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Isolation of Endophytic Fungi from Halophytic Plants and their Identification and Screening for Auxin Production and Other Plant Growth Promoting Traits

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Abstract

Naturally, all plants harbor a diversity of endophytes and can produce a variety of compounds which positively affect the growth of their host plant. Endophytes can contribute in providing plant supplements, conflicting with pathogens, or directly influencing the growth and development of plants through synthesis of phytohormones. The present study aimed to explore the diversity of endophytic fungi from different parts of the three healthy halophytic plants i.e., Solanum surattense Burm. f., Chenopodium album L. and Zizyphus nummularia (Burm. f). As sa result, twenty-two endophytic fungi mostly belonging to ascomycetes were isolated from 92 samples with an overall colonization frequency of 23.02%. The endophytic fungi showed a relatively high percentage of colonization frequency (25%) in roots as compared to other parts. The isolated fungal strains were tested for salt tolerance and for their ability to produce plant hormone indole-3-acetic acid (IAA). Out of 12 different strains, five strains have salt tolerance potential and eight strains have shown to produce IAA in culture media. Further the isolated strains were also screened for their growth promoting activities such as 1-aminocyclopropane1-carboxylate deaminase, flavonoids, phenol, solubilize phosphate and to produce siderophores.

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Data Availability

All the datasets generated or analyzed during the present study are included in this manuscript.

Abbreviations

CF:

Culture filtrate

DDW:

Double distilled water

GPA:

Glucose peptone assay

HPLC:

High performance liquid chromatography

IAA:

Indole acetic acid

PDA:

Potato-dextrose agar

References

  • Ahmad M (1973) Reconnaissance soil survey Bannu Basin. Directorate Soil Survey of Pakistan, Lahore

    Google Scholar 

  • Ahmad N, Hamayun M, Khan SA, Khan AL, Lee IJ, Shin DH (2010) Gibberellin-producing endophytic fungi isolated from Monochoria vaginalis. J Microbiol Biotechnol 20:1744–1749

    CAS  PubMed  Google Scholar 

  • Akbari GA, Arab SM, Alikhani HA, Allahdadi I, Arzanesh MH (2007) Isolation and election of indigenous Azospirillum spp. and the IAA of superior strains effects on wheat roots. World J Agric Sci 3:523–529

    Google Scholar 

  • Ali S, Khan SA, Hamayun M, Iqbal A, Khan AL, Hussain A (2019) Endophytic fungi from Caralluma acutangula can secrete plant growth promoting enzymes. Fresenius Environ Bull 28:2688–2696

    CAS  Google Scholar 

  • Alvin A, Miller KI, Neilan BA (2014) Exploring the potential of endophytes from medicinal plants as sources of anti myco bacterial compounds. Microbiol Res 169:483–495

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ansari AH (1974) Reconnaissance soil survey Kohat Area. Directorate Soil Survey of Pakistan, Lahore

    Google Scholar 

  • Arnold AE (2007) Understanding the diversity of foliar fungal endophytes: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66

    Google Scholar 

  • Barrera A, Hereme R, Ruiz-Lara S, Larrondo LF, Gundel PE, Pollmann S, Molina-Montenegro MA, Ramos P (2020) Fungal endophytes enhance the photoprotective mechanisms and photochemical efficiency in the Antarctic Colobanthus quitensis (Kunth) Bartl. Exposed to UV-B radiation. Front Ecol Evol 8:122

    Google Scholar 

  • Bhardwaj A, Sharma D, Jadon N, Agrawal P (2015) Antimicrobial and phytochemical screening of endophytic fungi isolated from spikes of Pinus roxburghii. Arch Clin Microbiol 6:1–9

    Google Scholar 

  • Bibi S, Hussain A, Hamayun M, Rahman H, Iqbal A, Shah M (2018) Bioremediation of hexavalent chromium by endophytic fungi; safe and improved production of Lactuca sativa L. Chemosphere 211:653–663

    CAS  PubMed  Google Scholar 

  • Bilal L, Asaf S, Hamayun M, Gul H, Iqbal A, Ullah I (2018) Plant growth promoting endophytic fungi Asprgillus fumigatus TS1 and Fusarium proliferatum BRL1 produce gibberellins and regulates plant endogenous hormones. Symbiosis 76:117–127

    CAS  Google Scholar 

  • Bilal S, Shahzad R, Imrana M, Jan R, Kim KM, Lee IJ (2020) Synergistic association of endophytic fungi enhances Glycine max L. resilience to combined abiotic stresses: heavy metals, high temperature and drought stress. Ind Crop Prod 143:111931

    CAS  Google Scholar 

  • Bononi L, Chiaramonte JB, Pansa CC, Moitinho MA, Melo IS (2020) Phosphorus-solubilizing Trichoderma spp. from Amazon soils improve soybean plant growth. Sci Rep 10:1–13

