitrogen cycle in tobacco. Plant Physiol 140:444–456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molins-Legua C, Meseguer-Lloret S, Moliner-Martinez Y, Campıns-Falco P (2006) A guide for selecting the most appropriate method for ammonium determination in water analysis. Trends Anal Chem 25:282–290

    Article  CAS  Google Scholar 

  • Ogawa K, Soutome R, Hiroyama K, Hagio T, Ida S, Nakagawa H (2000) Co-regulation of nitrate reductase and nitrite reductase in cultured spinach cells. J Plant Physiol 157:299–306

    Article  CAS  Google Scholar 

  • Prasad SM, Zeeshan M (2005) UV-B radiation and cadmium induced changes in growth, photosynthesis, and antioxidant enzymes of cyanobacterium Plectonema boryanum. Biologia Plant 49:229–236

    Article  CAS  Google Scholar 

  • Rao SSR, Vardhini BV, Sujatha E, Anuradha S (2002) Brassinosteroids – a new class of phytohormones. Curr Sci 82 (10):1239–1245

    Google Scholar 

  • Sabater B, Rodriquez MT (1978) Control of chlorophyll degradation in detached leaves of barley and oat through effect of kinetin on chlorophyllase levels. Physiologia Plant 43:274–276

    Article  CAS  Google Scholar 

  • Sharma RK, Agrawal M, Marshall FM (2006) Heavy metal contamination in vegetables grown in wastewater irrigated areas of Varanasi, India. Bull Environ Contam Toxicol 77:312–318

    Article  CAS  PubMed  Google Scholar 

  • Sharma RK, Agrawal M, Marshall F (2009) Heavy metals in vegetables collected from production and market sites of a tropical urban area of India. Food Chem Toxicol 47:583–591

    Article  CAS  PubMed  Google Scholar 

  • Sharma N, Hundal GS, Sharma I, Bhardwaj R (2014) 28-Homobrassinolide Alters Protein Content and Activities of Glutathione-S-Transferase and Polyphenol Oxidase in Raphanus Sativus L. Plants Under Heavy Metal Stress. Toxicol Int 21(1):44–50

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A, Prasad SM (2011) Reduction of heavy metal load in food chain: technology assessment. Rev Environ Sci Biotechnol 10:199–214

    Article  CAS  Google Scholar 

  • Singh S, Prasad SM (2014) Growth, photosynthesis and oxidative responses of Solanum melongena L. seedlings to cadmium stress: mechanism of toxicity amelioration by kinetin. Sci Hortic 176:1–10

    Article  CAS  Google Scholar 

  • Singh S, Prasad SM (2015) IAA alleviates Cd toxicity on growth, photosynthesis and oxidative damages in eggplant seedlings. Plant Growth Regul 77(1):87–98

    Article  CAS  Google Scholar 

  • Singh RP, Srivastava HS (1983) Regulation of glutamate dehydrogenase activity by amino acids in maize seedlings. Physiol Plant 57:549–554

    Article  CAS  Google Scholar 

  • Singh RP, Srivastava HS (1986) Increase in glutamate synthase (NADH) activity in maize seedlings in response to nitrate and ammonium nitrogen. Physiol Plant 66:413–416

    Article  CAS  Google Scholar 

  • Singh S, Singh A, Bashri G, Prasad SM (2016) Impact of Cd stress on cellular functioning and its amelioration by phytohormones: an overview on regulatory network. Plant Growth Regul 80(3):253–263

    Article  CAS  Google Scholar 

  • Skopelitis DS, Paranychianakis NV, Paschalidis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18:2767–2781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snell FD, Snell CT (1949) Colorimetric methods of analysis, vol 3. Van Nostrand, New York, NY, pp 804–805

  • Soaresa C, Alexandra de Sousa A, Pinto A, Azenha M, Teixeira J, Antunes Azevedoc R, Fidalgo F (2016) Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. Environ Exp Bot 122:115–125

    Article  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterise and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Taylor & Francis, London, pp 445–483

    Google Scholar 

  • Sun JY, Shen ZG (2007) Effects of Cd stress on photosynthetic characteristics and nutrient uptake of cabbages with different Cd-tolerance. Chin J App Ecol 18:2605–2610

    CAS  Google Scholar 

  • Tiwari BS, Belenghi B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 128:1271–1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Sun J, Du L, Liu X (2012) Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytol 196:110–124

    Article  CAS  PubMed  Google Scholar 

  • Yusuf M, Fariduddin Q, Hayat S, Hasan SA, Ahmad A (2011) Protective responses of 28 homobrssinolide in cultivars of Triticum aestivum with different levels of nickel. Arch Environ Contam Toxicol 60:68–76

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Wang J, Li X, Xia XJ, Zhou YH, Shi K (2014) H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J Exp Bot 65:4371–4383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are very grateful to University of Allahabad, Allahabad for providing necessary facilities. The University Grants Commission, New Delhi is thankfully acknowledged for providing financial assistant to Prof. S.M. Prasad as PI [Project No.: 41–460/2012(SR)] and to Shikha Singh as project fellow to carry out this work. I must acknowledge Prof. Anoop Chaturvedi, Head of the Statistic Department, and Dr. Anita Singh (DST Young Scientist) Department of Botany, University of Allahabad, Allahabad for their kind suggestion regarding statistical analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sheo Mohan Prasad.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, S., Prasad, S.M. Effects of 28-homobrassinoloid on key physiological attributes of Solanum lycopersicum seedlings under cadmium stress: Photosynthesis and nitrogen metabolism. Plant Growth Regul 82, 161–173 (2017). https://doi.org/10.1007/s10725-017-0248-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-017-0248-5

Keywords

Navigation