Skip to main content

Advertisement

Log in

Enhanced tolerance to salinity stress in grapevine plants through application of carbon quantum dots functionalized by proline

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Salinity has destructive impacts in plant production; therefore, application of new approaches such as nanotechnology and plant priming is attracting increasing attention as an innovative means to ameliorate salt stress effects. Considering the unique properties and recorded beneficial influence of carbon quantum dots (CQDs) and proline in plant growth and physiological parameters when applied individually, their conjugation in the form of carbon quantum dot nanoparticles functionalized by proline (Pro-CQDs NPs) could lead to synergistic effects. Accordingly, an experiment was conducted to evaluate the impact of this advanced nanomaterial (Pro-CQDs NPs) as a chemical priming agent, in grapevine plants cv. ‘Rasha’. For this purpose, proline, CQDs, and Pro-CQDs NPs at three concentrations (0, 50, and 100 mg L−1) were applied exogenously 48 h prior to salinity stress (0 and 100 mM NaCl) that was imposed for a month. Three days after imposing salt stress, an array of biochemical measurements was recorded, while agronomic and some physiological parameters were noted at the end of the stress period. Results revealed that proline treatment at both concentrations, as well as CQDs and Pro-CQDs NPs at low concentration, positively affected grapevine plants under both non-stress and stress conditions. Specifically, the application of proline at 100 mg L−1 and Pro-CQDs NPs at 50 mg L−1 resulted in optimal performance identifying 50 mg L−1 Pro-CQDs NPs as the optimal treatment. Proline treatment at 100 mg L−1 increased leaf fresh weight (FW) and dry weight (DW); chl a, b, and proline content; SOD activity under both non-stress and stress conditions; Y (II) under salinity and carotenoid content; and CAT activity under control conditions. Pro-CQDs NP treatment at 50 mg L−1 enhanced total phenol, anthocyanin, and Fv/Fo, as well as APX and GP activities under both conditions, while increasing carotenoid, Y (II), Fv/Fo, and CAT activity under salinity. Furthermore, it decreased MDA and H2O2 contents at both conditions and EL and Y (NO) under salt stress. Overall, conjugation of CQDs with proline at 50 mg L−1 resulted in further improving the protective effect of proline application at 100 mg L−1. Therefore, functionalization of NPs with chemical priming agents appears to be an effective means of optimizing plant-priming approaches towards efficient amelioration of abiotic stress–related damage in plants.

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

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

Chl:

Chlorophyll

CQDs:

Carbon quantum dots

DW:

Dry weight

FW:

Fresh weight

GP:

Guaiacol peroxidase

H2O2 :

Hydrogen peroxide

MDA:

Malondialdehyde

Pro:

Proline

Pro-CQDs NPs:

Carbon quantum dots nanoparticles functionalized by proline

SOD:

Superoxide dismutase

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

  • Ahammed GJ, Li Y, Li X, Han WY, Chen S (2018) Epigallocatechin-3-gallate alleviates salinity-retarded seed germination and oxidative stress in tomato. J Plant Growth Regul 37(4):1349–1356

    Article  CAS  Google Scholar 

  • Ahanger MA, Alyemeni MN, Wijaya L, Alamri SA, Alam P, Ashraf M, Ahmad P (2018) Potential of exogenously sourced kinetin in protecting Solanum lycopersicum from NaCl-induced oxidative stress through up-regulation of the antioxidant system, ascorbate-glutathione cycle and glyoxalase system. PLoS One 13(9):e0202175

    Article  CAS  Google Scholar 

  • Ahmad P, Ahanger MA, Alam P, Alyemeni MN, Wijaya L, Ali S, Ashraf M (2019) Silicon (Si) supplementation alleviates NaCl toxicity in mung bean [Vigna radiata (L.) Wilczek] through the modifications of physio-biochemical attributes and key antioxidant enzymes. J Plant Growth Regul 38(1):70–82

    Article  CAS  Google Scholar 

  • Ashraf MA, Ashraf M, Ali Q (2010) Response of two genetically diverse wheat cultivars to salt stress at different growth stages: leaf lipid peroxidation and phenolic contents. Pak J Bot 42(1):559–565

    CAS  Google Scholar 

  • Bai X, Purcell-Milton F, Gun’ko YK (2019) Optical properties, synthesis, and potential applications of Cu-based ternary or quaternary anisotropic quantum dots, polytypic nanocrystals, and core/shell heterostructures. Nanomaterials 9(1):85

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    Article  CAS  Google Scholar 