    Google Scholar 

  • Bouyoucos GJ (1936) Directions for making mechanical analyses of soils by the hydrometer method. Soil Sci 42:225–230

    CAS  Google Scholar 

  • Chang C, Yang M, Wen H, Chern J (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10:178–182

    CAS  Google Scholar 

  • Das SK, Varma A (2010) Role of enzymes in maintaining soil health. In: Soil enzymology. Springer, Berlin, Heidelberg, pp 25–42

  • Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106

    CAS  PubMed  Google Scholar 

  • Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis shypogaea L.) by application of plant growth promoting rhizobacteria. Microbiol Res 159:371–394

    CAS  PubMed  Google Scholar 

  • Du CX, Fan HF, Guo SR, Tezuka T, Juan L (2010) Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochem 71:1450–1459

    CAS  Google Scholar 

  • El-hawary SS, Moawad AS, Bahr HS, Abdelmohsen UR (2020) Natural product diversity from the endophytic fungi of the genus aspergillus. RSC Adv 10:22058–22079

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flegel TW (1980) Semipermanent microscope slides of micro fungi using sticky tape technique. Can J Microbio 26:551–553

    CAS  Google Scholar 

  • Floch G, Rey P, Benizri E, Benhamou N, Tirilly Y (2003) Impact of auxin-compounds produced by the antagonistic fungus Pythium oligandrum or the minor pathogen Pythium group F on plant growth. Plant Soil 257:459–470

    Google Scholar 

  • Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612

    Google Scholar 

  • Glickman E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for inolic compounds produced by phytopatogenic bacteria. Appl Envi Microbio 61:793–796

    Google Scholar 

  • Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997a) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914

    CAS  Google Scholar 

  • Hallmann J, Kloepper JW, Rodriguez-Kibana R (1997b) Application of the Scholander pressure bomb to studies on endophytic bacteria of plants. Can J Microbiol 43:411–416

    CAS  Google Scholar 

  • Hasan HA (2002) Gibberellin and auxin production by plant root-fungi and their biosynthesis under salinity-calcium interaction. Rost Yroba 3:101–106

    Google Scholar 

  • Heald WR (1965) Methods of soil and plant analysis: With special reference to strontium 90 contamination. Agricultural Research Service: US Department of Agriculture

  • Hereme R, Morales-Navarro S, Ballesteros G, Barrera A, Ramos P, Gundel PE, Molina-Montenegro MA (2020) Fungal endophytes exert positive effects on Colobanthus quitensis under water stress but neutral under a projected climate change scenario in Antarctica. Front Microbiol 11:264

    PubMed  PubMed Central  Google Scholar 

  • Hill TW, Kafer E (2001) Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solutions. Fungal Genet Rep 48:20–21

    Google Scholar 

  • Hyde KD, Soytong K (2007) Understanding microfungal diversity—a critique. Cryptogam Mycol 1:4–281

    Google Scholar 

  • Ikram M, Ali N, Jan G, Jan FG, Khan N (2020) Endophytic fungal diversity and their interaction with plants for agriculture sustainability under stressful condition. Recent Pat Food Nutr Agric 11(2):115–123

    PubMed  Google Scholar 

  • Imran A, Arif M, Shah Z, Bari A (2020) Soil application of Trichoderma and Peach (Prunus persica L.) residues possesses biocontrol potential for weeds and enhances growth and profitability of soybean (Glycine max). Sarhad J Agric 36:10–20

    Google Scholar 

  • Ismail MH, Hussain A, Iqbal A, Khan SA, Lee IJ (2018) Endophytic fungus Aspergillus japonicus mediates host plant growth under normal and heat stress conditions. BioMed Res Int 2:1–11

    Google Scholar 

  • Ismail MH, Hussain A, Iqbal A, Khan SA, Khan MA (2021) An endophytic fungus Gliocladium cibotii regulates metabolic and antioxidant system of Glycine max and Helianthus annuus under heat stress. Polish J Environ Stud 30:1–10

    Google Scholar 

  • Jamal A, Jamal H (2018) Assessment and distribution of macro and micro nutrients in different soil series of District Swabi, Khyber Pakhtunkhwa, Pakistan. J Horticul Plant Res 2:23–32

    Google Scholar 

  • Jan FG, Hamayun M, Hussain A, Jan G, Iqbal A, Khan A (2019) An endophytic isolate of the fungus Yarrowia lipolytica produces metabolites that ameliorate the negative impact of salt stress on the physiology of maize. BMC Microbiol 19:3

    PubMed  PubMed Central  Google Scholar 

  • Jeon JS, Lee SS, Kim HY, Ahn TS, Song HG (2003) Plant growth promotion in soil by some inoculated microorganisms. J Microbiol 41:271–276

