Skip to main content

Advertisement

SpringerLink
Log in

Alleviation of salt stress in Triticum aestivum by biopriming with Phanerochaete chrysosporium

  • Original Research
  • Published:
Journal of Crop Science and Biotechnology Aims and scope Submit manuscript

Abstract

Wheat is one of the most important cereals, vital basic crop in Egypt, covering approximately 32.6% of the total winter land. However, sensitivity to abiotic stress especially salinity is one the major current hurdles that reduce the global yield of this crop. Plant biopriming with fungi is the recent technology that might alleviate the salt stress effect. Thus, the objective of this work was to examine the effect of Triticum aestivum grains biopriming with Phanerochaete chrysosporium on the response of wheat to salt stress. From the physiological and biochemical parameters, biopriming of wheat grains with P. chrysosporium significantly alleviates the salt stress and markedly increases the growth parameters, photosynthetic pigments and osmolytes (soluble sugars, soluble protein and proline) contents. In addition, it alleviates the oxidative damage, as indicated by the lower accumulation of malondealdehyde and increasing the activity of antioxidant enzymes; superoxide dismutase, catalase, and ascorbate peroxidase in wheat seedlings. Results indicate the potential of using P. chrysosporium biopriming for reducing the deteriorating effects of salinity.

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abdelgawad H, Zinta G, Hegab MM, Pandey R, Asard H et al (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci 7:276

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aebi HE (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie, Weinhem, pp 273–286

    Google Scholar 

  • Afzal I, Rauf S, Basra S, Murtaza G (2008) Halopriming improves vigor, metabolism of reserves and ionic contents in wheat seedlings under salt stress. Plant Soil Environ 54:382–388

    CAS  Google Scholar 

  • Afzal I, Rehman HU, Naveed M, Basra SMA (2016) Recent advances in seed enhancements. In: New challenges in seed biology-basic and translational research driving seed technology (InTech)

  • Agarwal N, Kumar A, Agarwal S, Singh A (2015) Evaluation of soybean (Glycine max L.) cultivars under salinity stress during early vegetative growth. Int J Curr Microbiol Appl Sci 4:123–134

    CAS  Google Scholar 

  • Ahmad P, Abdel Latef AA, Hashem A, Abd Allah EF, Gucel S et al (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347

    PubMed  PubMed Central  Google Scholar 

  • Ali GS, Norman D, El-Sayed ASA (2015) Soluble and volatile metabolites of plant growth-promoting Rhizobacteria (PGPRs): role and practical applications in inhibiting pathogens and activating Induced Systemic Resistance (ISR). Adv Bot Res 75:241–284

    Google Scholar 

  • Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS et al (2015) Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121

    CAS  Google Scholar 

  • Aust SD (1990) Degradation of environmental pollutants byPhanerochaete chrysosporium. Microb Ecol 20:197–209

    CAS  PubMed  Google Scholar 

  • Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B et al (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510

    CAS  PubMed  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    CAS  Google Scholar 

  • Basra SMA, Zia MN, Mehmood T, Afzal I, Khaliq A (2002) Comparison of different invigoration techniques in wheat (Triticum aestivum L.) seeds. Pak J Arid Agric 5:11–16

    Google Scholar 

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

    CAS  Google Scholar 

  • Batool N, Shahzad A, Ilyas N, Noor T (2014) Plants and salt stress. Int J Agric Crop Sci 7:582

    CAS  Google Scholar 

  • Bernstein N (2013) Effects of salinity on root growth. In: Eshel A, Beeckman T (eds) Plant roots: the hidden half, 4th edn. CRC Press, Boca Raton, FL, p 848. https://doi.org/10.1201/b14550-42

    Chapter  Google Scholar 

  • Cardona R, Rodriguez H (2006) Effects of Trichoderma harzianum fungus on the incidence of the charcoal rot disease on sesame. Rev Fac Agron 23:44–50

    Google Scholar 

  • Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. In Abiotic stress in plants-mechanisms and adaptations (Intech)

  • Chakraborty K, Singh A, Bhaduri D, Sairam R (2013) Mechanism of salinity stress tolerance in crop plants and recent developments. Adv Plant Physiol 14:466–496

    Google Scholar 

  • Chaparzadeh N, Hosseinzad-Behboud E (2015) Evidence for enhancement of salinity induced oxidative damages by salicylic acid in radish (Raphanus sativus L.). J Plant Physiol Breed 5:23–33

    Google Scholar 

  • Chinnusamy V, Jagendorf A, Zhu J-K (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

    CAS  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Google Scholar 

  • De Zelicourt A, Al-Yousif M, Hirt H (2013) Rhizosphere microbes as essential partners for plant stress tolerance. Mol Plant 6:242–245