  • Biju V, Mundayoor S, Omkumar RV, Anas A, Ishikawa M (2010) Bioconjugated quantum dots for cancer research: present status, prospects and remaining issues. Biotechnol Adv 28(2):199–213

    Article  CAS  Google Scholar 

  • Chakravarty D, Erande MB, Late DJ (2015) Graphene quantum dots as enhanced plant growth regulators: effects on coriander and garlic plants. J Sci Food Agric 95(13):2772–2778

    Article  CAS  Google Scholar 

  • Doganlar ZB, Demir K, Basak H, Gul I (2010) Effects of salt stress on pigment and total soluble protein contents of three different tomato cultivars. Afr J Agric Res 5(15):2056–2065

    Google Scholar 

  • Eryilmaz F (2006) The relationships between salt stress and anthocyanin content in higher plants. Biotechnol Biotechnol Equip 20(1):47–52

    Article  CAS  Google Scholar 

  • Feng P, Geng B, Cheng Z, Liao X, Pan D, Huang J (2019) Graphene quantum dots-induced physiological and biochemical responses in mung bean and tomato seedlings. Brazil J Bot 42(1):29–41

    Article  Google Scholar 

  • Filippou P, Bouchagier P, Skotti E, Fotopoulos V (2014) Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ Exp Bot 97:1–10

    Article  CAS  Google Scholar 

  • Flohe L, Günzler WA (1984) Assays of glutathione peroxidase. Method Enzyme 105:114–120

    Article  CAS  Google Scholar 

  • Gharsallah C, Fakhfakh H, Grubb D, Gorsane F (2016) Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants 8:12–25

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930

    Article  CAS  Google Scholar 

  • Giusti MM, Wrolstad RE (2001) Characterization and measurement of anthocyanins by UV-visible spectroscopy. Curr Protocols Food Chem 2:1–13

    Google Scholar 

  • Gohari G, Alavi Z, Esfandiari E, Panahirad S, Hajihoseinlou S, Fotopoulos V (2020a) Interaction between hydrogen peroxide and sodium nitroprusside following chemical priming of Ocimum basilicum L. against salt stress. Physiol Plant 168(2):361–373

    CAS  Google Scholar 

  • Gohari G, Mohammadi A, Akbari A, Panahirad S, Dadpour MR, Fotopoulos V, Kimura S (2020b) Titanium dioxide nanoparticles (TiO2 NPs) promote growth and ameliorate salinity stress effects on essential oil profile and biochemical attributes of Dracocephalum moldavica. Sci Rep 10(1):1–14

    Article  CAS  Google Scholar 

  • Gohari G, Safai F, Panahirad S, Akbari A, Rasouli F, Dadpour MR, Fotopoulos V (2020c) Modified multiwall carbon nanotubes display either phytotoxic or growth promoting and stress protecting activity in Ocimum basilicum L. in a concentration-depended manner. Chemosphere 126:171

    Google Scholar 

  • Hasanuzzaman M, Bhuyan MHM, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Futija M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9(8):681

    Article  CAS  Google Scholar 

  • Hatami M (2017) Toxicity assessment of multi-walled carbon nanotubes on Cucurbita pepo L. under well-watered and water stressed conditions. Ecotoxic Environ Safety 142:274–283

    Article  CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466

    Article  CAS  Google Scholar 

  • Hoque MA, Banu MNA, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline and glycinebetaine increase NaCl-induced ascorbate–glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. J Plant Physiol 164(11):1457–1468

    Article  CAS  Google Scholar 

  • Hu X, Kang J, Lu K, Zhou R, Mu L, Zhou Q (2014) Graphene oxide amplifies the phytotoxicity of arsenic in wheat. Sci Rep 4:6122

    Article  CAS  Google Scholar 

  • Ioannou A, Gohari G, Papaphilippou P, Panahirad S, Akbari A, Dadpour MR, Krasia-Christoforou T, Fotopoulos V (2020) Advanced nanomaterials in agriculture under a changing climate: the way to the future? Environ Exp Bot 176:104048

    Article  CAS  Google Scholar 

  • Kaya C, Tuna AL, Ashraf M, Altunlu H (2007) Improved salt tolerance of melon (Cucumis melo L.) by the addition of proline and potassium nitrate. Environ Exp Bot 60(3):397–403

    Article  CAS  Google Scholar 

  • Khan MN, Mobin M, Abbas ZK, AlMutairi KA, Siddiqui ZH (2017) Role of nanomaterials in plants under challenging environments. Plant Physiol Biochem 110:194–209