    CAS  Google Scholar 

  • Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Medet Biol 18:355–364

    CAS  Google Scholar 

  • Khan S, Ahmad I, Shah MT, Rehman SS, Khaliq A (2009) Use of constructed wetland for the removal of heavy metals from industrial wastewater. J Environ Manag 90:3451–3457

    CAS  Google Scholar 

  • Khan MA, Alamgir A, Khan A, Shaukat SS, Kazmi SJ, Qureshi S (2015) Appraisal of climate change impacts on the coastal areas of sindh using remote sensing techniques. Environ Sci 15:1102–1112

    Google Scholar 

  • Khan MI, Ali N, Jan G, Hamayun M, Jan FG, Iqbal A, Hussain A, Lee I-J (2022) Salt stress alleviation in Triticum aestivum through primary and secondary metabolites modulation by Aspergillus terreus BTK-1. Front Plant Sci 13:779623

    PubMed  PubMed Central  Google Scholar 

  • Kpomblekou AK, Tabatabai MA (2003) Effect of low-molecular weight organic acids on phosphorus release and phyto availability of phosphorus in phosphate rocks added to soils. Agric Eco Environ 100:275–284

    Google Scholar 

  • Kumar A, Choudhary CS, Paswan D, Kumar B (2004) Sustainable way for enhancing phosphorus efficiency in agricultural soils through phosphate solubilizing microbes. Asian J Soil Sci 9:300–310

    Google Scholar 

  • Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Divers 17:69–90

    CAS  Google Scholar 

  • Kumar A, Maurya BR, Raghuwanshi R (2014) Isolation and characterization of PGPR and their effect on growth, yield and nutrient content in wheat (Triticum aestivum L.). Biocatal Agri Biotechnol 3:121–128

    Google Scholar 

  • Kumar K, Manigundan K, Amaresan N (2017) Influence of salt tolerant Trichoderma spp. on growth of maize (Zea mays) under different salinity conditions. J Basic Microbiol 57:141–150

    CAS  PubMed  Google Scholar 

  • Malik CP, Singh MB (1980) Plant enzymology and histo-enzymology: a text manual. Kalyani Publications, New Delhi, Ludhiana, p 434

    Google Scholar 

  • Marques APGC, Pires C, Moreira H, Rangel AOSS, Castro PML (2010) Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol Biochem 42:1229–1235

    CAS  Google Scholar 

  • Mehmood A, Hussain A, Irshad M, Hamayun M, Iqbal A, Khan N (2019a) In vitro production of IAA by endophytic fungus Aspergillus awamori and its growth promoting activities in Zea mays. Symbiosis 77:225–235

    CAS  Google Scholar 

  • Mehmood A, Hussain A, Irshad M, Hamayun M, Iqbal A, Rahman H (2019b) Cinnamic acid as an inhibitor of growth, flavonoids exudation and endophytic fungus colonization in maize root. Plant Physiol Biochem 135:61–68

    CAS  PubMed  Google Scholar 

  • Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proc Nat Acad Sci 105:19780–19785

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morales-Quintana L, Barrera A, Hereme R, Jara K, Rivera-Mora C, Valenzuela-Riffo F, Gundel PE, Pollmann S, Molina-Montenegro MA, Ramos P (2021) Molecular and structural characterization of expansins modulated by fungal endophytes in the Antarctic Colobanthus quitensis (Kunth) Bartl. Exposed to drought stress. Plant Physiol Biochem 168:465–476

    CAS  PubMed  Google Scholar 

  • Mordue JEM (1971) Colletotrichum capsici. Descriptions of fungi and bacteria. In: IMI descriptions of fungi and bacteria, pp 32–33

  • Muhammad I, Ali N, Jan G, Jan FG, Rahman IU, Iqbal A (2018) IAA producing fungal endophyte Penicillium roqueforti Thom., enhances stress tolerance and nutrients uptake in wheat plants grown on heavy metal contaminated soils. PLoS ONE 13:e0208150

    Google Scholar 

  • Muhammad I, Niaz A, Gul J, Amjad I, Muhammad H, Farzana GJ (2019) Trichoderma reesei improved the nutrition status of wheat crop under salt stress. J Plant Interact 14:590–602

    Google Scholar 

  • Nagamani A, Kunwar IK, Manoharachary C (2006) Handbook of soil fungi. I.K. International Private limited, New Delhi, pp 1–496

    Google Scholar 

  • Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270

    CAS  PubMed  Google Scholar 

  • Omomowo OI, Babalola O (2019) Bacterial and fungal endophytes: tiny giants with immense beneficial potential for plant growth and sustainable agricultural productivity. Microorganisms 4:7–481

    Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC Deaminase containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    CAS  PubMed  Google Scholar 

  • Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, Berlin, Heidelberg, New York, pp 179–197

    Google Scholar 

  • Petten C, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Envi Microbiol 68:3795–3801