    PubMed  Google Scholar 

  • Debbarma M, Priyadarshinee Das S (2017) Priming of seed: enhancing growth and development. Int J Curr Microbiol Appl Sci 6:2390–2396

    Google Scholar 

  • Dey P (1990) Oligosaccharides. Carbohydrates. Methods Plant Biochem 2:189–218

    CAS  Google Scholar 

  • Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U (2006) Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant Soil 284:363–373

    CAS  Google Scholar 

  • Durmus N, Yesilyurt AM, Pehlivan N, Karaoglu SA (2017) Salt stress resilience potential of a fungal inoculant isolated from tea cultivation area in maize. Biologia 72:619–627

    CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinf 5:113

    Google Scholar 

  • Elavarthi S, Martin B (2010) Spectrophotometric assays for antioxidant enzymes. In: Plants in plant stress tolerance. Springer, Berlin, pp 273–280

    Google Scholar 

  • El-Hendawy SE-S (2004) Salinity tolerance in Egyptian spring wheat genotypes. Technische Universität München, Universitätsbibliothek

    Google Scholar 

  • El-Sayed ASA, Ali GS (2020) Aspergillus flavipes is a novel efficient biocontrol agent of Phytophthora parasiticus. Biol Control 140:104072

    CAS  Google Scholar 

  • El-Sayed ASA, Shindia AA (2011) Characterization and immobilization of purified Aspergillus flavipesl-methioninase: continuous production of methanethiol. J Appl Microbiol 111:54–69

    CAS  PubMed  Google Scholar 

  • El-Sayed ASA, Hassan MN, Nada HMS (2015a) Purification, immobilization, and biochemical characterization of L-arginine deiminase from thermophilic Aspergillus fumigatus KJ434941: anticancer activity in vitro. Biotechnol Progress 31(2):396–405

    CAS  Google Scholar 

  • El-Sayed ASA, Yassin MA, Ali GS (2015b) Transcriptional and proteomic profiling of Aspergillus flavipes in response to sulfur starvation. PLoS ONE 10:e0144304

    PubMed  PubMed Central  Google Scholar 

  • El-Sayed ASA, Abdel-Ghany SE, Ali GS (2017a) Genome editing approaches: manipulating of lovastatin and taxol synthesis of filamentous fungi by CRISPR/Cas9 system. Appl Microbiol Biotechnol 101:3953–3976

    CAS  PubMed  Google Scholar 

  • El-Sayed ASA, Ruff L, Ghany SA, Ali GS, Esener E (2017b) Molecular and spectroscopic characterization of Aspergillus flavipes and Pseudomonas putidaL-Methionine γ-Lyase in vitro. Appl Biochem Biotechnol 181:1513–1532

    CAS  PubMed  Google Scholar 

  • El-Sayed ASA, Safan S, Mohamed NZ, Shaban L, Ali GS, Sitohy MZ (2018a) Induction of Taxol biosynthesis by Aspergillus terreus, endophyte of Podocarpus gracilior Pilger, upon intimate interaction with the plant endogenous microbes. Process Biochem 71:31–40

    CAS  Google Scholar 

  • El-Sayed ASA, Akbar A, Iqrar I, Ali R, Norman D, Brennan M, Ali GS (2018b) A glucanolytic Pseudomonas sp. associated with Smilax bona-nox L. displays strong activity against Phytophthora parasitica. Microbiol Res 207:140–152

    CAS  PubMed  Google Scholar 

  • El-Sayed ASA, Ali DMI, Yassin MA, Zayed RA, Ali GS (2019a) Sterol inhibitor “Fluconazole” enhance the Taxol yield and molecular expression of its encoding genes cluster from Aspergillus flavipes. Process Biochem 76:55–67

    CAS  Google Scholar 

  • El-Sayed ASA, Mohamed NZ, Safan S, Yassin MA, Shaban L, Shindia AA et al (2019b) Restoring the Taxol biosynthetic machinery of Aspergillus terreus by Podocarpus gracilior Pilger microbiome, with retrieving the ribosome biogenesis proteins of WD40 superfamily. Sci Rep 9:11534

    PubMed  PubMed Central  Google Scholar 

  • El-Sayed ASA, Shindia AA, Abou Zaid AA, Yassin AM, Shad Ali G, Sitohy MZ (2019c) Biochemical characterization of peptidylarginine deiminase like orthologs from thermotolerant Emericella dentata and Aspergillus nidulans. Enzyme Microb Technol. 124:41–53

    CAS  PubMed  Google Scholar 

  • Farooq M, Basra S, Afzal I, Khaliq A (2006) Optimization of hydropriming techniques for rice seed invigoration. Seed Sci Technol 34:507–512

    Google Scholar 

  • Gallego-Giraldo L, Jikumaru Y, Kamiya Y, Tang Y, Dixon RA (2011) Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). New Phytol 190:627–639