    Article  CAS  Google Scholar 

  • Khan I, Raza MA, Awan SA, Shah GA, Rizwan M, Ali B, Tariq R, Hassan MJ, Alyemeni MN, Brestic M, Zhang X (2020) Amelioration of salt induced toxicity in pearl millet by seed priming with silver nanoparticles (AgNPs): the oxidative damage, antioxidant enzymes and ions uptake are major determinants of salt tolerant capacity. Plant Physiol Biochem 156:221–232

    Article  CAS  Google Scholar 

  • Khanna-Chopra R, Semwal VK, Lakra N, Pareek A (2019) Proline–a key regulator conferring plant tolerance to salinity and drought. In: Plant tolerance to environmental stress: role of phytoprotectants. CRC Press, Boca Raton, pp 59–80

  • Kovinich N, Kayanja G, Chanoca A, Otegui MS, Grotewold E (2015) Abiotic stresses induce different localizations of anthocyanins in Arabidopsis. Plant Signal Behav 10(7):e1027850

    Article  CAS  Google Scholar 

  • Kubala S, Wojtyla Ł, Quinet M, Lechowska K, Lutts S, Garnczarska M (2015) Enhanced expression of the proline synthesis gene P5CSA in relation to seed osmopriming improvement of Brassica napus germination under salinity stress. J Plant Physiol 183:1–12

    Article  CAS  Google Scholar 

  • Li W, Tailhades J, O’Brien-Simpson NM, Separovic F, Otvos L, Hossain MA, Wade JD (2014) Proline-rich antimicrobial peptides: potential therapeutics against antibiotic-resistant bacteria. Amino Acids 46(10):2287–2294

    Article  CAS  Google Scholar 

  • Li H, Huang J, Lu F, Liu Y, Song Y, Sun Y, Lifshitz Y (2018) Impacts of carbon dots on rice plants: boosting the growth and improving the disease resistance. ACS Appl Bio Mater 1(3):663–672

    Article  CAS  Google Scholar 

  • Lim JH, Park KJ, Kim BK, Jeong JW, Kim HJ (2012) Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrum esculentum M.) sprout. Food Chem 135(3):1065–1070

    Article  CAS  Google Scholar 

  • Lim SY, Shen W, Gao Z (2015) Carbon quantum dots and their applications. Chem Soc Rev 44(1):362–381

    Article  CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J Exp Bot 46:1843–1852

    Article  CAS  Google Scholar 

  • Mane AV, Karadge BA, Samant JS (2010) Salinity induced changes in photosynthetic pigments and polyphenols of Cymbopogon nardus (L.) Rendle. J Chem Pharm Res 2(3):338–347

    CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51(345):659–668

    Article  CAS  Google Scholar 

  • Molassiotis A, Fotopoulos V (2011) Oxidative and nitrosative signaling in plants: two branches in the same tree? Plant Signal Behav 6:210–214

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880

    CAS  Google Scholar 

  • Omoto E, Kawasaki M, Taniguchi M, Miyake H (2009) Salinity induces granal development in bundle sheath chloroplasts of NADP-malic enzyme type C4 plants. Plant Prod Sci 12:199–207

    Article  CAS  Google Scholar 

  • Ozden M, Demirel U, Kahraman A (2009) Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Sci Hortic 119(2):163–168

    Article  CAS  Google Scholar 

  • Perveen SHAGUFTA, Nazir M (2018) Proline treatment induces salt stress tolerance in maize (Zea mays L. CV. Safaid Afgoi). Pak J Bot 50(4):1265–1271

    CAS  Google Scholar 

  • Pollastri S, Savvides A, Pesando M, Lumini E, Volpe MG, Ozudogru EA, Faccio A, De Cunzo F, Michelozzi M, Lambardi M, Fotopoulos V, Loretto F, Centritto M, Balestrini R (2018) Impact of two arbuscular mycorrhizal fungi on Arundo donax L. response to salt stress. Planta 247(3):573–585

    Article  CAS  Google Scholar 

  • Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50(1):2–18

    Article  CAS  Google Scholar 

  • Rao S, Shekhawat GS (2016) Phytotoxicity and oxidative stress perspective of two selected nanoparticles in Brassica juncea. Biotechnology 6(2):244

    Google Scholar 

  • Reddy PS, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, Kishor PK (2015) Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 94:104–113

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey R, Pessarkli M (2012a) Reactive oxygen species, oxidative da mage, and antioxidative defense mechanism in plants under stressful conditions. Aust J Bot 1:1–26

    Google Scholar 

  • Sharma P, Bhatt D, Zaidi MG, Saradhi PP, Khanna PK (2012b) Silver nanoparticle-mediated enhancement in growth and antioxidant status of Brassica juncea. Appl Biochem Biotechnol 167:2225–2233