    Google Scholar 

  • Pirttilä AM, Pospiech H, Laukkanen H, Myllylä R, Hoh-tola A (2003) Two endophytic fungi in different tissues of Scots pine buds (Pinus sylvestris L.). Microb Ecol 45:53–62

    PubMed  Google Scholar 

  • Qadir M, Hussain A, Hamayun M, Shah M, Iqbal A, Murad W (2020) Phytohormones producing rhizobacterium alleviates chromium toxicity in Helianthus annuus L. by reducing chromate uptake and strengthening antioxidant system. Chemosphere 258:127386

    CAS  PubMed  Google Scholar 

  • Raid A, Humaira G, Muhammad H, Mamoona R, Amjad I, Mohib S (2021) Aspergillus awamori ameliorates the physicochemical characteristics and mineral profile of mung bean under salt stress. Chem Biol Technol Agric 8:1–13

    Google Scholar 

  • Saad EH (2017) Plant growth-promoting activities for bacterial and fungal endophytes isolated from medicinal plant of Teucrium polium L. J Advan Res 8:667–695

    Google Scholar 

  • Santos IPD, Silva LCND, Silva MVD, Araújo JMD, Cavalcanti MDS, Lima VLDM (2015) Antibacterial activity of endophytic fungi from leaves of Indigofera suffruticosa Miller (Fabaceae). Front Microbiol 6:350

    PubMed  PubMed Central  Google Scholar 

  • Schwyn B, Neilands JB (1997) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Google Scholar 

  • Strobel G, Daisy B (2003) Bio prospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19(1):1–30

    Google Scholar 

  • Sudha MR, Gowri S, Prabhavathi P, Astapriya P, Devi YS, Saranya A (2012) Production and optimization of indole acetic acid by indigenous micro flora using agro waste as substrate. Pak J Biol Sci 15:39–43

    CAS  PubMed  Google Scholar 

  • Sullivan TS, Ramkissoon S, Garrison VH, Ramsubhag A, Thies JE (2012) Siderophore production of African dust microorganisms over Trinidad and Tobago. Aerobiol 28:391–401

    Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Klimova YS, Shestakov AI, Botina SG, Netrusov AI (2007) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 6:655–664

    Google Scholar 

  • Wahyudi AT, Astuti RP, Widyawati A, Meryandini AA, Nawangsih AA (2011) Characterization of Bacillus sp. strains isolated from rhizosphere of soybean plants for their use as potential plant growth for promoting Rhizobacteria. J Microbiol Antim 3:34–40

    Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    CAS  PubMed  Google Scholar 

  • Yadav M, Yadav A, Yadav JP (2014) Vitro antioxidant activity and total phenolic content of endophytic fungi isolated from Eugenia jambolana. Asian Pac J Trop Med 7:256–261

    Google Scholar 

  • Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23:753–771

    CAS  PubMed  Google Scholar 

  • Zhang J, Liu J, Meng L, Ma Z, Tang X, Cao Y (2012) Isolation and characterization of plant growth promoting rhizobacteria from wheat roots by wheat germ agglutinin labeled with fluoresce in isothiocyanate. J Microbiol 50:191–198

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are thankful to the Department of Botany, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan, for providing the research assistance.

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This research work received no external funding.

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Authors and Affiliations

  1. Department of Botany, Hazara University, Mansehra, Pakistan

    Muhammad Ikram, Niaz Ali & Rimsha Zainab

  2. Department of Botany, Abdul Wali Khan University, Mardan, Pakistan

    Gul Jan & Farzana Gul Jan

  3. Department of Botany, Government Girls Degree College Dargai, District Malakand, Khyber Pakhtunkhwa, Pakistan

    Rainaz Pervez

  4. Department of Botany, University of Chitral, Chitral, Pakistan

    Muhammad Romman

  5. Department of Bio-Sciences, COMSATS University, Islamabad, 45550, Pakistan

    Humaira Yasmin

  6. Department of Agronomy, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, USA

    Naeem Khan

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  1. Muhammad Ikram
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Contributions

MI: Methodology, Software, Data curation, Writing—Original draft preparation. NA: Supervision, Conceptualization, Visualization. GJ: Supervision, Methodology, Validation. FGJ: Data curation, helped in discussion. RP: Methodology, Software. MR: Editing, Visualization. RZ: Editing, Data curation. HY: manuscript editing and discussion. NK: Resources, Conceptualization, manuscript editing.

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Correspondence to Niaz Ali or Naeem Khan.

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Ikram, M., Ali, N., Jan, G. et al. Isolation of Endophytic Fungi from Halophytic Plants and their Identification and Screening for Auxin Production and Other Plant Growth Promoting Traits. J Plant Growth Regul 42, 4707–4723 (2023). https://doi.org/10.1007/s00344-022-10685-3

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