    CAS  PubMed  Google Scholar 

  • Gheyi H, Dias NDS, Lacerda CD, Gomes Filho E (2016) Physiology and biochemistry of plants growing under salt stress. Manejo da salinidade na agricultura: Estudos básicos e aplicados ISBN 978-85-420-0948-4

  • Ghezal N, Rinez I, Sbai H, Saad I, Farooq M et al (2016) Improvement of Pisum sativum salt stress tolerance by bio-priming their seeds using Typha angustifolia leaves aqueous extract. South Afr J Botany 105:240–250

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genom 1:701596

    Google Scholar 

  • Hasanuzzaman M, Nahar K, Rahman A, Anee TI, Alam MU, Bhuiyan TF, Oku H, Fujita M (2017) Approaches to enhance salt stress tolerance in wheat. In: Wanyera R, Owuoche J (eds) Wheat improvement, management and utilization. IntechOpen. https://doi.org/10.5772/67247.

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  PubMed  Google Scholar 

  • Heydecker W, Higgins J, Gulliver R (1973) Accelerated germination by osmotic seed treatment. Nature 246:42

    CAS  Google Scholar 

  • Iqbal N, Umar S, Khan NA, Iqbal M, Khan R (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42

    CAS  Google Scholar 

  • Jamil M, Bashir S, Anwar S, Bibi S, Bangash A et al (2012) Effect of salinity on physiological and biochemical characteristics of different varieties of rice. Pak J Bot 44:7–13

    CAS  Google Scholar 

  • Kapoor N, Pande V (2015) Effect of salt stress on growth parameters, moisture content, relative water content and photosynthetic pigments of fenugreek variety RMt-1. J Plant Sci 10:210–221

    CAS  Google Scholar 

  • Kebeish R, El-Sayed ASA, Fahmy H, Abdel-Ghany A (2016) Molecular cloning, biochemical characterization, and antitumor properties of a novel L-asparaginase from Synechococcus elongatus PCC6803. Biochemistry (Moscow) 81:1173–1181

    CAS  Google Scholar 

  • Khomari S, Davari M (2017) Trichoderma-induced enhancement of soybean seedling performance in response to salt stress. J Plant Physiol Breed 7:27–39

    Google Scholar 

  • Khosravinejad F, Heydari R, Farboodnia T (2008) Effects of salinity on photosynthetic pigments, respiration, and water content in two barley varieties. Pak J Biol Sci 11:2438–2442

    CAS  PubMed  Google Scholar 

  • Kumar D, Al Hassan M, Naranjo MA, Agrawal V, Boscaiu M et al (2017) Effects of salinity and drought on growth, ionic relations, compatible solutes and activation of antioxidant systems in oleander (Nerium oleander L.). PLoS ONE 12:e0185017

    PubMed  PubMed Central  Google Scholar 

  • Lata R, Chowdhury S, Gond SK, White JF Jr (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66:268–276

    CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Lutts S, Benincasa P, Wojtyla L, Kubala S, Pace R, Lechowska K, Quinet M, Garnczarska M (2016) Seed priming: new comprehensive approaches for an old empirical technique. In: New challenges in seed biology-basic and translational research driving seed technology, susana araujo and alma balestrazzi, IntechOpen. https://doi.org/10.5772/64420

  • Machado R, Serralheiro R (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3:30

    Google Scholar 

  • Maha A, Sanaa I, Mabrook Y, Amira Y, Gouda M (2017) Evaluation of some egyptian bread wheat (Triticum aestivum) cultivars under salinity stress. Alex Sci Exch J 38:260

    Google Scholar 

  • Milošević NA, Marinković JB, Tintor BB (2012) Mitigating abiotic stress in crop plants by microorganisms. Zbornik Matice srpske za prirodne nauke 2012:17–26

    Google Scholar 

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

    CAS  Google Scholar 

  • Nawaz K, Hussain K, Majeed A, Khan F, Afghan S et al (2010) Fatality of salt stress to plants: Morphological, physiological and biochemical aspects. Afr J Biotechnol 9:5475–5480

    CAS  Google Scholar 

  • Pang C-H, Wang B-S (2008) Oxidative stress and salt tolerance in plants. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in botany. Springer, Heidelberg, pp 231–245

    Google Scholar 

  • Prasad SR, Kamble UR, Sripathy K, Bhaskar KU, Singh D (2016) Seed bio-priming for biotic and abiotic stress management. In: Microbial inoculants in sustainable agricultural productivity. Springer, Berlin, pp 211–228

    Google Scholar 

  • Rasool S, Hameed A, Azooz M, Siddiqi T, Ahmad P (2013) Salt stress: causes, types and responses of plants. In: Ecophysiology and responses of plants under salt stress. Springer, Berlin, pp 1–24

