Skip to main content

Advertisement

SpringerLink
Log in

Enhanced growth and stress tolerance in Barley (Hordeum vulgare) through biopriming with Aspergillus niger CSR3: a promising approach for sustainable agriculture in saline environments

  • Original Paper
  • Published:
Cereal Research Communications Aims and scope Submit manuscript

Abstract

Barley (Hordeum vulgare) is the fourth largest cereal crop in the world, with considerable nutritional value. Recently more studies on the toleration of barley to salt stress have been published, indicating an increased concern for food safety. Salt stress is an increasing threat to agricultural productivity; thus, an attempt was made to explore the growth-promoting capacities of an endophytic fungal strain Aspergillus niger CSR3 in H. vulgare. In the current study, we investigated various physiological and biochemical characteristics of two H. vulgare varieties, namely OM-80 and OM-82, under 300 mM NaCl and 100% seawater treatments with and without the inoculation of CSR3. Our results showed that biopriming of H. vulgare seeds with CSR3 enhanced germination ratio both in control and salt treated conditions. Under salt stress, the growth of H. vulgare plants was significantly reduced; however, CSR3 alleviated the salt stress and significantly increased root/shoot length and weight compared to their respective counterparts both under control and stress conditions. The fungal strain showed an ameliorated response to salt stress by improving the photosynthetic machinery. Results demonstrate that accumulation of reduced glutathione (GSH), catalase (CAT), and flavonoids decreased in inoculated plants as compared to non-inoculated under saline conditions indicating the potential of CSR3 in maintaining cellular homeostasis against salinity stress. Moreover, our finding also revealed that starch accumulation decreased with a gradual increase of salt treatment; however, CSR3 inoculation enhanced starch and decreased sugar level, indicating its potential to convert excess sugar to starch. In conclusion, CSR3 can improve plant performance significantly and can greatly improve sustainable agricultural production in saline marginal lands.

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

Data availability

Not applicable.

References

  • Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5:369–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmad P, Jaleel CA, Azooz M, Nabi G (2009) Generation of ROS and non-enzymatic antioxidants during abiotic stress in plants. Bot Res Int 2:11–20

    CAS  Google Scholar 

  • Ahmadi A, Baker DA (2001) The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat. Plant Growth Regul 35:81–91

    Article  CAS  Google Scholar 

  • Aizaz M, Ahmad W, Asaf S, Khan I, Saad Jan S, Salim Alamri S, Bilal S, Jan R, Kim K-M, Al-Harrasi A (2023) Characterization of the seed biopriming, plant growth-promoting and salinity-ameliorating potential of halophilic fungi isolated from hypersaline habitats. Int J Mol Sci 24:4904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arulsekar S, Parfitt DE (1986) Isozyme analysis procedures for stone fruits, almond, grape, walnut, pistachio, and fig. HortScience 21(4):928–933

  • Araújo VC, Rossati KF, Xavier LV, De Oliveira VA, Dos Santos Carmo GJ, De Assis GA, De Oliveira Mendes G (2020) Enhanced growth in nursery of coffee seedlings inoculated with the rhizosphere fungus Aspergillus niger for field transplantation. Rhizosphere 15:100236

    Article  Google Scholar 

  • Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S (2020) Salinity induced physiological and biochemical changes in plants: an omic approach towards salt stress tolerance. Plant Physiol Biochem 156:64–77

    Article  CAS  PubMed  Google Scholar 

  • Arzu K, Onder O, Bilir O, Kosar F (2018) Application of multivariate statistical analysis for breeding strategies of spring safflower (Carthamus tinctorius L.). Turk J Field Crops 23:12–19

    Article  Google Scholar 

  • Asaf S, Jan R, Khan MA, Khan AL, Asif S, Bilal S, Ahmad W, Waqas M, Kim K-M, Ahmed A-H (2023a) Unraveling the mutualistic interaction between endophytic Curvularia lunata CSL1 and tomato to mitigate cadmium (Cd) toxicity via transcriptomic insights. Sci Total Environ 861:160542

    Article  CAS  PubMed  Google Scholar 

  • Asaf S, Jan R, Khan MA, Lubna, Khan AL, Asif S, Bilal S, Ahmad W, Waqas M, Kim K-M, Al-Harrasi A, Lee I-J (2023b) Unraveling the mutualistic interaction between endophytic Curvularia lunata CSL1 and tomato to mitigate cadmium (Cd) toxicity via transcriptomic insights. Sci Total Environ 861:160542