    Article  CAS  Google Scholar 

  • Sinha S, Saxena R, Singh S (2005) Chromium induced lipid peroxidation in the plants of Pistia stratiotes L.: role of antioxidants and antioxidant enzymes. Chemosphere 58:595–604

    Article  CAS  Google Scholar 

  • Stewart RRC, Bewley JD (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 65:245–258

    Article  CAS  Google Scholar 

  • Tang W, Newton RJ (2005) Peroxidase and catalase activities are involved in direct adventitious shoot formation induced by thidiazuron in eastern white pine (Pinus strobes L.) zygotic embryos. Plant Physiol Biochem 43:760–769

    Article  CAS  Google Scholar 

  • Tang X, Mu X, Shao H (2015) Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Crit Rev Biotechnol 35:425–437

    Article  CAS  Google Scholar 

  • Wang H, Zhang M, Song Y, Li H, Huang H, Shao M, Kang Z (2018) Carbon dots promote the growth and photosynthesis of mung bean sprouts. Carbon 136:94–102

    Article  CAS  Google Scholar 

  • Wani SH, Kumar V, Khare T, Guddimalli R, Parveda M, Solymosi K, Suprasanna P, Kishor PBK (2020) Engineering salinity tolerance in plants: progress and prospects. Planta 251:76

    Article  CAS  Google Scholar 

  • Xu C, Zhang Y, Cao L, Lu J (2010) Phenolic compounds and antioxidant properties of different grape cultivars grown in China. Food Chem 119:1557–1565

    Article  CAS  Google Scholar 

  • Yan Z, Guo S, Shu S, Sun J, Tezuka T (2011) Effects of proline on photosynthesis, root reactive oxygen species (ROS) metabolism in two melon cultivars (Cucumis melo L.) under NaCl stress. Afr J Biotechnol 10(80):18381–18390

    CAS  Google Scholar 

  • Yan K, Shao H, Shao C, Chen P, Zhao S, Brestic M, Chen X (2013) Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. Acta Physiol Plant 35(10):2867–2878

    Article  CAS  Google Scholar 

  • Yi Z, Li S, Liang Y, Zhao H, Hou L, Yu S, Ahammed GJ (2018) Effects of exogenous spermidine and elevated CO2 on physiological and biochemical changes in tomato plants under iso-osmotic salt stress. J Plant Growth Regul 37(4):1222–1234

    Article  CAS  Google Scholar 

  • Zhang M, Gao B, Chen J, Li YC (2015) Effects of graphene on seed germination and seedling growth. J Nanopart Res 17(2):78

    Article  CAS  Google Scholar 

  • Zouari M, Ahmed CB, Elloumi N, Bellassoued K, Delmail D, Labrousse P, Rouina BB (2016) Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L. cv Chemlali exposed to cadmium stress. Ecotoxic Environ Safety 128:195–205

    Article  CAS  Google Scholar 

  • Zouari M, Elloumi N, Labrousse P, Rouina BB, Abdallah FB, Ahmed CB (2018) Olive trees response to lead stress: exogenous proline provided better tolerance than glycine betaine. South Afric J Bot 118:158–165

    Article  CAS  Google Scholar 

Download references

Acknowledgements

S. Panahirad acknowledges University of Tabriz (Tabriz, Iran) for the grant research support (grant number 4602). The authors express sincere thanks to the University of Maragheh for providing the research facilities to carry out the present research study.

Author information

Authors and Affiliations

Authors

Contributions

GG, SP, VF, and AA designed the experimental setup. NS and AF performed greenhouse experiments, and applied biochemical and physiological parameters. AA and HJ synthesized the nanomaterials. SMZ performed statistical analysis. GG, MD, and AA analyzed data and results, while GG, SP, and VF wrote the manuscript.

Corresponding author

Correspondence to Gholamreza Gohari.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Gangrong Shi

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

Fig. S1 Effect of Pro-CQD NPs (0, 50 and 100 mg L−1) treatments under non-stress (A) and 100 mM NaCl salt stress conditions (B) on Vitis vinifera cv. ‘Rasha’ plant phenotypes. i: no treatment; ii: Pro-CQDs NPs 50 mg L−1; iii: Pro-CQDs NPs 100 mg L−1. (DOCX 662 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gohari, G., Panahirad, S., Sepehri, N. et al. Enhanced tolerance to salinity stress in grapevine plants through application of carbon quantum dots functionalized by proline. Environ Sci Pollut Res 28, 42877–42890 (2021). https://doi.org/10.1007/s11356-021-13794-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-13794-w

Keywords

Navigation