    Google Scholar 

  • Rawat L, Singh Y, Shukla N, Kumar J (2011) Alleviation of the adverse effects of salinity stress in wheat (Triticum aestivum L.) by seed biopriming with salinity tolerant isolates of Trichoderma harzianum. Plant Soil 347:387

    CAS  Google Scholar 

  • Rawat L, Singh Y, Shukla N, Kumar J (2012) Seed biopriming with salinity tolerant isolates of Trichoderma harzianum alleviates salt stress in rice: growth, physiological and biochemical characteristics. J Plant Pathol 94:353–365

    Google Scholar 

  • Sami F, Yusuf M, Faizan M, Faraz A, Hayat S (2016) Role of sugars under abiotic stress. Plant Physiol Biochem 109:54–61

    CAS  PubMed  Google Scholar 

  • Sánchez-Calderón L, Ibarra-Cortés M, Zepeda-Jazo I (2013) Root development and abiotic stress adaptation. In: Abiotic stress-plant responses and applications in agriculture. Kourosh Vahdati and Charles Leslie, IntechOpen. https://doi.org/10.5772/55043

  • Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hortic 103:93–99

    CAS  Google Scholar 

  • Savvides A, Ali S, Tester M, Fotopoulos V (2016) Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci 21:329–340

    CAS  PubMed  Google Scholar 

  • Sayyad-Amin P, Jahansooz M-R, Borzouei A, Ajili F (2016) Changes in photosynthetic pigments and chlorophyll-a fluorescence attributes of sweet-forage and grain sorghum cultivars under salt stress. J Biol Phys 42:601–620

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109:6241–6246

    CAS  PubMed  Google Scholar 

  • Sharma R (2015) Genotypic response to salt stress: I-Relative tolerance of certain wheat cultivars to salinity. Adv Crop Sci Technol. 3:192. https://doi.org/10.4172/2329-8863.1000192

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26

    Google Scholar 

  • Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    CAS  PubMed  Google Scholar 

  • Thalmann M, Santelia D (2017) Starch as a determinant of plant fitness under abiotic stress. New Phytol 214:943–951

    CAS  PubMed  Google Scholar 

  • Torabi M (2014) Physiological and biochemical responses of plants to salt stress. Paper presented at: The 1 st International Conference on New Ideas in Agriculture

  • Vardharajula S, Skz A, Shiva KP, Vurukonda S, Shrivastava M (2017) Plant growth promoting endophytes and their interaction with plants to alleviate abiotic stress. Curr Biotechnol 6:252–263

    Google Scholar 

  • Vicas S, Laslo V, Pantea S, Bandici G (2010) Chlorophyll and carotenoids pigments from Mistletoe (Viscum album) leaves using different solvents. Analele Universitatii din Oradea, Fascicula Biologie 17:213–218

    Google Scholar 

  • Yan J, Aznar A, Chalvin C, Birdseye DS, Baidoo EE et al (2018) Increased drought tolerance in plants engineered for low lignin and low xylan content. Biotechnol Biofuels 11:195

    PubMed  PubMed Central  Google Scholar 

  • Yasmeen R, Siddiqui ZS (2017) Physiological responses of crop plants against Trichoderma harzianum in saline environment. Acta Botanica Croatica 76:154–162

    CAS  Google Scholar 

  • Yesilyurt AM, Pehlivan N, Durmus N, Karaoglu SA (2018) Trichoderma citrinoviride: a potent biopriming agent for the alleviation of salt stress in maize. Hacettepe J Biol Chem 46:101–111

    Google Scholar 

  • Zhang S, Gan Y, Xu B (2016) Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01405

    Article  PubMed  PubMed Central  Google Scholar 

  • Zorrig W, Attia H, Msilini N, Ouhibi C, Lachaâl M et al (2013) Photosynthetic behaviour of Arabidopsis thaliana (Pa-1 accession) under salt stress. Afr J Biotechnol 12:4594–4602

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Botany and Microbiology Department, Faculty of Science, Zagazig University, Zagazig, 44519, Egypt

    Hanan El-Sayed Dief, El-Sayed A. Hashem, Salwa Fawzan & Ashraf S. A. El-Sayed

Authors
  1. Hanan El-Sayed Dief
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. El-Sayed A. Hashem
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Salwa Fawzan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ashraf S. A. El-Sayed
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ashraf S. A. El-Sayed.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dief, H.ES., Hashem, ES.A., Fawzan, S. et al. Alleviation of salt stress in Triticum aestivum by biopriming with Phanerochaete chrysosporium. J. Crop Sci. Biotechnol. 24, 103–116 (2021). https://doi.org/10.1007/s12892-020-00064-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12892-020-00064-3

Keywords

Search

Navigation