    Article  CAS  PubMed  Google Scholar 

  • Attia MS, Hashem AH, Badawy AA, Abdelaziz AM (2022) Biocontrol of early blight disease of eggplant using endophytic Aspergillus terreus: improving plant immunological, physiological and antifungal activities. Bot Stud 63:26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Auten RL, Davis JM (2009) Oxygen toxicity and reactive oxygen species: the devil is in the details. Pediatr Res 66:121–127

    Article  CAS  PubMed  Google Scholar 

  • Badea A, Wijekoon C (2021) Benefits of barley grain in animal and human diets. In: Goyal AK (ed) Cereal grains-volume 1. IntechOpen, London

    Google Scholar 

  • Bamisile BS, Siddiqui JA, Akutse KS, Ramos Aguila LC, Xu Y (2021) General limitations to endophytic entomopathogenic fungi use as plant growth promoters, pests and pathogens biocontrol agents. Plants 10:2119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ Exp Bot 32:85–100

    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 

  • Canellas LP, Olivares FL (2014) Physiological responses to humic substances as plant growth promoter. Chem Biol Technol Agric 1:1–11

    Article  Google Scholar 

  • Dkhil BB, Denden M (2010) Salt stress induced changes in germination, sugars, starch and enzyme of carbohydrate metabolism in Abelmoschus esculentus L. (Moench.) seeds. Afr J Agric Res 5:1412–1418

    Google Scholar 

  • Egamberdieva D, Alimov J, Shurigin V, Alaylar B, Wirth S, Bellingrath-Kimura SD (2021) Diversity and plant growth-promoting ability of endophytic, halotolerant bacteria associated with Tetragonia tetragonioides (Pall.) Kuntze. Plants 11:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  PubMed  Google Scholar 

  • Elsawy HIA, Mekawy AMM, Elhity MA, Abdel-Dayem SM, Abdelaziz MN, Assaha DVM, Ueda A, Saneoka H (2018) Differential responses of two Egyptian barley (Hordeum vulgare L.) cultivars to salt stress. Plant Physiol Biochem 127:425–435

    Article  CAS  PubMed  Google Scholar 

  • Errasquın EL, Vazquez C (2003) Tolerance and uptake of heavy metals by Trichoderma atroviride isolated from sludge. Chemosphere 50:137–143

    Article  Google Scholar 

  • Gujar PD, Bhavsar KP, Khire JM (2013) Effect of phytase from Aspergillus niger on plant growth and mineral assimilation in wheat (Triticum aestivum Linn.) and its potential for use as a soil amendment. J Sci Food Agric 93:2242–2247

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Schillaci M, Walker R, Smith PMC, Watt M, Roessner U (2021) Alleviation of salinity stress in plants by endophytic plant-fungal symbiosis: current knowledge, perspectives and future directions. Plant Soil 461:219–244

    Article  CAS  Google Scholar 

  • Gupta A, Singh AN, Tiwari RK, Sahu PK, Yadav J, Srivastava AK, Kumar S (2023) Salinity alleviation and reduction in oxidative stress by endophytic and rhizospheric microbes in two rice cultivars. Plants 12:976

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Alam MM, Rahman A, Hasanuzzaman M, Nahar K, Fujita M (2014) Exogenous proline and glycine betaine mediated upregulation of antioxidant defense and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. BioMed Res Int 2014:757219

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang R-D (2018) Research progress on plant tolerance to soil salinity and alkalinity in sorghum. J Integr Agric 17:739–746

    Article  CAS  Google Scholar 

  • Hung R, Rutgers SL (2016) Applications of Aspergillus in plant growth promotion. In: Kostas M (ed) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp 223–227

  • Ismail MA, Amin MA, Eid AM, Hassan SE-D, Mahgoub HA, Lashin I, Abdelwahab AT, Azab E, Gobouri AA, Elkelish A (2021) Comparative study between exogenously applied plant growth hormones versus metabolites of microbial endophytes as plant growth-promoting for Phaseolus vulgaris L. Cells 10:1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaeger A, Zannini E, Sahin AW, Arendt EK (2021) Barley protein properties, extraction and applications, with a focus on brewers’ spent grain protein. Foods 10:1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jhuma TA, Rafeya J, Sultana S, Rahman MT, Karim MM (2021) Isolation of endophytic salt-tolerant plant growth-promoting rhizobacteria from Oryza sativa and evaluation of their plant growth-promoting traits under salinity stress condition. Front Sustain Food Syst 5:687531

