Elsevier

Scientia Horticulturae

Volume 285, 27 July 2021, 110170
Scientia Horticulturae

Glycine betaine mediated changes in growth, photosynthetic efficiency, antioxidant system, yield and quality of mustard

https://doi.org/10.1016/j.scienta.2021.110170Get rights and content

Highlights

  • Glycine betaine (GB) is a key osmoprotectant and regulates diverse processes in plants.

  • The osmoprotectant improved growth and physio-biochemical parameters.

  • GB enhanced the antioxidant system for scavenging reactive oxygen species.

  • Augmentation in yield and quality characteristics was noted in GB treated plants.

  • GB also improved histochemical and microscopical parameters.

Abstract

The present experiment was designed to assess the role of glycine betaine (GB) on growth, photosynthetic efficiency, antioxidant system, yield and quality of Brassica juncea L. cv. Pusa Agrani. Four graded concentrations of GB, i.e. 0, 10, 20 or 30 mM were applied as foliar spray at 50 and 70 days after sowing (DAS). The plants were sampled at 80 DAS to analyze growth, physio-biochemical, microscopical and histochemical parameters. Yield and quality parameters were analyzed at 120 DAS. The data revealed that the increasing levels of GB up to 20 mM enhanced growth characters, net photosynthetic rate and its associated attributes, carbonic anhydrase, GB content, proline content, nitrate reductase activity, antioxidant enzymes activities, carbohydrate content, potassium content and yield and quality parameters. Additionally, the graded levels of GB up to 20 mM modulated histochemical studies (superoxide anion and hydrogen peroxide (H2O2) generation) and microscopic studies (stomatal aperture, root cell viability and H2O2 production). No further improvement in various parameters was observed after 20 mM GB. However, proline and GB contents were found to be improved with GB in a concentration dependent manner. It may be concluded that two sprays of 20 mM GB proved to be the best for this crop.

Introduction

Glycine betaine (GB) is a well-known quaternary ammonium compound (zwitterion) naturally found in haemophilic archaebacterial, bacteria, marine invertebrates, plants and animals (Chen and Murata, 2002, 2008, 2011; Figueroa-Soto and Valenzuela-Soto, 2018) and was isolated first from Beta vulgaris (Scheibler et al. 1869). GB is an organic metabolite and its extreme water-solubility and low viscosity make it a key osmoregulatory (Fariduddin et al. 2013). Besides acting as an osmoprotectant, it stabilizes quaternary structure of proteins and enzymes, improves the antioxidant defense system, photosystem-II, reduces membrane permeability and H2O2 mediated signaling (Ma et al. 2007; Chen and Murata, 2011; Oukarroum et al. 2012; Tian et al. 2017; Annunziata et al. 2019; Ali et al. 2020; Huang et al. 2020). GB generally accumulates in the cytosol, plastids, chloroplast and mitochondria of many plant species and further its accumulation increases in response to stressful conditions (Ashraf and Foolad, 2007; Park et al. 2007; Ahmed et al. 2019). In plants, GB biosynthesis occurs via a two-step oxidation pathway of choline. The first step is catalyzed by choline monooxygenase (CMO) via the oxidation of choline to an intermediate betaine aldehyde. While the second oxidation step is mediated by a NAD(P)+ dependent betaine aldehyde dehydrogenase (BADH) enzyme (Xu et al. 2018; Ali et al. 2020). Amaranthaceae, Asteraceae, Malvaceae, Portulacaceae and Poaceae are among the naturally GB accumulating families (Ashraf and Foolad, 2007; Chen and Murata, 2011). However, GB accumulation varies considerably from species to species, and in tolerant genotypes generally it accumulates at higher level than the sensitive ones. Plants utilize exogenously applied GB and translocate it to almost all plant organs. This exogenous application enhances the level of GB in plants that are unable to synthesize it. Exogenously applied or transgenes generated GB can regulate the gene expression and trigger responses to abiotic stress conditions (Ashraf and Foolad, 2007; Chen and Murata, 2011; Giri, 2011). Previous reports showed that as an osmoprotectant, GB has the potential to improve the growth and physiology of plants under normal and stressful conditions. For example, exogenously applied GB promoted crop growth and improved plant water status, accumulation of proline, CO2 fixation, water use efficiency and stomatal conductance under normal and stressed conditions (Ather et al. 2015; Ahmad et al. 2020).