    Article  Google Scholar 

  • Khan M, Panda S (2008) Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl-salinity stress. Acta Physiol Plant 30:81–89

    Article  CAS  Google Scholar 

  • Khan AL, Hamayun M, Ahmad N, Hussain J, Kang S-M, Kim Y-H, Adnan M, Tang D-S, Waqas M, Radhakrishnan R (2011) Salinity stress resistance offered by endophytic fungal interaction between Penicillium minioluteum LHL09 and Glycine max L. J Microbiol Biotechnol 21:893–902

    Article  CAS  PubMed  Google Scholar 

  • Khan MA, Asaf S, Khan AL, Jan R, Kang SM, Kim KM, Lee IJ (2020) Extending thermotolerance to tomato seedlings by inoculation with SA1 isolate of Bacillus cereus and comparison with exogenous humic acid application. PLoS ONE 15:e0232228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan I, Khan S, Zhang Y, Zhou J, Akhoundian M, Jan SA (2021a) CRISPR-Cas technology based genome editing for modification of salinity stress tolerance responses in rice (Oryza sativa L.). Mol Biol Rep 48:3605–3615

    Article  CAS  PubMed  Google Scholar 

  • Khan MA, Sahile AA, Jan R, Asaf S, Hamayun M, Imran M, Adhikari A, Kang S-M, Kim K-M, Lee I-J (2021b) Halotolerant bacteria mitigate the effects of salinity stress on soybean growth by regulating secondary metabolites and molecular responses. BMC Plant Biol 21:176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan I, Zhang Y, Akbar F, Khan J (2022) Abiotic stress tolerance in cereals through genome editing. In: Roychoudhury A, Aftab T, Acharya K (eds) Omics approach to manage abiotic stress in cereals. Springer, Singapore, pp 295–319

    Chapter  Google Scholar 

  • Kumar A, Verma JP (2018) Does plant—microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Xun W, Chen L, Xu Z, Zhang N, Feng H, Zhang Q, Zhang R (2022) Rhizosphere microbes enhance plant salt tolerance: toward crop production in saline soil. Comput Struct Biotechnol J 20:6543–6551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubna, Asaf S, Hamayun M, Gul H, Lee I-J, Hussain A (2018a) Aspergillus niger CSR3 regulates plant endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic acid. J Plant Interact 13:100–111

    Article  CAS  Google Scholar 

  • Lubna, Asaf S, Hamayun M, Khan AL, Waqas M, Khan MA, Jan R, Lee I-J, Hussain A (2018b) Salt tolerance of Glycine max L. induced by endophytic fungus Aspergillus flavus CSH1, via regulating its endogenous hormones and antioxidative system. Plant Physiol Biochem 128:13–23

    Article  CAS  PubMed  Google Scholar 

  • Lubna, Asaf S, Jan R, Khan AL, Bilal S, Asif S, Al-Harrasi A, Kim K-M (2022) Unraveling the genome sequence of plant growth promoting Aspergillus niger (CSR3) provides insight into the synthesis of secondary metabolites and its comparative genomics. J Fungi 8:107

    Article  CAS  Google Scholar 

  • Lushchak VI (2014) Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact 224:164–175

    Article  CAS  PubMed  Google Scholar 

  • Meng F, Luo Q, Wang Q, Zhang X, Qi Z, Xu F, Lei X, Cao Y, Chow WS, Sun G (2016) Physiological and proteomic responses to salt stress in chloroplasts of diploid and tetraploid black locust (Robinia pseudoacacia L.). Sci Rep 6:1–15

    Google Scholar 

  • Mishra AK, Das R, George Kerry R, Biswal B, Sinha T, Sharma S, Arora P, Kumar M (2023) Promising management strategies to improve crop sustainability and to amend soil salinity. Front Environ Sci 10:962581

    Article  Google Scholar 

  • Newton AC, Flavell AJ, George TS, Leat P, Mullholland B, Ramsay L, Revoredo-Giha C, Russell J, Steffenson BJ, Swanston JS, Thomas WTB, Waugh R, White PJ, Bingham IJ (2011) Crops that feed the world 4. Barley: a resilient crop? Strengths and weaknesses in the context of food security. Food Secur 3:141–178

    Article  Google Scholar 

  • Park Y-S, Jung S-T, Kang S-G, Heo BG, Arancibia-Avila P, Toledo F, Drzewiecki J, Namiesnik J, Gorinstein S (2008) Antioxidants and proteins in ethylene-treated kiwifruits. Food Chem 107:640–648

    Article  CAS  Google Scholar 

  • Salih G, Jilal A, Garcia MS, Visioni A (2022) L’orge alimentaire en Afrique du nord: etat des connaissances et opportunités de développement. Afr Mediterr Agric J Al Awamia 137:41–64

    Google Scholar 

  • Sarker U, Oba S (2018) Drought stress effects on growth, ROS markers, compatible solutes, phenolics, flavonoids, and antioxidant activity in Amaranthus tricolor. Appl Biochem Biotechnol 186:999–1016

    Article  CAS  PubMed  Google Scholar 

  • Schulte D, Close TJ, Graner A, Langridge P, Matsumoto T, Muehlbauer G, Sato K, Schulman AH, Waugh R, Wise RP, Stein N (2009) The international Barley sequencing consortium—at the threshold of efficient access to the Barley genome. Plant Physiol 149:142–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuster E, Dunn-Coleman N, Frisvad J, Van Dijck P (2002) On the safety of Aspergillus niger—a review. Appl Microbiol Biotechnol 59:426–435

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Lou K, Li C (2010) Growth and photosynthetic efficiency promotion of sugar beet (Beta vulgaris L.) by endophytic bacteria. Photosynth Res 105:5–13

    Article  CAS  PubMed  Google Scholar 

  • Vaishnav A, Shukla AK, Sharma A, Kumar R, Choudhary DK (2019) Endophytic bacteria in plant salt stress tolerance: current and future prospects. J Plant Growth Regul 38:650–668

    Article  CAS  Google Scholar 

  • Verma T, Bhardwaj S, Singh J, Kapoor D, Prasad R (2022) Triacontanol as a versatile plant growth regulator in overcoming negative effects of salt stress. J Agric Food Res 10:100351

    CAS  Google Scholar 

  • Waqas M, Khan AL, Kamran M, Hamayun M, Kang S-M, Kim Y-H, Lee I-J (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Zhao H, Zhao X, Xu X, Di Y, Jiang C, Shi J, Shao D, Huang Q, Yang H (2018) Production of bioproducts by endophytic fungi: chemical ecology, biotechnological applications, bottlenecks, and solutions. Appl Microbiol Biotechnol 102:6279–6298

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Chen J, Ma Y, Huang M, Qiu T, Bian H, Han N, Wang J (2022) Function, mechanism, and application of plant melatonin: An update with a focus on the cereal crop, barley (Hordeum vulgare L.). Antioxidants 11:634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zavřel T, Očenášová P, Sinetova MA, Červený J (2018) Determination of storage (starch/glycogen) and total saccharides content in algae and cyanobacteria by a phenol-sulfuric acid method. Bio-Protoc 8:e2966–e2966

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Ministry of Higher Education, Research & Innovation and the Ministry of Agriculture, Fisheries & Water Resources under the project (MoHERI/SRPP/MoAFWR/1/2022/RI/01). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Author notes

  1. Ibrahim Khan and Lubna have equally contributed to this work.

Authors and Affiliations

  1. Natural and Medical Sciences Research Center, University of Nizwa, 616, Nizwa, Oman

    Ibrahim Khan,  Lubna, Sajjad Asaf, Saqib Bilal, Safiya Salim Alamri & Ahmed AL-Harrasi

  2. Department of Applied Biosciences, Kyungpook National University, Daegu, 41566, Republic of Korea

    Rahmatullah Jan, Saleem Asif & Kyung-Min Kim

Authors
  1. Ibrahim Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lubna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sajjad Asaf
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Saqib Bilal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Safiya Salim Alamri
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rahmatullah Jan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Saleem Asif
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kyung-Min Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ahmed AL-Harrasi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

IK, L, SSA, and SA performed experimental and analysis. RJ, SA, and SB performed antioxidant analysis and wrote the draft manuscript and statistical analysis. K-MK and AA-H, supervision and arranging resources.

Corresponding author

Correspondence to Sajjad Asaf.

Ethics declarations

Ethical approval

Not applicable.

Informed consent

Not applicable.

Additional information

Communicated by Katalin Posta.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 19 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, I., Lubna, Asaf, S. et al. Enhanced growth and stress tolerance in Barley (Hordeum vulgare) through biopriming with Aspergillus niger CSR3: a promising approach for sustainable agriculture in saline environments. CEREAL RESEARCH COMMUNICATIONS (2023). https://doi.org/10.1007/s42976-023-00456-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s42976-023-00456-5

Keywords

Search

Navigation