Indian mustard is the second important edible oilseed crop of India and supplies about 7% of worlds edible oil. However, its production is still insufficient to fulfil the daily needs of the people (Hayat et al. 2012). Several efforts have been made to enhance its productivity by utilizing the ‘treatment-response strategies”. Keeping this in view, the present experiment was designed to explore the optimal concentration of leaf-applied GB so that the full genetic potential of the crop could be exploited.

Section snippets

Plant material

The healthy seeds of Brassica juncea L. cv. Pusa Agrani were brought from the Indian Agricultural Research Institute, New Delhi. Prior to sowing these seeds were surface sterilized by mercuric chloride (0.01%) solution for about five minutes with continuous shaking accompanied by thorough rinsing with double distilled water (DDW) three to four times to remove the mercuric chloride from the seed coats.

Treatment preparation

The stock solution of GB was prepared by dissolving the desired amount of GB in 5 ml of DDW in

Effect of GB on growth attributes

The data (Fig. 1A-G) showed that root length (RL), shoot length (SL), root fresh mass (RFM), shoot fresh mass (SFM), root dry mass (RDM), shoot dry mass (SDM) and APL were found to be increased by the foliar application of GB. The spray application of 30 mM GB gave the maximum values but its effect was statistically similar with that of 20 mM GB. The application of 20 mM GB increased RL by 12.2%, SL by 11.79%, RFM by 12.5%, RDM by 11.26%, SFM by 13.39%, SDM by 13.40% per plant and APL by 14.73%

Discussion

GB regulates diverse metabolic processes in plants under normal and myriad conditions (Ather at al., 2015). The present experiment was performed to improve the understanding of effect of GB on the performance of Indian mustard by undertaking growth, physio-biochemical, histochemical, microscopical, yield and quality analyses (Fig 1-8). The data (Fig. 1A-B, G) revealed that the GB-treated plants showed a beneficial effect on RL, SL and APL. Such improvement in these characters could be ascribed

Conclusion

The present study revealed that the foliar spray of GB enhanced the overall performance of the oilseed crop. Foliar spray of 20 mM GB proved beneficial for most of the parameters studied and this was further supported by the histochemical and confocal microscopic studies. The effects of 30 mM GB on most parameters were found to be at par with that of 20 mM GB. However, proline and GB contents were found to be increased with the foliar spray of GB in a concentration dependent manner. The foliar

Author(s) contribution

SI performed the experiment, analyzed the data and wrote the article.

ZAP and SHS helped in histochemical and microscopic studies as also in the preparation of histogram.

FM designed and supervised the experiment as well as guided the preparation of manuscript.

Declaration of Competing Interest

The authors declare that no conflict of interest exists.

Acknowledgements

SI, ZAP and SHS are thankful to UGC New Delhi, India for providing the Non-Net Fellowship. The authors are also grateful to the University Sophisticated Instrumentation Facility (USIF) AMU, Aligarh for carrying out the confocal and SEM analyses.

References (60)

  • C.G. Figueroa-Soto et al.

    Glycine betaine rather than acting only as an osmolyte also plays a role as regulator in cellular metabolism

    Biochimie

    (2018)
  • C.H. Fiske et al.

    The colorimetric determination of phosphorus

    J. Biol. Chem.

    (1925)
  • S. Hayat et al.

    Comparative effect of 28 homobrassinolide and salicylic acid in the amelioration of NaCl stress in Brassica juncea L

    Plant Physiol. Biochem.

    (2012)
  • R.L. Heath et al.

    Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation

    Arch. Biochem. Biophys.

    (1968)
  • E.G. Jaworski

    Nitrate reductase assay in intact plant tissues

    Biochem. Biophys. Res. Commun.

    (1971)
  • Y. Kono

    Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase

    Arch. Biochem. Biophys.

    (1978)
  • M.O. Rady et al.

    Up-regulation of antioxidative defense systems by glycine betaine foliar application in onion plants confer tolerance to salinity stress

    Sci. Hort.

    (2018)
  • S.H. Raza et al.

    Glycinebetaine-induced modulation of antioxidant enzymes activities and ion accumulation in two wheat cultivars differing in salt tolerance

    Environ. Exp. Bot.

    (2007)
  • F. Tian et al.

    Over accumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress

    Crop J

    (2017)
  • V. Velikova et al.

    Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines

    Plant Sci

    (2000)
  • G.L. Wu et al.

    Fluroxypyr triggers oxidative damage by producing superoxide and hydrogen peroxide in rice (Oryza sativa)

    Ecotoxicology

    (2010)
  • T. Aftab et al.

    Stimulation of crop productivity, photosynthesis and artemisinin production in Artemisia annua L. by triacontanol and gibberellic acid application

    J. Plant Interact.

    (2010)
  • R. Ahmad et al.

    Glycine betaine alleviates the chromium toxicity in Brassica oleracea L. by suppressing oxidative stress and modulating the plant morphology and photosynthetic attributes

    Environ. Sci. Pollut. Res.

    (2020)
  • F. Alasvandyari et al.

    Effect of glycinebetaine on growth and antioxidant enzymes of safflower under salinity stress condition

    Agric. For.

    (2017)
  • F. Alasvandyari et al.

    Glycinebetaine affects the antioxidant system and ion accumulation and reduces salinity-induced damage in safflower seedlings

    Arch. Biol. Sci.

    (2017)
  • S. Ali et al.

    Glycine Betaine Accumulation, Significance and Interests for Heavy Metal Tolerance in Plants

    Plants

    (2020)
  • M.G. Annunziata et al.

    Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses

    Front. Plant Sci.

    (2019)
  • H.U.R. Athar et al.

    Inducing salt tolerance in canola (Brassica napus L.) by exogenous application of glycinebetaine and proline: response at the initial growth stages

    Pak. J. Bot.

    (2009)
  • H.U.R. Athar et al.

    Glycinebetaine improved photosynthesis in canola under salt stress: evaluation of chlorophyll fluorescence parameters as potential indicators

    J. Agron. Crop Sci.

    (2015)
  • L.S. Bates et al.

    Rapid determination of free proline for water-stress studies

    Plant soil

    (1973)
  • Cited by (26)

    • Auxin regulates growth, photosynthetic efficiency and mitigates copper induced toxicity via modulation of nutrient status, sugar metabolism and antioxidant potential in Brassica juncea

      2022, Plant Physiology and Biochemistry
      Citation Excerpt :

      Cu stress limits the CA activity in plants (Table 5) seemingly due to its intervention with the organization and permeability of plasma membrane. However, limited uptake of zinc ion essential for the activity of CA (Islam et al., 2021; Alatawi et al., 2022). In contrast, IAA application blocks the Cu-induced decline and enhanced CA activity, compared to the control.

    • Modulation of growth, photosynthetic efficiency, leaf biochemistry, cell viability and yield of Indian mustard by the application of trehalose

      2021, Scientia Horticulturae
      Citation Excerpt :

      More importantly, the ameliorative effect of Tre on NR activity (Fig. 3C) is self-explanatory. NR is a key enzyme for conversion of nitrate into nitrite to maintain a sufficient supply of nitrogen in plants (Islam and Mohammad, 2020; Mushtaq et al. 2020; Islam et al. 2021). In the present study, the Tre treated plants had an enhanced leaf NR activity compared with the water-sprayed control (Fig. 3C).

    View all citing articles on Scopus
    View full text